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Neurosurgery Books Full


Neurosurgery Books Full
Neurosurgery Books Full
Neurovascular Surgery
2nd Edition

Rob er t F. Sp et zler, MD
Division of Neu rological Su rger y
Barrow Neu rological In st it u te
St . Joseph’s Hospit al an d Medical Cen ter
Ph oen ix, Arizon a

M. Yash ar S. Kalan i, MD, Ph D


Division of Neu rological Su rger y
Barrow Neu rological In st it u te
St . Joseph’s Hospit al an d Medical Cen ter
Ph oen ix, Arizon a

Peter Nakaji, MD
Division of Neu rological Su rger y
Barrow Neu rological In st it u te
St . Joseph’s Hospit al an d Medical Cen ter
Ph oen ix, Arizon a

With 1904 Figu res

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New York • St ut tgar t • Delh i • Rio de Jan eiro

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Execu t ive Editor: Tim Hiscock Im p ort an t n ote: Medicin e is an ever-ch anging scien ce u n dergoing con -
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Neurosurgery Books Full


To th e m any p at ien t s w h o h ave taugh t m e so m u ch . To th e m em or y of a good frien d an d colleague, Ph il Car ter.
Robert F. Spetzler, MD

To m y paren t s, Afrou z an d Moh am m ad, for teach ing m e th e value of edu cat ion , to Maziyar for h is frien dsh ip,
an d to Krist in for su pp or t ing m e th rough out m y jou rn ey.
M. Yashar S. Kalani, MD, PhD

To m y w ife, Nicole, an d m y ch ildren , Nath an , Caden , an d Madelin e, w ith ou t w h om I am n oth ing.


Peter Nak aji, MD

Neurosurgery Books Full


Neurosurgery Books Full
Contents

Video Co n ten ts xiii


Preface xix
Acknow ledgm ents xxi
Co n tributo rs xxiii

Sectio n I Develo pm en t, Anato m y, and Physio logy o f the Central Nervo us System
1 Developm en t of th e Cerebrovascu lat u re . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Zam an Mirzadeh and Robert F. Spetzler

2 Microsu rgical An atom y of th e In tern al Carot id an d Ver tebral Ar teries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .12


Maria Peris-Celda, Alvaro Cam pero, Pablo Rubino, and Albert L. Rhoton, Jr.

3 Cran ial Vascu lar An atom y of th e An terior Circu lat ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .37
João Paulo C. de Alm eida, Feres Chaddad, Albert L. Rhoton, Jr., and Evandro de Oliveira

4 Cran ial Vascu lar An atom y of th e Posterior Circu lat ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .49
Michaël Bruneau and Henri-Benjam in Pouleau

5 Cran ial Ven ous An atom y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .71


Mauro A.T. Ferreira

6 Spin al Vascu lar An atom y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .89


Peter Kim Nelson and Mak sim Shapiro

7 Cerebrovascu lar Physiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .105


Jens Bjerregaard and Richard A. Jaffe

Sectio n II Evaluatio n and Treatm ent Co nsideratio n s fo r Neurovascular Disease


8 Neurovascular Histor y an d Exam in at ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .119
M. Yashar S. Kalani, Luis Pérez-Orribo, Gaurav Bhardw aj, Ian C. Francis, and Joseph M. Zabram sk i

9 In t raop erat ive Evalu at ion of Blood Flow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .131


Sepideh Am in-Hanjani and Fady T. Charbel

10 Neuroan esth esia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .142


Alana M. Flexm an and Pekk a O. Talke

11 Neurom on itoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .150


Christ ian Musahl, Claudia W eissbach, and Nikolai J. Hopf

12 Cerebral Protect ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .167


Douglas J. Cook , Jacob Fairhall, Crist ian Valdes, and Michael Tym iansk i

13 Prin ciples an d Tech n iques of Hypoth erm ia an d Cardiac Arrest for Neu rovascu lar An om alies . . . . . . . . . . . .175
Javier Lorenzo and Richard A. Jaffe

14 Invasive an d Non invasive Im aging of th e Vascu lat u re . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .182


Joseph E. Heiserm an

15 Ap plicat ion s of In docyan in e Green Video Angiograp hy in Neu rovascu lar Su rger y . . . . . . . . . . . . . . . . . . . . . .194
Jack y T. Yeung, M. Yashar S. Kalani, and Peter Nak aji

vii

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viii Contents

Sectio n III Ischem ic Stro ke an d Vascular Insufficiency


16 Th e Path op hysiology of Cerebral Isch em ia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .203
Andrew M. Bauer and Robert J. Dem psey

17 Medical Man agem en t of Cardiogen ic Cerebral Em bolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .216


Yazan J. Alderazi and Sean I. Savitz

18 Diagn osis of Brain In farct ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .230


Moham ed Teleb, Paul Singh, and Maarten Lansberg

19 Carot id Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .243


Nohra Chalouhi, Rohan Chitale, Pascal M. Jabbour, Stavropoula I. Tjoum akaris,
Aaron S. Dum ont, Robert Rosenw asser, and L. Fernando Gonzalez

20 Carot id En dar terectom y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .252


Mark us Bookland and Christopher M. Loft us

21 En dovascular Treat m en t of Carot id Sten osis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .262


Travis M. Dum ont, Kenneth V. Snyder, Adnan H. Siddiqui, L. Nelson Hopk ins, and Elad I. Levy

22 Medical Man agem en t of Vertebrobasilar Occlu sive Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .278


Matthew R. Reynolds, Gyanendra Kum ar, Jin-Moo Lee, and Gregory J. Zipfel

23 Surgical Treat m en t of Ver tebrobasilar In su fficien cy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .290


Moham ed Sam y Elham m ady and Jacques J. Morcos

24 En dovascular Treat m en t of Vertebrobasilar In sufficien cy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .320


Ram sey Ashour and Moham m ad Ali Aziz-Sultan

25 Medical Man agem en t of In t racran ial Ath ero- Occlu sive Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .330
Shakeel A. Chow dhry and Peter Nak aji

26 Medical Man agem en t an d Th rom bolyt ic Th erapy for Acu te Isch em ic St roke . . . . . . . . . . . . . . . . . . . . . . . . . . .337
W . David Freem an and Thom as G. Brot t

27 Curren t En dovascu lar Treat m en t of Acu te Isch em ic St roke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .351


Philipp Taussk y, Rabih G. Taw k , David A. Miller, and Ricardo A. Hanel

28 Path ophysiology an d Su rgical Man agem en t of In t racerebral Hem atom as . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .360


A. David Mendelow

29 Medical an d En dovascu lar Treat m en t of Cerebral Sin u s an d Ven ou s Th rom bosis . . . . . . . . . . . . . . . . . . . . . . .369
Nohra Chalouhi, Stavropoula I. Tjoum akaris, L. Fernando Gonzalez,
Aaron S. Dum ont, Robert Rosenw asser, and Pascal M. Jabbour

30 Spin al Cord In farct ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .377


Michael J. W ang, W illiam P. Cheshire, and Jam es F. How ard, Jr.

31 Medical, Su rgical, an d En dovascu lar Treat m en t of Clau dicat ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .385


Chelsea A. Dorsey and Jason T. Lee

32 Medical, Su rgical, an d En dovascu lar Treat m en t of Ar terial Inju r y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .391


Benjam in D. Fox and Adam S. Arthur

33 Pit u it ar y Ap op lexy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .400


Ram i O. Alm eft y, Andrew S. Little, Shih Sing Liu, and W illiam L. W hite

Sectio n IV Cerebral and Spin al Caverno us Malfo rm atio ns


34 Cavern ous Malform at ion s: Nat u ral Histor y, Ep idem iology, Presen tat ion , an d Treat m en t Opt ion s . . . . . . . .413
Hasan A. Zaidi and Joseph M. Zabram ski

35 Surgical Man agem en t of Su praten torial Cavern ous Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .419
Helm ut Bertalanffy, Venelin Gerganov, and Vincen zo Paterno

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Contents ix

36 Surger y for Brain stem Cavern ous Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .436


Adib A. Abla, M. Yashar S. Kalani, and Robert F. Spetzler

37 Microsu rger y of In t ram edu llar y Spin al Cavern ou s Malform at ion s. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .448
M. Yashar S. Kalani, Maziyar A. Kalani, and Robert F. Spetzler

Sectio n V Cerebral and Spinal Aneurysm s


38 In t racran ial An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .457
Mart in Lehecka, Juhana Frösen, Miikka Korja, Hanna Lehto, Rik u Kivisaari,
Rossana Rom ani, Mik a Niem elä, and Juha Hernesniem i

39 Subarach n oid Hem orrh age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .468


Giuseppe Lanzino and Alejandro A. Rabinstein

40 Cerebral Vasospasm an d Delayed Isch em ic Com p licat ion s Associated


w ith Subarach n oid Hem orrh age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .478
Guarav Gupta and E. Sander Connolly

41 Medical Man agem en t of Su barach n oid Hem orrh age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .484


Shaw n Eugene W right

42 En dovascular Man agem en t of Subarach n oid Hem orrh age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .493


Nohra Chalouhi, Pascal M. Jabbour, Aaron S. Dum ont, L. Fernando Gonzalez,
Robert Rosenw asser, and Stavropoula I. Tjoum akaris

43 Surgical Th erapies for Saccular An eu r ysm s of th e In tern al Carot id Ar ter y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .505


Leonardo Rangel-Cast illa and Robert F. Spetzler

44 En dovascular Th erapies for An eur ysm s of th e In tern al Carot id Arter y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .516


Tarek Y. El Ahm adieh, Najib E. El Tecle, Salah G. Aoun, Allan Douglas Nanney III,
Joseph G. Adel, and Bernard R. Bendok

45 Man agem en t St rategies for In t racavern ou s An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .529


Babu G. W elch, Christopher S. Eddlem an, Aw ais Z. Vance, and Duke S. Sam son

46 Surgical Th erapies for Carot id- Oph th alm ic An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .538
Arthur L. Day, Yoshua Esquenazi, and Buelent Yapicilar

47 En dovascular Treat m en t of Carot id- Oph th alm ic An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .547


Rosa Mart inez, Marta Aguilar Perez, Nikolai J. Hopf, Hansjörg Bäzner, and Hans Henkes

48 Surgical Th erapies for Middle Cerebral Ar ter y An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .556


Hani Malone and Robert Solom on

49 En dovascular Th erapies for Middle Cerebral Arter y An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .569


Jorge L. Eller, Travis M. Dum ont, Grant C. Sork in, Maxim Mok in, Kenneth V. Snyder,
L. Nelson Hopkins, Adnan H. Siddiqui, and Elad I. Levy

50 Surgical Th erapies for An terior Com m un icat ing Ar ter y An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .584
Salah G. Aoun, Bernard R. Bendok , Tarek Y. El Ahm adieh, Najib E. El Tecle, and H. Hunt Batjer

51 En dovascular Th erapies for An terior Com m un icat ing Arter y An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .595
Douglas L. Stofko, Zak aria Hak m a, and Erol Veznedaroglu

52 Surgical Th erapies for Dist al An terior Cerebral Ar ter y An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .605
Clem ens M. Schirm er and Carlos A. David

53 Com preh en sive Man agem en t of Dist al An terior Cerebral Arter y An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . .613
Daniel W . Zum ofen, Donato Pacione, Peter Kim Nelson, and How ard A. Riina

54 Surgical Th erapies for Basilar Ar ter y An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .623


Ali F. Krisht

55 En dovascular Th erapies for Basilar Arter y An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .635


Robert W .J. Ryan, Abhineet Chow dhary, and Michael J. Alexander

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56 Surgical Th erapies for Ver tebral Ar ter y an d Posterior In ferior Cerebellar Ar ter y An eur ysm s . . . . . . . . . . . . .647
Ana Rodríguez-Hernández, Matthew B. Potts, and Michael T. Law ton

57 Microsu rgical Man agem en t of An eu r ysm s of th e Posterior Cerebral, Su perior Cerebellar,


an d An terior In ferior Cerebellar Ar teries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .661
Jonathan J. Russin and Robert F. Spetzler

58 En dovascular Treat m en t of Vertebrobasilar Circulat ion An eur ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .679


Daniel W . Zum ofen, Eytan Raz, Mak sim Shapiro, Tibor Becske, Peter Kim Nelson, and How ard A. Riina

59 In fect iou s In t racran ial An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .689


Jonathan J. Russin, W illiam J. Mack , and Steven L. Giannotta

60 Trau m at ic an d Dissect ing In t racran ial An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .698


Giuseppe Lanzino and Fredric B. Meyer

61 Gian t An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .710


M. Yashar S. Kalani and Robert F. Spetzler

62 In ciden t al An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .748


Issam A. Aw ad, Mahua Dey, Jam es Brorson, and Seon-Kyu Lee

63 Flow -Diver t ing Sten t s in th e Man agem en t of Com plex An eu r ysm s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .761
David Fiorella

64 An eu r ysm s of Sp in al Arteries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .772


Sam uel Kalb, Luis Pérez-Orribo, Mark E. Oppenlander, M. Yashar S. Kalani, and Robert F. Spetzler

65 Cerebral An eu r ysm s: To Clip or Coil? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .778


Brian P. W alcott and Christopher S. Ogilvy

Sectio n VI Cerebral and Spinal Arterioveno us Fistulas and Malfo rm atio ns


66 Cerebral Ar terioven ou s Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .787
Moham ed Sam y Elham m ady, Seth Hayes, and Roberto C. Heros

67 Vascular Malform at ion s an d Epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .819


Matthias Sim on, Christ ian von der Brelie, and Johannes Schram m

68 Cran ial Dural Ar terioven ous Fist u las . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .833


Mark J. Dannenbaum , Albert J. Schuette, Daniel B. Case, C. Michael Caw ley, and Daniel L. Barrow

69 En dovascular Treat m en t of Cerebral Arterioven ou s Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .843


R. W ebster Crow ley, Andrew F. Ducruet, Cam eron G. McDougall, and Felipe C. Albuquerque

70 Supraten torial Ar terioven ous Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .853


Aki Laak so, Mart in Lehecka, Ahm ed Elsharkaw y, and Juha Hernesniem i

71 Posterior Fossa Ar terioven ou s Malform at ion s an d Du ral Ar terioven ou s Fist u las . . . . . . . . . . . . . . . . . . . . . . . .866
Joao Paulo C. de Alm eida, Alexander L. Coon, Judy Huang, and Rafael J. Tam argo

72 Gian t Ar terioven ous Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .877


Aki Laak so, Mart in Lehecka, Ahm ed Elsharkaw y, and Juha Hernesniem i

73 Microsu rgical Treat m en t of Vein of Galen Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .886


Daniel D. Cavalcant i, M. Yashar S. Kalani, and Robert F. Spetzler

74 En dovascular Treat m en t of Vein of Galen Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .900


Jason A. Ellis, Hannah Goldstein, Randall T. Higashida, and Philip M. Meyers

75 Presen t at ion , Clin ical Feat ures, an d Nat ural Histor y of Carot id-Cavern ous Sin us Fist ulas . . . . . . . . . . . . . . . .908
Nikolai J. Hopf, Christ ian Musahl, Marta Aguilar Perez, Hansjörg Bäzner, and Hans Henkes

76 En dovascular Treat m en t for Carot id-Cavern ous Sin us Fist ulas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .918
Jeffrey C. Mai and Brian L. Hoh

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77 En dovascular Man agem en t of In t racran ial Fist u las . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .928


George A.C. Mendes, Paulo Puglia, Jr., Michel Eli Frudit, and José Guilherm e Mendes Pereira Caldas

78 Stereot act ic Radiosu rger y for Cran ial Vascu lar Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .949
Hideyuk i Kano, Douglas Kondziolk a, L. Dade Lunsford, and John C. Flick inger

79 Radiosurger y for Spin al Ar terioven ou s Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .955


Maziyar A. Kalani, Syed Aftab Karim , Scott G. Solt ys, and Steven D. Chang

80 Surgical Man agem en t of Spin al Vascu lar Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .964


Maziyar A. Kalani, M. Yashar S. Kalani, and Robert F. Spetzler

81 En dovascular Treat m en t of Spin al Arterioven ous Malform at ion s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .984


Andrew F. Ducruet, R. W ebster Crow ley, Cam eron G. McDougall, and Felipe C. Albuquerque

Sectio n VII Diso rders o f Ephaptic Transm issio n


82 Trigem in al an d Glossop h ar yngeal Neu ralgia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .999
Peter J. Jannet ta

83 Microvascu lar Decom pression for Trigem in al Neu ralgia: Op erat ive Resu lt s in 2,488 Cases . . . . . . . . . . . . 1007
Tak anori Fuk ushim a and Kentaro W atanabe

84 Surgical Man agem en t of Hem ifacial Spasm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1016


Charles Teo and Brian J. Dlouhy

Sectio n VIII Vascular Co nsideratio ns in the Managem ent o f Tum o rs


85 Em bolizat ion of Vascular Tum ors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1025
Joshua W . Osbun, Michael R. Levit t, Manuel Ferreira, Jr., and Louis J. Kim

86 Microsu rgical Man agem en t of Vascu lar Tu m ors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1037


Fangxiang Chen, Juliet Kim , Vilaas Shett y, and Saleem I. Abdulrauf

87 Microsu rgical Man agem en t of Vascu lar Sp in al Tu m ors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1046


Yury Kushel

Sectio n IX Surgical Appro aches


88 Skull Base Approach es to th e An terior an d Middle Cran ial Fossa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1055
Kaith K. Alm eft y and Ossam a Al-Meft y

89 Surgical Approach es to th e Posterior Fossa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1069


Just in M. Sw eeney, A. Sam y Youssef, and Harry R. van Loveren

90 Ap plicat ion s of En doscopy to Cerebrovascu lar Su rger y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1082


Nancy McLaughlin, Daniel M. Prevedello, Ricardo L. Carrau , and Am in B. Kassam

91 Keyh ole Cran ial Approach es for Cerebrovascu lar Surger y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1097
Peter Nakaji

92 Surgical Exposu re of th e Ver tebral Ar ter y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1111


Bernard George and Michaël Bruneau

Sectio n X Cerebral Revascularizatio n


93 Bypass Surger y for An eu r ysm s an d Tu m ors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1127
Laligam N. Sekhar, Farzana Tariq, Basavaraj Ghodke, and Louis J. Kim

94 Excim er Laser-Assisted Non occlusive An astom osis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1147


Albert van der Zw an, Tristan van Doorm aal, Luca Regli, and Cornelis A.F. Tulleken

95 In t racran ial–Ext racran ial Byp ass Su rger y for Moyam oya Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1156
Peter A. Gooderham and Gary K. Steinberg

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96 In t racran ial–In t racran ial Byp ass Su rger y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1172


Matthew B. Potts, Ana Rodríguez-Hernández, and Michael T. Law ton

97 Surgical Cerebral Revascularizat ion for Isch em ia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1180


Eric S. Nussbaum

98 Posterior Circu lat ion Bypass Su rger y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1186


Yasuhiro Yonekaw a

99 En dovascular Cerebral Revascu larizat ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203


Mahan Ghiassi, Scott L. Zuckerm an, Mayshan Ghiassi, and J Mocco

Index 1215

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Video Contents

Chapter 3 Cranial Vascular Anato m y o f the Anterio r Circulatio n


João Paulo C. de Alm eida, Feres Chaddad, Albert L. Rhoton, Jr., and Evandro de Oliveira
3.1 Circle of Willis An im at ion

Chapter 5 Cranial Veno us Anato m y


Mauro A. T. Ferreira
5.1 Ven ous An atom y An im at ion

Chapter 6 Spinal Vascular Anato m y


Peter Kim Nelson and Mak sim Shapiro
6.1 Sp in al Cord An atom y An im at ion

Chapter 9 In trao perative Evaluatio n o f Blo o d Flow


Sepideh Am in-Hanjani and Fady T. Charbel
9.1 Left MCA An eu r ysm , Un iversit y of Illin ois at Ch icago
9.2 M1 An eur ysm , Un iversit y of Illin ois at Ch icago

Chapter 13 Principles and Techn iques o f Hypotherm ia and Cardiac Arrest fo r


Neurovascular Ano m alies
Javier Lorenzo and Richard A. Jaffe
13.1 An eu r ysm Clipp ing An im at ion using Hypoth erm ia

Chapter 14 Invasive and No ninvasive Im aging o f the Vasculature


Joseph E. Heiserm an
14.1 3D Angiograp hy

Chapter 15 Applicatio ns o f Indo cyanine Green Video Angio graphy in Neurovascular Surgery
Jack y T. Yeung, M. Yashar S. Kalani, and Peter Nak aji
15.1 MCA An eur ysm ICG
15.2 Posterior Fossa AVM ICG
15.3 STA-to-MCA Bypass ICG
15.4 Con u s AVM ICG

Chapter 17 Medical Managem ent o f Cardio genic Cerebral Em bo lism


Yazan J. Alderazi and Sean I. Savitz
17.1 Em bolic St roke An im at ion

Chapter 20 Carotid En darterecto m y


Mark us Bookland and Christopher M. Loft us
20.1 Carot id En dar terectom y
20.2 Carot id En dar terectom y

Chapter 21 Endovascular Treatm ent o f Carotid Steno sis


Travis M. Dum ont, Kenneth V. Snyder, Adnan H. Siddiqui, L. Nelson Hopk ins, and Elad I. Levy
21.1 Carot id Sten t ing, Un iversit y at Buffalo Neurosurger y

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Chapter 23 Surgical Treatm ent o f Vertebro basilar Insufficiency


Moham ed Sam y Elham m ady and Jacques J. Morcos
23.1 VA-to- CCA Tran sp osit ion
23.2 VA-to- CCA Tran sp osit ion

Chapter 35 Surgical Man agem ent o f Supratento rial Caverno us Malfo rm atio ns
Helm ut Bertalanffy, Venelin Gerganov, and Vincenzo Paterno
35.1 Fron t al Cavern ou s Malform at ion
35.2 Orbitozygom at ic Cavern ous Malform at ion
35.3 Parieto- Occip ital In tern al Capsular Cavern ou s Malform at ion

Chapter 36 Surgery fo r Brainstem Caverno us Malfo rm atio ns


Adib A. Abla, M. Yashar S. Kalani, and Robert F. Spetzler
36.1 In terh em isph eric Cavern ous Malform at ion
36.2 Midlin e Cavern ou s Malform at ion
36.3 Ret rosigm oid Pon t in e Cavern ous Malform at ion
36.4 Ret rosigm oid Cavern ou s Malform at ion
36.5 Su pracerebellar In fraten torial Cavern ou s Malform at ion

Chapter 37 Micro surgery o f Intram edullary Spin al Caverno us Malfo rm atio ns


M. Yashar S. Kalani, Maziyar A. Kalani, and Robert F. Spetzler
37.1 Su boccip ital C1 Cavern ou s Malform at ion
37.2 C3 to C4 Cavern ou s Malform at ion
37.3 Gian t Cavern ou s Malform at ion
37.4 T12 to L1 Cavern ous Malform at ion

Chapter 40 Cerebral Vaso spasm and Delayed Ischem ic Co m plicatio ns Asso ciated
w ith Subarachno id Hem o rrhage
Guarav Gupta and E. Sander Connolly
40.1 Vasosp asm An im at ion

Chapter 41 Medical Managem ent o f Subarachno id Hem o rrhage


Shaw n Eugene W right
41.1 Neu rogen ic St un n ed Myocardiu m An im at ion

Chapter 43 Surgical Therapies fo r Saccular Aneurysm s o f the Internal Carotid Artery


Leonardo Rangel-Cast illa and Robert F. Spetzler
43.1 Modified Orbitozygom at ic Ch oroidal An eu r ysm
43.2 Modified Orbitozygom at ic Ch oroidal An eu r ysm
43.3 Modified Orbitozygom at ic ICA An eur ysm
43.4 Modified Orbitozygom at ic ICA an d PCoA An eu r ysm s
43.5 Orbitozygom at ic ICA Blister An eu r ysm

Chapter 45 Managem en t Strategies fo r Intracaverno us Aneurysm s


Babu G. W elch, Christopher S. Eddlem an, Aw ais Z. Vance, and Duke S. Sam son
45.1 Cavern ou s ICA An eu r ysm w ith ICA-to-MCA Bypass
45.2 Cavern ou s ICA An eu r ysm w ith ICA-to-MCA Bypass

Chapter 46 Surgical Therapies fo r Carotid-Ophthalm ic Aneurysm s


Arthur L. Day, Yoshua Esquenazi, and Buelent Yapicilar
46.1 Orbitozygom at ic Op h th alm ic An eu r ysm
46.2 Orbitozygom at ic Bilateral Para Oph th alm ic An eur ysm

Chapter 47 Endovascular Treatm ent o f Carotid-Ophthalm ic Aneurysm s


Rosa Mart inez, Marta Aguilar Perez, Nikolai J. Hopf, Hansjörg Bäzner, and Hans Henkes
47.1 En dovascu lar Oph th alm ic An eur ysm

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Chapter 48 Surgical Therapies fo r Middle Cerebral Artery Aneurysm s


Hani Malone and Robert Solom on
48.1 MCA An eur ysm , Colu m bia Un iversit y
48.2 Min i-Pterion al MCA An eur ysm
48.3 Large Th rom bosed MCA An eu r ysm
48.4 Modified Orbitozygom at ic MCA Fu siform An eu r ysm
48.5 Orbitozygom at ic Bilateral MCA An eur ysm s
48.6 Len t icu lost riate Ar ter y An eur ysm

Chapter 50 Surgical Therapies fo r Anterio r Co m m unicating Artery Aneurysm s


Salah G. Aoun, Bernard R. Bendok , Tarek Y. El Ahm adieh, Najib E. El Tecle, and H. Hunt Batjer
50.1 Previou sly Coiled ACoA An eur ysm , Un iversit y of Texas Sou th w estern Medical Cen ter
50.2 Min i- Orbitozygom at ic Ru pt u red ACoA An eu r ysm
50.3 Mu lt ilobu lated ACoA An eu r ysm at A1–A2 Ju n ct ion

Chapter 52 Surgical Therapies fo r Distal Anterio r Cerebral Artery Aneurysm s


Clem ens M. Schirm er and Carlos A. David
52.1 In terh em isph eric Pericallosal Ar ter y An eur ysm
52.2 In terh em isph eric Pericallosal Ar ter y An eur ysm at A2–A3 Ju n ct ion
52.3 In terh em isph eric A3-to-A3 Bypass for A2 Fu siform An eu r ysm

Chapter 54 Surgical Therapies fo r Basilar Artery Aneurysm s


Ali F. Krisht
54.1 Orbitozygom at ic Basilar Apex An eur ysm
54.2 ICA, Basilar Apex, an d SCA An eur ysm s
54.3 Ret rosigm oid Com p lex Blister Midbasilar Ar ter y An eur ysm

Chapter 56 Surgical Therapies fo r Vertebral Artery and Po sterio r Inferio r Cerebellar Artery Aneurysm s
Ana Rodríguez-Hernández, Matthew B. Potts, and Michael T. Law ton
56.1 Far-Lateral C1 Lam in ectom y Ver tebral Ar ter y An eu r ysm
56.2 Ver tebral Ar ter y An eu r ysm Clipped an d Wrap ped
56.3 Cer vical VA-to–Facial Bran ch ECA Bypass
56.4 Far-Lateral PICA An eu r ysm
56.5 Far-Lateral PICA-to-VA Bypass

Chapter 57 Micro surgical Managem ent o f Aneurysm s o f the Po sterio r Cerebral, Superio r Cerebellar,
and Anterio r Inferio r Cerebellar Arteries
Jonathan J. Russin and Robert F. Spetzler
57.1 Orbitozygom at ic PCA An eur ysm at P1-P2 Ju n ct ion
57.2 Lateral Su p racerebellar In fraten torial PCA An eur ysm
57.3 Presigm oid Su p racerebellar In fraten torial PCA An eur ysm
57.4 Modified Orbitozygom at ic SCA An eu r ysm
57.5 Ret rosigm oid AICA An eu r ysm

Chapter 59 In fectio us Intracranial An eurysm s


Jonathan J. Russin, W illiam J. Mack , and Steven L. Giannotta
59.1 Mycot ic Midbasilar Ar ter y An eu r ysm Secon dar y to Coccidioides im m it is

Chapter 61 Giant Aneurysm s


M. Yashar S. Kalani and Robert F. Spetzler
61.1 Min i-Pterion al Gian t MCA An eu r ysm
61.2 Orbitozygom at ic Gian t ACoA An eu r ysm
61.3 Far-Lateral Gian t PICA An eur ysm
61.4 Modified Orbitozygom at ic Previou sly Coiled ACoA An eur ysm
61.5 Previou sly Coiled Gian t Basilar Apex An eu r ysm
61.6 An terior Tem poral Lobectom y for Clip ping an d Rem oval of Gian t Th rom bosed Coiled An eur ysm

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Chapter 62 In cidental Aneurysm s


Issam A. Aw ad, Mahua Dey, Jam es Brorson, and Seon-Kyu Lee
62.1 Mu lt ilobu lated MCA An eu r ysm , Un iversit y of Ch icago
62.2 ICA An eu r ysm Near Perforators, Un iversit y of Ch icago

Chapter 64 Aneurysm s o f Spinal Arteries


Sam uel Kalb, Luis Pérez-Orribo, Mark E. Oppenlander, M. Yashar S. Kalani, and Robert F. Spetzler
64.1 Sp in al Ar ter y An eu r ysm
64.2 Ar ter y of Adam kiew icz An eu r ysm

Chapter 69 Endovascular Treatm ent o f Cerebral Arterioven o us Malfo rm atio n s


R. W ebster Crow ley, Andrew F. Ducruet, Cam eron G. McDougall, and Felipe C. Albuquerque
69.1 Em bolizat ion of Fron tal Ar terioven ous Malform at ion

Chapter 70 Supratento rial Arterioveno us Malfo rm atio ns


Aki Laak so, Mart in Lehecka, Ahm ed Elsharkaw y, and Juha Hernesniem i
70.1 Ru pt u red Parietal Ar terioven ous Malform at ion , Helsin ki Un iversit y Cen t ral Hospital
70.2 Fron t al Ar terioven ou s Malform at ion
70.3 Su praten torial Ar terioven ous Malform at ion
70.4 Ven ous An eu r ysm Associated w ith Ar terioven ous Malform at ion
70.5 Left Fron t al Ar terioven ou s Malform at ion

Chapter 71 Po sterio r Fo ssa Arterioven o us Malfo rm atio n s and Dural Arterioveno us Fistulas
Joao Paulo C. de Alm eida, Alexander L. Coon, Judy Huang, and Rafael J. Tam argo
71.1 Posterior Fossa Verm ian Ar terioven ou s Malform at ion
71.2 Ret rosigm oid Cerebellar Ar terioven ou s Malform at ion

Chapter 72 Giant Arterioveno us Malfo rm atio ns


Aki Laak so, Mart in Lehecka, Ahm ed Elsharkaw y, and Juha Hernesniem i
72.1 Gian t Ar terioven ou s Malform at ion , Helsin ki Un iversit y Cen t ral Hospit al
72.2 Grade IV Ar terioven ou s Malform at ion

Chapter 76 Endovascular Treatm ent fo r Carotid-Caverno us Sinus Fistulas


Jeffrey C. Mai and Brian L. Hoh
76.1 Bicoron al Ar terioven ous Fist u la
76.2 Eth m oidal Du ral Ar terioven ou s Fist u la
76.3 Eth m oidal Du ral Ar terioven ou s Fist u la

Chapter 80 Surgical Man agem ent o f Spinal Vascular Malfo rm atio n s


Maziyar A. Kalani, M. Yashar S. Kalani, and Robert F. Spetzler
80.1 C3 to C6 Ar terioven ou s Malform at ion
80.2 C7 to T3 Ar terioven ous Malform at ion
80.3 T10 to T11 Ar terioven ou s Fist u la
80.4 Ar terioven ou s Malform at ion of th e Con u s Medu llaris

Chapter 81 Endovascular Treatm ent o f Spinal Arterioveno us Malfo rm atio ns


Andrew F. Ducruet, R. W ebster Crow ley, Cam eron G. McDougall, and Felipe C. Albuquerque
81.1 Sp in al Angiogram of Ar terioven ous Fist ula at T4

Chapter 82 Trigem in al an d Glo sso pharyngeal Neuralgia


Peter J. Jannet ta
82.1 Ret rosigm oid Decom pression of Glossoph ar yngeal Ner ve
82.2 Ret rosigm oid Decom pression of Glossoph ar yngeal Ner ve

Chapter 83 Microvascular Deco m pressio n fo r Trigem inal Neuralgia: Operative Results in 2,488 Cases
Tak anori Fuk ushim a and Kentaro W atanabe
83.1 Microvascu lar Decom p ression for Trigem in al Neuralgia, Carolin a Neuroscien ce In st it u te
83.2 Microvascu lar Decom p ression for Trigem in al Neuralgia

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Video Contents xvii

Chapter 84 Surgical Man agem ent o f Hem ifacial Spasm


Charles Teo and Brian J. Dlouhy
84.1 Microvascu lar Decom p ression for Hem ifacial Spasm s
84.2 Microvascu lar Decom p ression for Hem ifacial Spasm s
84.3 Microvascu lar Decom p ression for Hem ifacial Spasm s

Chapter 86 Micro surgical Managem ent o f Vascular Tum o rs


Fangxiang Chen, Juliet Kim , Vilaas Shett y, and Saleem I. Abdulrauf
86.1 Carot id Body Tum or

Chapter 87 Micro surgical Managem ent o f Vascular Spinal Tum o rs


Yury Kushel
87.1 T1 to T2 In t ram edu llar y Hem angioblastom a, Bu rd en ko Neurosurgical In st it u te
87.2 Large Cer vical Epen dym om a
87.3 C3 to T1 Ep en dym om a
87.4 L1 to L2 In t radu ral Ext ram ed ullar y Tu m or of th e Filu m Term in ale

Chapter 88 Skull Base Appro aches to the Anterio r and Middle Cranial Fo ssa
Kaith K. Alm eft y and Ossam a Al-Meft y
88.1 Orbitozygom at ic Ap proach An im at ion
88.2 Min i- Orbitozygom at ic Ap p roach An im at ion
88.3 Pterion al Ap p roach An im at ion
88.4 Middle Fossa Ap proach An im at ion
88.5 In terh em isph eric Approach An im at ion

Chapter 89 Surgical Appro aches to the Po sterio r Fo ssa


Just in M. Sw eeney, A. Sam y Youssef, and Harry R. van Loveren
89.1 Far-Lateral Ap p roach An im at ion
89.2 Ret rosigm oid Approach An im at ion
89.3 Kaw ase Ap proach An im at ion
89.4 Ret rolabyrin th in e App roach An im at ion

Chapter 91 Keyho le Cran ial Appro aches fo r Cerebrovascular Surgery


Peter Nakaji
91.1 Brain stem Cavern ou s Malform at ion
91.2 Brain stem Cavern ou s Malform at ion
91.3 Brain stem Cavern ou s Malform at ion
91.4 Brain stem Cavern ou s Malform at ion
91.5 In t racerebellar Lesion

Chapter 92 Surgical Expo sure o f the Vertebral Artery


Bernard George and Michaël Bruneau
92.1 Ver tebral Ar ter y V3 Segm en t Exposure During Ju xt acon dylar App roach for Tum or, Hôpit al Erasm e
92.2 Far-Lateral Ver tebral Ar ter y Decom pression
92.3 Ver tebral Ar ter y Decom pression

Chapter 93 Bypass Surgery fo r Aneurysm s and Tum o rs


Laligam N. Sekhar, Farzana Tariq, Basavaraj Ghodke, and Louis J. Kim
93.1 Bon n et Bypass Left STA Bifu rcat ion to Righ t MCA
93.2 Bon n et Bypass Left STA Bifu rcat ion to Righ t MCA
93.3 Bon n et Bypass Left STA Bifu rcat ion to Righ t MCA

Chapter 94 Excim er Laser-Assisted No no cclusive Anasto m o sis


Albert van der Zw an, Tristan van Doorm aal, Luca Regli, and Cornelis A.F. Tulleken
94.1 ELANA Byp ass, Un iversit y Medical Cen ter Ut rech t

Chapter 95 In tracranial–Extracranial Bypass Surgery fo r Moyam oya Disease


Peter A. Gooderham and Gary K. Steinberg
95.1 STA-to-MCA Bypass for Moyam oya Disease, St an ford Un iversit y Sch ool of Medicin e
95.2 STA-to-MCA Bypass for Moyam oya Disease
95.3 MCA In direct Byp ass for Moyam oya Disease

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xviii Video Contents

Chapter 96 In tracranial–Intracranial Bypass Surgery


Matthew B. Potts, Ana Rodríguez-Hernández, and Michael T. Law ton
96.1 Pterion al An terior Tem poral Ar ter y–to-MCA Bypass
96.2 Modified Orbitozygom at ic An terior Tem p oral Ar ter y–to-MCA Bypass
96.3 Far-Lateral PICA-to-PICA Bypass

Chapter 98 Po sterio r Circulatio n Bypass Surgery


Yasuhiro Yonekaw a
98.1 Orbitozygom at ic STA-to-SCA Bypass
98.2 Far-Lateral PICA-to- Occipit al Ar ter y Bypass

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Preface

In th e t w o decades th at h ave passed sin ce th e first copy of Neu- As w e n ote above, th e diseases th at plagu ed ou r p at ien t s a score
rovascular Surgery w as edited by Drs. Car ter, Sp et zler, an d Ham - of years ago h ave n ot ch anged greatly, so th e subject m at ter of
ilton , m uch h as h app en ed in th e w orld. Th e in tern et h as m oved Neurovascular Surgery is also n ot greatly ch anged. How ever, th e
from n ovelt y to u biqu it y, th e developing w orld h as seen a m ajor specific topics and content have been revised extensively, reflect-
rise in w ealth an d in flu en ce, an d 1.5 billion m ore p eople w alk ing th e advan ces in kn ow ledge th at h ave been ach ieved an d th e
th e ear th . Th e cerebrovascu lar diseases an d con dit ion s th at af- exp an sion in n ew tech n iqu es th at th e field h as enjoyed in th e
flict people today are broadly sim ilar to th ose in decades past , in ter ven ing years. With th ese u pdates, th e book again represen t s
but our un derstan ding of th ese con dit ion s an d our approach es to a com pilat ion of w h at is cu rren tly kn ow n , to ser ve as both a text
t reat ing th em h ave evolved m ore in th e last 20 years th an in any for st udy by th ose en tering th e field an d a referen ce for th ose
prior in ter val. already p ract icing.
Ju st as it did 20 years ago, n eu rovascu lar su rger y st ill repre- Th e book is divided in to 10 sect ion s sp an n ing 99 ch apters.
sen ts an ap ex su bsp ecialt y, a p ar t icu larly t reach erou s field th at Th e first sect ion is fou n dat ion al, covering develop m en t , an at-
dem an ds com plete com m it m en t from th ose w h o w ou ld scale its om y, an d physiology relevan t to n orm al an d abn orm al cerebral
rarefied h eigh t s (an d frequ en t depth s). Th e goal of th e first edi- an d spin al vasculat ure. Th e secon d covers evaluat ion an d t reat-
t ion of th is book w as to su m m arize w h at w as kn ow n abou t th e m en t con siderat ion s for n eurovascular disease. Th e th ird covers
diagn osis an d t reat m en t of n eu rovascu lar con dit ion s th at cou ld isch em ic st roke an d vascular in su fficien cy, an area w h ich is of
be t reated w ith surger y, in cluding n at u ral h istor y, epid em iology, equ al in terest to n eu rologist s an d n eu rosu rgeon s, an d an area
p ath op hysiology, an d t reat m en t tech n iqu es. It w as a m assive w h ere societ y h as realized m u ch w ork rem ain s to be don e. Th e
tom e th at filled a defin ite n eed. Th e dram at ic sh ift th at w as just fourth details the biology, pathophysiology, and th e surgical m an-
begin n ing to occu r in n eu rovascu lar su rger y w h en th e book w as agem en t of cerebral an d spin al cavern ou s m alform at ion s. Th e
released in 1994 w as th e rise of en d ovascular th erapy, w h ich fifth focuses on cerebral an d spin al an eur ysm s; an eur ysm care
w as th en a develop ing m odalit y th at w as st ill m odest in scop e h as evolved exten sively sin ce th e last edit ion , an d th is sect ion
an d dissem in at ion . In th e in ter ven ing years, en dovascular th er- reflect s th at . Th e sixth sect ion u pdates ou r kn ow ledge of cere-
apy h as m at ured greatly, expan ded in cap abilit y, an d its use h as bral an d spin al ar terioven ou s fist ulas an d m alform at ion s, a rare
becom e w idespread. but often con fusing an d t roublesom e set of en t it ies. Th e seven th
Healthy an d vigorou s debate abou t w h en to u se w h ich th er- section, covering disorders of ephaptic t ransm ission , encom passes
apy for w h ich n eu rovascular con dit ion carries on , n o less h ere at m icrovascular com pression syn drom es. Th ese syn drom es are of
Barrow Neurological Institute than elsew here. A book such as th is in terest to m any n eu rosu rgeon s w h o perform op en p rocedures,
edit ion of Neurovascular Surgery h elps th ose pract icing en dovas- as th ese disorders are caused by blood vessels an d addressed by
cular surger y to m ake th ough tfu l progress in w h at is st ill a ver y th e m oving of blood vessels. Th e eigh th con cern s it self w ith vas-
n ew an d ch anging field. Th e learn ing cu r ve for open n eurovascu- cu lar con sid erat ion s in t h e m an agem en t of t u m ors. Th e su rgi-
lar su rger y h as already h it a tech n ically h igh level, bu t com pet ing cal ap proach es to h igh ly vascular t u m ors h ave m u ch in com m on
th erapies m ean fu t u re p roficien cy is h am pered som ew h at —by w it h th ose p er t in en t to vascu lar m alfor m at ion s, an d m ay be
learn ing a m u ltit u de of tech n iqu es an d app roach es, th e exp eri- sim ilarly ad d ressed w it h em bolizat ion . Th e n in t h sect ion d e-
ence of new practitioners w ith each individual techniques is m ore scribes su rgical ap proach es, w ith a p ar t icu lar em ph asis on sku ll
lim ited com p ared w ith th e previou s gen erat ion of p ract it ion ers. base approach es, m in im ally invasive ap proach es, an d th e role of
For th ese reason s, esp ecially d eep st u dy an d p reparat ion is en doscopy. Th e ten th sect ion addresses th e various tech n iques
n eeded by th ose early in th eir n eu rovascular careers to be able to an d applicat ion s of cerebral revascularizat ion , a field th at h as
ach ieve th e levels of exp er t ise at t ain ed by t h eir m en tors w h o been put un der pressure by results from recen t clin ical t rials,
gain ed exp er ien ce in a m u ch d ifferen t era. Ap p rop r iately, w e w h ich pu t its use for isch em ia in to dou bt again . How ever, th is
th ree editors rep resen t in dividu als at th e early, m iddle, an d late sect ion sh ow s th e rich ap p licat ion s of byp asses for st ill solid in -
st ages of t h eir careers (w e leave it for th e reader to sp ecu late dicat ion s, an d th erefore th e m aster y of bypass in t ricacies is st ill
w h o represen t s each stage). w or th w h ile.
Th e process of sh aring ou r kn ow ledge from gen erat ion to Th e n ext p h ase of n eu rovascu lar u n derst an d ing an d care w ill
gen erat ion an d w ith in gen erat ion s, even as w e m ake n ew ad- likely be in m olecu lar diagn ost ics an d th erapeut ics. Much h as
van ces, is a key com m it m en t th at drives all of us. In th is secon d been learn ed in th is regard, th ough w e h ave th e sen se th at w e
edit ion of Neurovascular Surgery, w e h ave p reser ved th e goal of are like th e early Egyptologist s w h o saw h ieroglyph ics but w h o
th e first edit ion by p resen t ing a com p reh en sive, accessible, an d h ad n ot yet foun d th e Roset t a ston e n eeded to decode th em .
practical com pilation of know ledge about n eurovascular diseases. W h at is n ow kn ow n is tou ch ed on in m any areas of t h is text . On e

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xx Preface

h op es t h at t h e n ext ed it ion of t h is book, likely soon er t h an 20 in g an d m an aging t h e p rocess, an d Alison Hu ebn er an d Man d i
years h en ce, w ill be rep lete w it h su ch con ten t becau se of t h e Leite for for m at t ing t h e text an d keep ing u s on t rack. Mark
su bstan t ive p rogress th at w ill h ave been m ade in th is area an d Sch orn ak, Kristen Larson , an d Jen n ifer Darcy provided m any of
th e im pact it w ill h ave on pat ien ts’ lives. th e sen sat ion al illu st rat ion s th at bring t h e operat ive tech n iqu es
Neurosurgical kn ow ledge ch anges rap idly. In th is digital age, an d an atom ical st ruct ures to life. Mich ael Hickm an com posed
m u ch in form at ion is available on lin e. You m ay as likely read th e im age th at graces th e cover of th is edit ion , an d Marie Clark-
th ese w ords on an elect ron ic device as on p ap er. For som e of u s, son edited th e n u m erou s op erat ive videos th at com p lem en t th e
th ere is a p leasu re in th e com for t ing h eft of a prin ted book an d text . Jaim e-Lyn n Can ales an d Cassan dra Todd m et iculou sly for-
th e t u rn ing of p ages th at feels alm ost lu xu riou s in th is pixelated m at ted an d m an aged each figu re in t h is w ork. Ou r fr ien d s at
age. How ever, t h e add it ion of a large cach e of vid eos p er t in en t Th iem e are to be recogn ized for t h eir con t in u ed com m it m en t
to topics in th is book m ean s th at th e reader w ill in evit ably t u rn to excellen ce in p u blish in g, an d w e are d eligh ted to h ave t h em
back to a digit al form at . Non eth eless, th e m ain reason for a tom e as th e n ew publish ers for th is edit ion . We recogn ize am ong ou r
su ch as th is, in w h atever form , is th at th ere is m u ch n eed for an ow n n um ber Dr. Yash ar Kalan i, w h o u n dertook th e lion’s sh are of
auth oritat ive book th at h as been m et iculously edited. Our prin - th e effor t in m aking th is secon d edit ion in to th e realit y you h old
cipal h ope an d in ten t ion is th at th e large am oun t of h igh -qualit y in your h an ds.
per t in en t in form at ion assem bled h erein w ill ben efit th e care of As a fin al n ote, w e w ish to recogn ize an d m ou rn th e passing
you r pat ien ts w ith n eu rovascular problem s. of Ph il Car ter, th e last lead editor of th is book. His con t ribut ion s
Th is book represen ts a colossal effor t from a great m any in di- w ere m any an d h e is rem em bered w ith fon dn ess an d respect .
vidu als. We th an k th e m any au th ors w h o con t ributed th eir t im e Please enjoy th e book. We h ope to fin d read ers su ch as you on
an d en ergy to th e in dividual ch apters an d videos. Th e Barrow th e auth or list in th e n ext edit ion of Neurovascular Surgery.
Neu rological In st it u te’s Neu roscien ce Pu blicat ion s office, forever
supportive despite the Herculean tasks w e pile on th em , deser ves Robert F. Spetzler, MD
special recogn it ion . Our sin cere th an ks go to Sh elley Kick, Daw n M. Yashar S. Kalani, MD, PhD
Mu tch ler, an d Pau la Card Higgin son for th eir diligen t edit ing of Peter Nakaji, MD
each ch apter, an d w e also th an k Clare Pren dergast for p roofread-

Neurosurgery Books Full


Acknow ledgments

We th an k th e au th ors of th e ch apters for taking t im e from th eir Jaim e-Lyn n Can ales, Clare Pren dergast , Daw n Mu tch ler, Pau la
clin ical p ract ice to h elp p rodu ce th is volu m e. Sp ecial th an ks to Card Higgin son , Mich ael Hickm an , Marie Clarkson , an d Kristen
th e editors, illu st rators, an d an im ators at th e Neu roscien ce Pu b - Larson . Th e editors w ish to exten d a n ote of grat it u de to Kay
licat ion s office at Barrow Neu rological In st it u te. Th is w ork w ou ld Con erly, Judith Tom at , an d Tim Hiscock at Th iem e Publish ing for
n ot be possible w ith ou t th e dedicated w ork of Mark Sch orn ak, th eir assistan ce w ith th is w ork.

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Neurosurgery Books Full
Contributors

Salee m I Abdulrauf, MD, FACS Ossam a Al-Mefty, MD, FACS


Professor an d Ch airm an Director
Depart m en t of Neu rosu rger y Sku ll Base Su rger y
Sain t Lou is Un iversit y Depar t m en t of Neu rological Surger y
Sain t Lou is, Missou ri Brigh am an d Wom en’s Hospital an d Har vard Medical Sch ool
Lect urer
Har vard Medical Sch ool
Adib A Abla, MD
Boston , Massach u set t s
Assistan t Professor
Director of Cerebrovascu lar Su rger y
Kaith K Alm efty, MD
Director of Neurovascular Research
Neu rosu rger y Residen t
Depart m en t of Neu rosu rger y
Barrow Neurological In st it ute
Un iversit y of Arkan sas
St . Joseph’s Hospit al an d Medical Cen ter
for Medical Scien ces College of Medicin e
Ph oen ix, Arizon a
Lit tle Rock, Arkan sas
Ram i O Alm efty, MD
Jo seph G Adel, MD Neu rosu rger y Residen t
Neu rosu rgeon Barrow Neurological In st it it u e
Depart m en t of Cerebrovascu lar/En dovascu lar an d St . Joseph’s Hospit al an d Medical Cen ter
Sku ll Base Ph oen ix, Arizon a
St . Mar y’s of Mich igan
Sagin aw, Mich igan Jo ão Paulo C de Alm eida, MD
Neu rosu rger y Residen t
Depar t m en t of Neu rosurger y
Felipe C Albuque rque, MD St ate Un iversit y of Cam pin as (UNICAMP)
Assistan t Director an d Professor Cam p in as, São Paulo, Brazil
En dovascu lar Su rger y
Division of Neu rological Surger y Se pideh Am in-Hanjani, MD, FAANS, FACS, FAHA
Barrow Neu rological In st it ute Professor & Residen cy Program Director
St . Joseph’s Hospital an d Medical Cen ter Co-Director, Neu rovascular Su rger y
Ph oen ix, Arizon a Depar t m en t of Neu rosurger y
Un iversit y of Illin ois at Ch icago
Ch icago, Illin ois
Yazan J Alde razi, MB, BCh
Fellow, En dovascular Su rgical Neu roradiology
Salah G Ao un, MD
Depart m en t of Neu rological Su rger y
3rd Year Residen t
Rutgers, New Jersey Medical Sch ool
Depar t m en t of Neu rological Surger y
Th e State Un iversit y of New Jersey
Th e Un iversit y of Texas South w estern
New ark, New Jersey
Dallas, Texas

Michael J Alexander, MD Adam S Arthur, MD, MPH


Professor an d Vice- Ch airm an Associate Professor
Director, Neu rovascu lar Research Depar t m en t of Neu rosurger y
Cedars San ai Medical Cen ter Un iversit y of Ten n essee Dep ar t m en t of Neu rosu rger y
Depart m en t of Neu rosu rger y Sem m es Murph ey Neurologic an d Sp in e In st it ute
Los Angeles, Californ ia Mem ph is, Ten n essee

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xxiv Contributors

Ram sey Asho ur, MD Helm ut Be rtalanffy, MD


Cerebrovascu lar Fellow Professor of Neu rosu rger y
Depart m en t of Neu rosu rger y Director of Vascular Neurosu rger y
Brigh am an d Wom en’s Hospit al In tern at ion al Neuroscien ce In st it u te Han n over
Har vard Medical Sch ool Han n over, Germ any
Boston , Massach u set t s
Gaurav Bhardw aj, MBBS, PhD
Issam A Aw ad, MD, MSc, FACS, MA (ho n)
Oph th alm ologist
Th e Joh n Harper Seeley Professor
Fellow in Medical Ret in a an d Uveit is
Su rger y (Neu rosu rger y), Neu rology an d th e Can cer Cen ter
Th e Royal Victorian Eye an d Ear Hosp ital
Director of Neu rovascu lar Su rger y
Sydn ey, Au st ralia
Un iversit y of Ch icago Med icin e an d Biological Scien ces
Ch icago, Illin ois
Je ns Bjerregaard, MD, MS
Mo ham m ad Ali Aziz-Sultan, MD An esth esiologist
Sect ion Ch ief, Cerebrovascu lar/En dovascular Su rger y Depar t m en t of An esth esiology
Depart m en t of Neu rosu rger y Kaiser Perm an en te
Brigh am an d Wom en’s Hospit al Sacram en to, Californ ia
Har vard Medical Sch ool
Boston , Massach u set t s
Markus Bo o kland, MD
Assistan t Professor
Daniel L Barrow , MD, FACS
Division of Pediat ric Neurosu rger y
MBNA, Bow m an Professor & Ch airm an
Con n ect icu t Ch ildren’s Medical Cen ter
Director, Em or y MBNA St roke Cen ter
Har tford, Con n ect icu t
Depart m en t of Neu rosu rger y
Em or y Universit y Sch ool of Medicin e
Atlan ta, Georgia Jam es Bro rso n, MD
Associate Professor
H Hunt Batje r, III, MD, FACS Depar t m en t of Neu rology
Professor & Ch air Th e Un iversit y of Ch icago
Depart m en t of Neu rological Su rger y Ch icago, Illin ois
UT Sou th w estern Medical Sch ool
Dallas, Texas
Tho m as G Brott, MD
Professor
Andrew M Bauer, MD, MBA
Depar t m en t of Neu rology
Clin ical Associate
Mayo Clin ic Florida
Cerebrovascu lar Cen ter
Jacksonville, Florida
Clevelan d Clin ic
Clevelan d, Oh io
Michaël Bruneau, MD, PhD
Hansjö rg Bäzner, MD Professor
Neu rosu rgeon Sku ll Base an d Vascu lar Program s Director
Depart m en t of Neu rology Depar t m en t of Neu rosurger y
Un iversitäts Medizin Man n h eim UMM Erasm e Hospit al
Un iversit y of Heidelberg Br ussels, Belgiu m
Man n h eim , Germ any
Jo sé Guilhe rm e Mendes Pere ira Caldas, MD, PhD
Tibo r Becske, MD
Director, In ter ven t ion al Neuroradiology
Assistan t Professor
Depar t m en t of Radiology
Radiology (Neu ro In ter ven t ion al) an d Neu rology
Un iversit y of São Paulo
New York Un iversit y Langon e Medical Cen ter
São Paulo, Brazil
New York, New York

Be rnard R Be ndo k, MD, MSCI Alvaro Cam pero, MD, PhD


Ch air Assistan t Professor
Depart m en t of Neu rological Su rger y Depar t m en t of Neu rosurger y
Mayo Clinic Hospit al Hospit al Padilla
Ph oen ix, Arizon a Tucu m án , Argen t in a

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Contributors xxv

Ricardo L Carrau, MD Fangxiang Chen, MD


Professor Assistan t Professor
Depart m en t of Otolar yngology Depar t m en t of Neu rological Surger y
Head & Neck Su rger y St . Lou is Un iversit y
Director St . Lou is, Missouri
Th e Com preh en sive Sku ll Base Surger y Program
Co-Director William P Cheshire, Jr , MD
An atom y Laborator y Tow ard Visu osp at ial Su rgical Professor of Neu rology
In n ovat ion s in Otolar yngology an d Neu rosu rger y Depar t m en t of Neu rology
(ALT-VISION) Mayo Clin ic
Th e Oh io State Un iversit y Wexn er Medical Cen ter Starling Jacksonville, Florida
Loving Hall
Colu m bus, Oh io Ro han Chitale, MD
Assistan t Professor
Daniel B Case, MD Depar t m en t of Neu rological Surger y
Fellow Depar t m en t of Radiology an d Radiological Scien ces
Neu roin ter ven t ion al Surger y Van derbilt Un iversit y Medical Cen ter
Radiology Associates of Florida Nashville, Ten n essee
Tam pa, Florida
Shakeel A Chow dhry, MD
Clin ical Assistan t Professor
Daniel D Cavalcanti, MD
Division of Neu rological Su rger y
Assistan t Professor
Barrow Neurological In st it ute
Depart m en t of Neu rosu rger y
St . Joseph’s Hospit al an d Medical Cen ter
Pau lo Niem eyer State Brain In st it u te
Ph oen ix, Arizon a
Rio de Jan eiro, Brazil
Abhineet Chow dhary, MD
C Michael Caw ley, MD, FACS Director of Neurosurger y
Associate Professor Director of Neuro-In ter ven t ion al Su rger y
Depart m en t of Neu rosu rger y & Radiology Overlake Hosp ital
Em or y Un iversit y Sch ool of Medicin e Bellevue, Wash ington
Atlan ta, Georgia
E Sande r Co nno lly, Jr , MD
Feres Chaddad, MD, PhD Ben n et t M. Stein Professor an d Vice- Ch airm an
Professor of Vascular Neu rosurger y Depar t m en t of Neu rological Surger y
Depart m en t of Neu rosu rger y Colum bia Un iversit y
Federal Un iversit y of São Pau lo-UNIFESP New York, New York
São Pau lo, Brazil
Do uglas J Co o k, MD, PhD, FRCS(C)
Assistan t Professor
No hra Chalo uhi, MD
Director, Tran slat ion al St roke Research Program
PGY-2 Resid en t
Depar t m en t of Su rger y, Division of Neurosurger y
Depart m en t of Neu rosu rger y
Queen’s Un iversit y
Th om as Jefferson Un iversit y an d Jefferson Hospit al for
Kingston , On tario, Can ada
Neu roscien ce
Ph ilad elp h ia, Pen n sylvan ia
Alexander L Co o n, MD
Assistan t Professor of Neu rosu rger y, Neurology, an d Radiology
Steve n D Chang, MD Director of En dovascular Neurosu rger y
Rober t C. an d Jean n et te Pow ell Professor Depar t m en t of Neu rosurger y
Depart m en t of Neu rosu rger y Joh n s Hopkin s Un iversit y Sch ool of Medicin e
St an ford Un iversit y Sch ool of Medicin e Th e Joh n s Hopkin s Hosp ital
St an ford, Californ ia Balt im ore, Mar ylan d

Fady T Charbel, MD R Webster Crow ley, MD


Professor an d Head Assistan t Professor
Depart m en t of Neu rosu rger y Division of Neu rosu rger y an d Radiology
Un iversit y of Illin ois at Ch icago Un iversit y of Virgin ia Health System
Ch icago, Illin ois Ch arlot tesville, Virgin ia

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xxvi Contributors

Mark J Dannenbaum , MD Andrew F Ducruet, MD


Assistan t Professor Assistan t Professor
Depar t m en t of Neu rosu rger y Neu rological Su rger y
Th e Un iversit y of Texas Medical Sch ool Hou ston Un iversit y of Pit tsburgh
Misch er Neuroscien ce In st it u te Pit t sbu rgh , Pen n sylvan ia
Mem orial Herm an n /Texas Medical Cen ter
Hou ston , Texas Aaro n S Dum o nt, MD
Ch airm an
Carlo s A David, MD Depar t m en t of Neurosurger y
Director, Cerebrovascu lar an d Sku ll Base Su rger y Tulan e Un iversit y Sch ool of Pu blic Health
Depar t m en t of Neu rosu rger y Tulan e Neurosu rger y Clin ic
Lah ey Health New Orlean s, Louisian a
Bu rlington , Massach u set ts
Travis M Dum o nt, MD
Assistan t Professor of Neurosurger y
Arthur L Day, MD
Assistan t Professor of Medical Im aging
Professor, Vice Ch airm an , an d Residen cy Program
Director, Neurovascular Program
Director
Division of Neu rosu rger y, Dep ar t m en t of Su rger y
Depar t m en t of Neu rological Su rger y
Un iversit y of Arizon a
Misch er Neuroscien ce In st it u te
Tucson , Arizon a
Un iversit y of Texas Medical Sch ool at Houston
Hou ston , Texas Christo pher S Eddlem an, MD, PhD
Neu rosu rgeon
Evandro de Olive ira, MD, PhD Neu rovascu lar In ter ven t ion alist
Professor of Neu rosu rger y Hen drick Medical Cen ter
In st it ute of Neurological Scien ces Abilen e, Texas
In st it ut ion Ben eficên cia Por t uguesa Hospit al Adju n ct Assistan t Professor in Neu rological Surger y
São Pau lo, Brazil UT Sou th w estern Medical Cen ter
Dallas, Texas
Ro bert J De m psey, MD
Ch airm an an d Man uch er J. Javid Professor of Neu rological Tarek Y El Ahm adieh, MD
Su rger y Su rger y Residen t
Depar t m en t of Neu rological Su rger y Depar t m en t of Neurological Su rger y
Un iversit y of Wiscon sin Sch ool of Medicin e an d Pu blic Un iversit y of Texas South w estern
Health Dallas, Texas
Madison , Wiscon sin
Mo ham e d Sam y Elham m ady, MD
Mahua Dey, MD Assistan t Professor
Neu rosu rger y Residen t Un iversit y of Miam i
Neu rovascular Surger y Program Depar t m en t of Neurological Su rger y
Sect ion of Neurosu rger y Lois Pop e Life Cen ter
Un iversit y of Ch icago Miam i, Florida
Ch icago, Illin ois
Jo rge L Eller, MD, FAANS
Clin ical Assist an t Professor
Brian J Dlo uhy, MD
Depar t m en t of Neurological Su rger y
Neu rosu rgical Fellow
Th om as Jefferson Un iversit y at Atlan t icare Region al Medical
Cen t re for Min im ally Invasive Neu rosu rger y
Cen ter
Ken sington , New Sou th Wales, Au st ralia
Atlan t ic Cit y, New Jersey

Tristan van Do o rm aal, MD, PhD Jaso n A Ellis, MD


Neu rosu rgeon Neu rosu rgeon
Depar t m en t of Neu rosu rger y Depar t m en t of Neurological Su rger y
Un iversit y Medical Cen ter Ut rech t Colum bia Un iversit y Medical Cen ter
Ut rech t , Th e Neth erlan ds New York, New York

Chelsea A Do rsey, MD Ahm e d Elsharkaw y, MD, PhD


Ch ief Residen t Lect u rer of Neu rosu rger y
Vascu lar an d En d ovascu lar Surger y Neu rosu rger y Dep ar t m en t
St an ford Un iversit y Tan t a Un iversit y
Palo Alto, CA Tan t a, Egypt

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Contributors xxvii

Najib E El Te cle, MD, MS Ian C Francis, OAM, MB, BS (Syd), FRACS, FRANZCO,
Residen t FASOPRS, PhD (NSW), FANZSOPS
Depart m en t of Neu rological Su rger y Associate Professor
Nor th w estern Mem orial Hosp ital Depar t m en t of Opth alm ology
Ch icago, Illin ois Oph th alm ic Surgeon
Depar t m en t of Op h th alm ology
Yo shua Esque nazi, MD Prin ce of Wales Hospital
Ch ief Residen t Sydn ey, Au st ralia
Depart m en t of Neu rosu rger y
Un iversit y of Texas W David Free m an, MD
Health Scien ce Cen ter at Hou ston Professor of Neu rology, Dep ar t m en t s of Neurosurger y,
Houston , Texas Neu rology an d Crit ical Care, Neuroscien ces ICU Director
Neu rosu rger y
Jaco b Fairhall, MB, BS (Ho ns), BSc (Med), FRACS Mayo Clin ic
Con su ltan t Neurosu rgeon Jacksonville, Florida
Prin ce of Wales Hosp ital
Sydn ey, New Sou th Wales, Aust ralia Juhana Frö sen, MD, PhD
Associate Professor
Con sultan t Neurosu rgeon
Manuel Fe rre ira, Jr , MD, PhD
Depar t m en t of Neu rosurger y
Co-director of Sku ll Base an d Min im ally Invasive
Kuop io Un iversit y Hosp ital
Neu rosu rger y
Kuop io, Fin lan d
Harbor view Medical Cen ter
Assistan t Professor of Neu rological Su rger y
Michel Eli Frudit, MD, PhD
Un iversit y of Wash ington
Assistan t Doctor
Seat tle, Wash ington
Depar t m en t of Neu rosurger y
Depar t m en t of In ter ven t ion al Neu roradiology
Mauro A T Ferreira, MD, PhD
Federal Un iversit y of São Paulo-UNIFESP
Professor, Dep ar t m en t s of An atom y an d Radiology
Un iversit y of São Paulo
Federal Un iversit y of Miin as Gerais
São Paulo, Brazil
Belo Horizon te, Brazil
Form er Dr. Robert F. Sp et zler Research Fellow on
Takano ri Fukushim a, MD, DMSc
Micron eu rosu rgical An atom y
Director
Barrow Neurological In st it u te
Carolin a Neu roscien ce In st it ute
Ph oen ix, Arizon a
Raleigh , Nor th Carolin a

David Fio rella, MD, PhD Bernard Ge o rge, PhD


Professor of Radiology an d Neu rosu rger y Professor Em erit u s
Depar t m en t of Neu rosu rger y Depar t m en t of Neu rosurger y
Stony Brook Medical Cen ter Hôp ital Lariboisière
Stony Brook, New York Paris, Fran ce

Alana M Flexm an, MD Venelin Gerganov, MD, PhD


Clin ical Assistan t Professor Associate Professor
Depar t m en t of An esth esiology, Ph arm acology, an d Depar t m en t of Neu rosurger y
Th erapeut ics In tern at ion al Neuroscien ce In st it u te
Un iversit y of Brit ish Colu m bia Han n over, Germ any
Van couver, Brit ish Colum bia, Can ada
Mahan Ghiassi, MD
Jo hn C Flickinge r, MD Co-Director Cerebrovascu lar an d En dovascular
Professor Neu rosu rger y
Depar t m en t of Radiat ion On cology Depar t m en t of Neu rosurger y
Un iversit y of Pit tsbu rgh Wash ington Region al Medical Cen ter
Pit t sbu rgh , Pen n sylvan ia Fayet teville, Arkan sas

Be njam in D Fox, MD Mayshan Ghiassi, MD


Neu rovascular Medical Director Co-Director Cerebrovascu lar an d En dovascular
Sou th ern Ut ah Neu roscien ces In st it u te Neu rosu rger y
In term oun tain Health care Wash ington Region al Medical Cen ter
St . George, Utah Fayet teville, Arkan sas

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xxviii Contributors

Basavaraj Gho dke, MD Hans He nkes, MD


Associate Professor Medical Director
Depar t m ent of Radiology Klin iku m St u t tgar t
Neu rological Su rger y St ut tgar t , Germ any
Un iversit y of Wash ington
Harbor view Medical Cen ter
Juha He rnesniem i, MD, PhD
Seat tle, Wash ington
Professor an d Ch airm an
Depar t m en t of Neu rosurger y
Steve n L Giannotta, MD
Helsin ki Un iversit y Cen t ral Hospital
Ch airm an Dep ar t m en t of Neu rological Su rger y
Helsin ki, Fin lan d
Keck/USC Sch ool of Med icin e
Los Angeles, Californ ia
Ro berto C Hero s, MD
Hannah Goldste in, MD Professor, Co- Ch airm an an d Program Director
Residen t Depar t m en t of Neu rosurger y
Depar t m ent of Neu rosu rger y Un iversit y of Miam i Miller Sch ool of Medicin e
Colu m bia Un iversit y Med ical Cen ter Miam i, Florida
New York, New York

L Fe rnando Go nzález, MD Randall T Higashida, MD


Associate Professor of Neu rosu rger y Clin ical Professor of Radiology
Co-director Cerebrovascu lar an d En dovascu lar Neu rosu rger y Neu rological Su rger y
Duke Un iversit y Neu rology an d An esth esiology
Durh am , Nor th Carolin a Director an d Ch ief Of In ter ven t ion al Neurovascular
Radiology
Pete r A Goo derham , MD, FRCSC Radiology
Act ive Staff Un iversit y of Californ ia, San Fran cisco Medical Cen ter
Depar t m ent of Neu rosu rger y San Fran cisco, Californ ia
Un iversit y of Brit ish Colu m bia
Van couver, Brit ish Colum bia, Can ada Brian L Ho h, MD
Jam es an d New ton Eblen Professor of Neurosu rger y,
Gaurav Gupta, MD, MS Radiology, an d Neu roscien ce
Residen t Ch ief
Neu rological Su rger y Th e UF Neu rovascular Program
Colu m bia Un iversit y Med ical Cen ter Depar t m en t of Neu rosurger y
New York, New York Un iversit y of Florida
Gain esville, Florida
Zakaria Hakm a, MD
Neu rosu rgeon
Depar t m ent of Neu rosu rger y Niko lai J Ho pf, MD, PhD
Cap ital In stit u te for Neu roscien ce Neu rosu rgeon
Pen n ington , New Jersey Cen ter for En doscopic an d Min im al Invasive Su rger y
St ut tgar t , Germ any
Ricardo A Hanel, MD, PhD
En dovascu lar Su rgical Neu roradiology Fellow sh ip
L Nelso n Ho pkins, MD
Program Director
Dist ingu ish ed Professor
Mayo Sch ool of Graduate Medical Ed ucat ion
Depar t m en t of Neu rosurger y
Jacksonville, Florida
Presiden t , CEO
Gates Vascu lar In st it u te
Seth Hayes, MD
CEO
Neu rosu rger y Residen t
Jacobs In st it u te
Depar t m ent of Neu rosu rger y
Bu ffalo, New York
Un iversit y of Miam i-Miller Sch ool of Medicin e
Miam i, Florida
Jam es F How ard, Jr , MD
Jo seph E Heiserm an, MD, PhD Dist ingu ish ed Professor of Neu rom uscu lar Disease
St aff Neu roradiologist Professor of Neu rology & Medicin e
Division of Neu roradiology Depar t m en t of Neu rology
Barrow Neurological In st it u te Un iversit y of Nor th Carolin a
Ph oen ix, Arizon a Ch apel Hill, Nor th Carolin a

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Contributors xxix

Judy Huang, MD, FAANS Am in B Kassam , MD


Associate Professor of Neu rosu rger y Vice Presiden t
Program Director, Neu rosurger y Residen cy Neu roscien ces System Clin ical Program
Director, Fellow sh ip in Cerebrovascu lar Neu rosu rger y Aurora Neu roscien ce In n ovat ion In st it u te
Joh n s Hopkin s Un iversit y Sch ool of Medicin e Medical Director
Balt im ore, Mar ylan d Neu rosu rger y-Au rora St . Luke’s Medical Cen ter
Milw aukee, Wiscon sin
Pascal M Jabbo ur, MD
Associate Professor Juliet Kim , MD
Depart m en t of Neu rological Su rger y Residen t
Ch ief Division of Neu rovascu lar Surger y an d Un iversit y of Californ ia–Los Angeles Depart m en t
En dovascular Neu rosu rger y of Su rger y
Th om as Jefferson Un iversit y Hospit al Los Angeles, Californ ia
Ph ilad elp h ia, Pen n sylvan ia

Lo uis J Kim , MD
Richard A Jaffe, MD, PhD
Associate Professor
Professor
Depar t m en t s of Neurological Surger y & Radiology
Depart m en t s of An esth esiology an d
Un iversit y of Wash ington Sch ool of Medicin e
Neu rosu rger y
Seat tle, Wash ington
St an ford Un iversit y Sch ool of Medicin e
St an ford, Californ ia
Riku Kivisaari, MD, PhD
Pete r J Jannetta, MD Associate Professor
Neu rosu rgeon Depar t m en t of Neu rosurger y
Depart m en t of Neu rological Su rger y Helsin ki Un iversit y Cen t ral Hosp ital
West Pen n Allegh eny Gen eral Hosp ital Helsin ki, Fin lan d
Pit t sbu rgh , Pen n sylvan ia
Do uglas Ko ndzio lka, MD
Maziyar A Kalani, MD Peter J. Jan n et t a Professor an d Vice- Ch airm an of Neu rological
Neu rosu rger y Residen t Su rger y
Depart m en t of Neu rosu rger y Depar t m en t of Neu rological Surger y
St an ford Un iversit y Sch ool of Medicin e Un iversit y of Pit tsburgh
St an ford, Californ ia Pit t sburgh , Pen n sylvan ia

M Yashar S Kalani, MD, PhD Miikka Ko rja, MD, PhD


Assistan t Professor of Neu rological Su rger y Associate Professor, Cerebrovascu lar Con sultan t
Barrow Neu rological In st it ute Depar t m en t of Neu rosurger y
St . Joseph’s Hospital an d Medical Cen ter Helsin ki Un iversit y Cen t ral Hosp ital
Ph oen ix, Arizon a Helsin ki, Fin lan d

Sam uel Kalb, MD


Ali F Krisht, MD, FACS
Neu rosu rger y Residen t
Professor an d Director
Barrow Neu rological In st it ute
Arkan sas Neuroscien ce In st it u te at St . Vin cen t’s
St . Joseph’s Hospital an d Medical Cen ter
Director, Cerebrovascular an d Neu roen d ocrin e Clin ics
Ph oen ix, Arizon a
Lit tle Rock, Arkan sas

Hideyuki Kano, MD, PhD


Research Associate Professor Gyanendra Kum ar, MD
Director of Clin ical Research at Cen ter for Im age- Gu ided Assistan t Professor
Neu rosu rger y Neu rology
Depart m en t of Neu rological Su rger y Kirklin Clin ic
Un iversit y of Pit tsbu rgh Un iversit y of Alabam a–Birm ingh am
Pit t sbu rgh , Pen n sylvan ia Birm ingh am , Alabam a

Syed Aftab Karim , MD Yury Kushel, MD, PhD


Neu rosu rgeon Neu rosu rgeon
Depart m en t of Neu rosu rger y 2n d Neu rosu rgical Dep ar t m en t
St an ford Un iversit y Medical Cen ter Bu rden ko Neurosurgical In st it u te
St an ford, Californ ia Moscow, Ru ssia

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xxx Contributors

Aki Laakso, MD, PhD Michael R Levitt, MD


Associate Professor En dovascular Neurosurger y Fellow
Depar t m en t of Neu rosu rger y Depar t m en t of Neu rological Surger y
Helsin ki Un iversit y Cen t ral Hosp ital Barrow Neurological In st it u te
Helsin ki, Fin lan d St . Joseph’s Hospit al an d Medical Cen ter
Ph oen ix, Arizon a
Maarten Lansbe rg, MD
Assistan t Professor Elad I Levy, MD, MBA
Depar t m en t s of Neu rology, Neu rosu rger y, an d Neu rological Professor an d Ch airm an of Neurological Surger y, Medical
Scien ces Director, Neuroen dovascu lar Ser vices, Gates Vascular
St an ford Sch ool of Medicin e In st it u te at Kaleida Health
St an ford, Californ ia Neu rosu rger y
Un iversit y at Bu ffalo, Th e St ate Un iversit y of New York
Giuseppe Lan zino , MD Bu ffalo, New York
Professor of Neu rologic Su rger y an d Radiology
Andrew S Little, MD
Mayo Clin ic
Assistan t Professor of Neurosurger y
Roch ester, Min n esot a
Director, Neurological In ten sive Care Un it
Director, Barrow Pit u itar y Ou tcom es Project
Michael T Law to n, MD
Barrow Neurological In st it u te
Professor of Neu rological Surger y
St . Joseph’s Hospit al an d Medical Cen ter
Ch ief of Vascular an d Sku ll Base Neu rosu rger y
Ph oen ix, Arizon a
Vice- Ch airm an , Dep ar t m en t of Neurological Surger y
Un iversit y of Californ ia, San Fran cisco Shih Sing Liu, MD
San Francisco, Californ ia Clin ical In st ru ctor
Depar t m en t of Neu rosurger y an d Brain Repair
Jaso n T Le e, MD Un iversit y of South Florida
Associate Professor of Su rger y Tam pa, Florida
Program Director
Vascu lar Su rger y Residen cy/Fellow sh ip Division of Vascular Christo pher M Lo ftus, MD, Drhc(Ho n), FAANS
Su rger y Treasurer, World Federat ion of Neurological Societ ies
St an ford Un iversit y Medical Cen ter Ch air, AANS In tern at ion al Program s
St an ford, Californ ia Professor an d Ch airm an
Depar t m en t of Neu rosurger y
Jin-Mo o Lee, MD, PhD Professor of Neu rology
Professor of Neu rology, Rad iology, an d Biom edical Engin eering Loyola Un iversit y St ritch Sch ool of Medicin e
Head, Cerebrovascular Disease Sect ion Mayw ood, Illin ois
Depar t m en t of Neu rology
Wash ington Un iversit y Sch ool of Medicin e Javier Lo ren zo , MD
St . Louis, Missouri Clin ical In st ru ctor
An esth esia an d Crit ical Care
Se o n-Kyu Lee, MD, PhD St an ford Un iversit y Sch ool of Medicin e
Director Depar t m en t of An esth esiology, Pain an d Perioperat ive
Neu roin ter ven t ion al Radiology Ser vice Medicin e
Associate Professor of Radiology, Su rger y, an d Neu rology St an ford, Californ ia
In ter vent ion al Neu roradiology Program
L Dade Lunsfo rd, MD, FACS
Sect ion of Neuroradiology
Lars Leksell an d Dist inguish ed Professor
Un iversit y of Ch icago
Depar t m en t of Neu rological Surger y
Ch icago, Illin ois
Un iversit y of Pit tsburgh
Pit t sbu rgh , Pen n sylvan ia
Martin Lehecka, MD, PhD
Associate Professor, Head of Sect ion William J Mack, MD, MS
Depar t m en t of Neu rosu rger y Associate Professor
Helsin ki Un iversit y Cen t ral Hosp ital Depar t m en t of Neu rosurger y
Helsin ki, Fin lan d Un iversit y of South ern Californ ia
Los Angeles, Californ ia
Hanna Lehto , MD
Fellow in Vascu lar Neurosu rger y Jeffrey C Mai, MD, PhD
Depar t m en t of Neu rosu rger y Neu rosu rgeon
Helsin ki Un iversit y Cen t ral Hosp ital In n ova Medical Group
Helsin ki, Fin lan d Fairfax, Virgin ia

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Contributors xxxi

Hani Malo ne, MD David A Mille r, MD


Residen t Physician Assistan t Professor
Depart m en t of Neu rological Su rger y Depar t m en t of Radiology
Colu m bia Un iversit y Mayo Clin ic Florida
New York, New York Jacksonville, Florida

Ro sa Martinez, MD Zam an Mirzadeh, MD, PhD


Fellow Neu rosu rger y Residen t
Clin ic for Neu roradiology Barrow Neurological In st it ute
Neu rozen t r um , Klin iku m St u t tgar t St . Joseph’s Hospit al an d Medical Cen ter
St ut tgar t , Germ any Ph oen ix, Arizon a

Cam ero n G McDo ugall, MD, FRCSC J Mo cco, MD, MS


Professor of Neu rological Surger y Professor an d Vice Ch airm an for Educat ion
Director of En dovascu lar Neu rosu rger y Depar t m en t of Neu rologic Su rger y
Lou an d Evelyn Gr u bb En dow ed Ch air Mou n t Sin ai Health System
Division of Neu rological Surger y New York, New York
Barrow Neu rological In st it ute
St . Joseph’s Hospital an d Medical Cen ter Maxim Mo kin, MD, PhD
Ph oen ix, Arizon a Assistan t Professor
Neu rology an d Neurosu rger y
Nancy McLaughlin, MD, PhD
Un iversit y of South Florida
Neu rosu rgeon
Tam pa, Florida
Depart m en t of Neu rosu rger y
David Geffen Sch ool of Medicin e at Un iversit y of
Jacques J Mo rco s, MD
Californ ia, Los Angeles
Professor of Clin ical Neurosurger y an d Otolar yngology
Los Angeles, Californ ia
Un iversit y of Miam i Miller Sch ool of Medicin e
Miam i, Florida
A David Mendelow , MB, BCh, FRCS (Edinburgh), PhD, FRCS
(Surgical Neuro lo g y)
Christian Musahl, MD
Professor of Neu rosu rger y
Neu rosu rgeon
Depart m en t of Neu rosu rger y
Depar t m en t of Neu rosurger y
In st it u te of Neu roscien ce
Dr. Horst Sch m idt Klin ik
New castle Un iversit y, UK
Wiesbaden , Germ any
Geo rge A C Me ndes, MD
Neu rosu rgeon Pete r Nakaji, MD
Division of Neu rological Surger y Director, Neurosurger y Residen cy Program an d Min im ally
Barrow Neu rological In st it ute Invasive Neurosurger y
St . Joseph’s Hospital an d Medical Cen ter Division of Neu rological Su rger y
Ph oen ix, Arizon a Barrow Neurological In st it ute
St . Joseph’s Hospit al an d Medical Cen ter
Fredric B Meyer, MD Ph oen ix, Arizon a
Uih lein Professor an d Ch air
Depart m en t of Neu rological Su rger y Allan Do uglas Nanney III, MD
En terp rise Ch air of Neu rosurger y Ch ief Residen t
Director of Neuroregen erat ive Medicin e Neu rosu rger y
Mayo Clin ic an d Mayo Grad u ate Sch ools Nor th w estern Un iversit y
Roch ester, Min n esot a Ch icago, Illin ois

Philip M Meyers, MD Pete r Kim Nelso n, MD


Depart m en t of Neu rological Su rger y an d Depar t m en t of Ch ief, Neuroin ter ven t ion al Ser vice
Radiology Depar t m en t s of Radiology, Neu rology an d Neurosu rger y
College of Physician s an d Surgeon s New York Un iversit y Langon e Medical Cen ter
Colu m bia Un iversit y New York, New York
Associate Professor of Radiology an d Neu rological
Su rger y Mika Niem elä, MD, PhD
Clin ical Co-Director Associate Professor, Ch airm an
Neu roen dovascu lar Ser vices Depar t m en t of Neu rosurger y
Depart m en t of Neu rosu rger y Helsin ki Un iversit y Cen t ral Hosp ital
New York, New York Helsin ki, Fin lan d

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xxxii Contributors

Eric S Nussbaum , MD Matthew B Potts, MD


Ch air, Nat ion al Brain An eu r ysm Cen ter Residen t
Joh n Nasseff Neu roscien ce In st it u te Depar t m en t of Neu rological Surger y
Min n esota Neu rovascu lar & Sku ll Base Su rger y Un iversit y of Californ ia, San Fran cisco
Tw in Cit ies, Min n esot a San Fran cisco, Californ ia

Christo pher S Ogilvy, MD Henri-Be njam in Po uleau, MD


Director, En dovascu lar an d Op erat ive Neu rovascu lar Neu rosu rgeon
Su rger y Depar t m en t of Neu rosurger y
Professor of Su rger y, Har vard Medical Sch ool Erasm e Hospit al
Director, Beth Israel Deacon ess Medical Cen ter Brain Un iversité Libre de Bru xelles
An eu r ysm In st it u te Br ussels, Belgium
Boston , Massach u set t s
Daniel M Preve dello , MD
Associate Professor
Mark E Oppe nlander, MD
Director
Neu rosu rger y Residen t
Min im ally Invasive Cran ial Surger y Program
Barrow Neurological In st it ute
Depar t m en t of Neu rological Surger y
St . Josep h’s Hosp it al an d Medical Cen ter
Th e Wexn er Medical Cen ter at Th e Oh io State
Ph oen ix, Arizon a
Un iversit y
Colum bus, Oh io
Jo shua W Osbun, MD
Fellow, Cerebrovascu lar Su rger y an d In ter ven t ion al Paulo Puglia Jr , MD, PhD
Neu roradiology Depar t m en t of Radiology
Depar t m en t of Neu rosu rger y Division of In ter ven t ion al Neu roradiology
Em or y Universit y Un iversit y of São Paulo
Atlan ta, Georgia Brazil

Do nato Pacio ne, MD Alejandro A Rabinste in, MD


Assistan t Professor Professor of Neu rology
Depar t m en t of Neu rosu rger y Medical Director, Neuroscien ce ICU
New York Un iversit y Langon e Medical Cen ter Depar t m en t of Neu rology
New York, New York Mayo Clin ic
Roch ester, Min n esot a
Vince n zo Pate rno , MD
Associate Neurosurgeon Leo nardo Rangel-Castilla, MD
Depar t m en t of Neu rosergy Cerebrovascu lar/Skull Base Fellow
In tern at ion al Neuroscien ce In st it u te—Han over Division of Neu rological Su rger y
Han n over, Germ any Barrow Neurological In st it ute
St . Joseph’s Hospit al an d Medical Cen ter
Ph oen ix, Arizon a
Marta Aguilar Perez, MD
Neu rosu rgeon
Eytan Raz, MD
Depar t m en t of Neu roradiology
Clin ical In st ru ctor
Kath arin en h osp ital
Depar t m en t of Radiology, Sect ion of Neuroradiology
St u t tgar t , Germ any
New York Un iversit y Langon e Medical Cen ter
New York, New York
Luis Pérez-Orribo, MD
Fellow Luca Regli, MD
Division of Neu rological Su rger y Professor an d Director
Barrow Neurological In st it ute Depar t m en t of Neu rosurger y
St . Josep h’s Hosp it al an d Medical Cen ter Un iversit y Hosp ital Zurich
Ph oen ix, Arizon a Zu rich , Sw it zerlan d

Maria Pe ris-Celda, MD, PhD Matthew R Reyno lds, MD, PhD


Research Fellow Ch ief Residen t
Depar t m en t of Neu rological Su rger y Depar t m en t of Neu rological Surger y
Un iversit y of Florida Wash ington Un iversit y in St . Louis
Gain esville, Florida St . Lou is, Missouri

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Contributors xxxiii

Albert L Rhoto n, Jr , MD Sean I Savitz, MD


Professor an d Ch airm an Professor
Depart m en t of Neu rosu rger y Depar t m en t of Neu rology
Un iversit y of Florida Fran k M. Yat su , MD Ch air in Neu rology
Gain esville, Florida Depar t m en t of Neu rology
Director
How ard A Riina, MD Vascu lar Neu rology Program & Fellow sh ip
Professor an d Vice Ch airm an Depar t m en t of Neu rosurger y
Depart m en t of Neu rosu rger y Un iversit y of Texas Health Scien ce Cen ter at Houston
New York Un iversit y Sch ool of Medicin e Hou ston , Texas
New York Un iversit y Langon e Medical Cen ter
New York, New York Clem ens M Schirm e r, MD
Neu rosu rgeon
Ana Ro dríguez-He rnández, MD Neu rological Su rger y
Neu rosu rgeon , At ten d ing Baystate Health
Depart m en t of Neu rological Su rger y Springfield, Massach uset t s
Vall d’Hebron Un iversit y Hospit al
Barcelon a, Spain Jo hannes Schram m , MD, PhD
Professor Em erit u s
Ro ssana Ro m ani, MD, PhD Deapar t m en t of Neu rosu rger y
Adju n ct Professor of Neu rosu rger y Medical Facu lt y
Un iversit y of Helsin ki Bon n Un iversit y
Depart m en t of Neu rosu rger y Bon n , Germ any
Qu een’s Hosp ital
Albe rt J Schuette, MD
Bar ts an d Th e Lon d on
Neu rosu rgeon
Qu een Mar y’s Sch ool of Medicin e an d Den t ist r y
Depar t m en t of Neu rosurger y
Un iversit y of Lon don
Em or y Un iversit y
Lon don , Englan d, Un ited Kingdom
Atlan ta, Georgia
Ro bert Ro se nw asse r, MD, FACS, FAHA
Laligam N Sekhar, MD, FACS, FAANS
Jew ell Osterh olm Professor an d Ch airm an ,
William Joseph Leedom an d Ben n et t Bigelow & Leedom
Depart m en t of Neu rological Su rger y
Professor
Th om as Jefferson Un iversit y
Vice Ch airm an
Ph ilad elp h ia, Pen n sylvan ia
Director of Cerebrovascu lar Surger y
Director of Skull Base Su rger y
Pablo Rubino, MD
Harbor view Medical Cen ter
Ch ief of Cerebrovascu lar Sect ion an d
Un iversit y of Wash ington
Vice- Ch airm an of Depar t m en t of Neu rosu rger y, Hospital El
Seat tle, Wash ington
Cru ce, Provin cia de Bu en os Aires, Argen t in a
Maksim Shapiro , MD
Jo nathan J Russin, MD Assistan t Professor
Assistan t Professor an d Assistan t Su rgical Director Bern ard an d Iren e Sch w ar t z In ter ven t ion al
Cen ter for Neu rorestorat ion Neu roradiology Sect ion
Depart m en t of Neu rological Su rger y Depar t m en t s of Radiology an d Neu rology
Un iversit y of South ern Californ ia New York Un iversit y Sch ool of Medicin e, New York Un iversit y
Los Angeles, Californ ia Langon e Medical Cen ter
New York, New York
Ro bert W J Ryan, MD, MSc, FRCSC
Assistan t Clin ical Professor Vilaas Shetty, MD
Division of Neu rosurger y Assistan t Professor of Radiology
Un iversit y Neurosu rger y Associates Depar t m en t of Radiology, Neuroradiology Division
Un iversit y of Californ ia, San Fran cisco, at Fresn o Sain t Lou is Un iversit y Sch ool of Medicin e
Fresn o, Californ ia Sain t Lou is, Missou ri

Duke S Sam so n, MD Adnan H Siddiqui, MD, PhD


Professor Em erit u s Professor an d Vice- Ch airm an
Neu rological Su rger y Depar t m en t of Neu rosurger y
Un iversit y of Texas Sou th w estern Un iversit y at Bu ffalo, th e State Un iversit y of New York
Dallas, Texas Bu ffalo, New York

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xxxiv Contributors

Matthias Sim o n, MD Justin M Sw e eney, MD


Associate Professor Neu rosu rgeon
Neu roch irurgisch e Klin ik Neu rosu rgical Specialist s of West Cou n t y
Un iversitätsklin iken Bon n St . Lou is, Missouri
Bon n , Germ any
Pekka O Talke, MD
Paul Singh, MD, MPH Professor of An esth esiology
Assistan t Professor An esth esia/Periop erat ive Care
Neu roEn dovascu lar Surger y & Vascu lar Neu rology Sch ool of Medicin e
Neu rological In st it u te of New Jersey Un iversit y of Californ ia, San Fran cisco
New ark, New Jersey San Fran cisco, Californ ia

Ke nneth V Snyder, MD, PhD Rafael J Tam argo, MD, FAANS, FACS
Assistan t Professor Walter E. Dan dy Professor of Neu rosurger y
Depar t m ent s of Neu rosu rger y, Radiology an d Neu rology Director, Division of Cerebrovascular Neurosu rger y
St ate Un iversit y of New York at Bu ffalo Vice- Ch airm an , Depar t m en t of Neurosu rger y
Bu ffalo, New York Neu rosu rger y Co-Director, Neu roscien ces Crit ical
Care Un it
Depar t m en t of Neu rosurger y
Ro bert So lo m o n, MD
Th e Joh n s Hopkin s Un iversit y Sch ool of Medicin e
Byron Stookey Professor an d Ch airm an
Balt im ore, Mar ylan d
Depar t m ent of Neu rological Su rger y
Colu m bia Un iversit y College of Physician s an d Surgeon s
Farzana Tariq, MD
New York Presbyterian Hospit al
Depar t m en t of Neu rosurger y
New York, New York
Wayn e St ate Un iversit y
Det roit , Mich igan
Scott G So ltys, MD
Assistan t Professor
Philipp Taussk y, MD
Depar t m ent of Radiat ion On cology
Assistan t Professor
St an ford Un iversit y
Division Ch ief, En dovascular Neurosurger y
St an ford, Californ ia
Un iversit y of Utah
Salt Lake Cit y, Ut ah
Grant C So rkin, MD
Neu rosu rgeon Rabih G Taw k, MD
Roch estor Region al Health System Assistan t Professor
Th e Maxw ell Boev Clin ic Depar t m en t of Neu rosurger y
Roch ester, New York Mayo Clin ic Florida
Jacksonville, Florida
Ro bert F Spetzle r, MD
Director, Barrow Neu rological In st it ute Mo ham e d Teleb, MD
J. N. Harber Ch airm an Neu roin ter ven t ion al Su rger y
Professor of Neu rological Surger y St roke an d Neurocrit ical Care Physician
Division of Neu rological Su rger y Neu rology
Barrow Neurological In st it u te Ban n er Health
St . Josep h’s Hospit al an d Medical Cen ter Ph oen ix, Arizon a
Ph oen ix, Arizon a
Charles Te o, MBBS, FRACS
Gary K Steinbe rg, MD, PhD Director
Bern ard and Ron n i Lacrou te-William Ran dolph Hearst Cen t re for Min im ally Invasive Neu rosu rger y
Professor of Neurosu rger y an d th e Neu roscien ces Prin ce of Wales Hospital
Ch airm an , Dep ar t m en t of Neu rosu rger y Sydn ey, New Sou th Wales, Au st ralia
St an ford Un iversit y Sch ool of Medicin e
St an ford, Californ ia Stavro po ula I Tjo um akaris, MD
Assistan t Professor
Do uglas L Sto fko , DO Associate Program Director
Cerebrovascu lar Fellow Fellow sh ip Director, En dovascu lar Su rger y an d
Neu rosu rger y Cerebrovascu lar Neurosu rger y
Cap ital In stit u te for Neu roscien ces Th om as Jefferson Un iversit y Hospit al
Tren ton , New Jersey Ph iladelph ia, Pen n sylvan ia

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Contributors xxxv

Cornelis A F Tulleke n, MD, PhD Michael J Wang, MD


Neu rosu rgeon Clin ical Assistan t Professor
Depart m en t of Neu rosu rger y Depar t m en t of Neu rology
Rudolf Magn u s In st it u te of Neu roscien ce Un iversit y of Nor th Carolin a- Ch ap el Hill
Un iversit y Medical Cen ter Ut rech t Ch apel Hill, Nor th Carolin a
Ut rech t , Th e Neth erlan ds
Ke ntaro Watanabe, MD
Michael Tym ianski, MD, PhD, FRCSC Fellow
Head, Division of Neu rosu rger y Depar t m en t of Su rger y
Un iversit y of Toron to Division of Neu rosu rger y
Un iversit y Health Net w ork Du ke Un iversit y
Sen ior Scien t ist In tern at ion al Neurosurger y Edu cat ion an d Research
Toron to Western Research In st it u te Fou n dat ion
Toron to Western Hosp ital Du rh am , Nor th Carolin a
Toron to, On tario, Can ada

Cristian Valdes-Whittle, MD Claudia Weissbach, MD


Neu rosu rgeon Fellow of Cerebrovascu lar Su rger y Neu rosu rgeon
Depart m en t of Neu rosu rger y Depar t m en t of Neu rosurger y
In st it u te of Neu rosu rger y Asenjo Klin iku m St u t tgar t
San t iago, Ch ile St ut tgar t , Germ any

Albert van der Zw an, MD Babu G Welch, MD, FAANS


Neu rosu rgeon Associate Professor of Neurosurger y an d Radiology
Rudolf Magn u s In st it u te of Neu roscien ce Th e Un iversit y of Texas South w estern Medical Cen ter
Depart m en t of Neu rosu rger y Dallas, Texas
Un iversit y Medical Cen ter Ut rech t
Ut rech t , Th e Neth erlan ds William L White, MD, FACS
Ch ief of Surgical En docrin ology
Harry R van Love ren, MD, FAANS
Division of Neu rological Su rger y
Professor an d Ch airm an
Su rgical Director, Barrow Pit uitar y Cen ter
Depart m en t of Neu rological Su rger y
Barrow Neurological In st it ute
Th e Un iversit y of South Florida
St . Joseph’s Hospit al an d Medical Cen ter
Tam pa, Florida
Ph oen ix, Arizon a
Aw ais Z Vance, MD
First Year Residen t Shaw n Eugene Wright, MD
Depart m en t or Neu rological Su rger y Lu ng Can cer an d In ter ven t ion al Pu lm on ology
Brow n Un iversit y Alper t Medical Sch ool Arizon Pulm on ar y Specialists Ltd.
Providen ce, Rh ode Islan d Ph oen ix, Arizon a

Ero l Veznedaro glu, MD, FAANS, FACS, FAHA Bülent Yapicilar, MD


Ch airm an , Dep ar t m en t of Neu rosu rger y Assistan t Professor
Director, Capital In st it u te for Neu roscien ces Neu rosu rger y
St roke an d Cerebrovascu lar Cen ter of New Jersey Met ro Health Medical Cen ter
Ch ief, Cerebrovascu lar an d En dovascu lar Neu rosurger y Case Western Reser ve Un iversit y
Capital Health System Clevelan d, Oh io
Capital In st it u te for Neuroscien ces
Pen n ington , New Jersey
Jack y T Yeung, MD
Residen t , Neu rosu rger y
Christian vo n der Brelie, MD
Yale Sch ool of Medicin e
Neu rosu rgeon
New Haven , Con n ect icu t
Depart m en t s of Neu rosu rger y an d Ep ileptology
Un iversit y of Bon n Medical Cen ter
Bon n , Germ any Yasuhiro Yo nekaw a, MD
Professor Em erit u s
Brian P Walcott, MD Un iversit y of Zü rich
Rober t G. an d A. Jean Ojem an n Professor of Neu rosu rger y Zü rich , Sw it zerlan d
Har vard Medical Sch ool Con sultan t Neurosu rgeon
Massach u set ts Gen eral Hospit al Klin ik im Park, Zü rich an d Kan ton sspit al
Boston , Massach u set t s Aarau , Sw it zerlan d

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xxxvi Contributors

A Sam y Youssef, MD Gre go ry J Zipfel, MD


Associate Professor, Neu rosu rger y Associate Professor an d Program Director
Director of Skull Base Su rger y Depar t m en t of Neu rological Surger y
Un iversit y of Colorado Neu rosu rger y Wash ington Un iversit y Sch ool of Medicin e
Denver, Colorado St . Lou is, Missouri

Scott L Zuckerm an, MD


Jo seph M Zabram ski, MD
Residen t
Professor of Neu rological Surger y
Depar t m en t of Neu rosurger y
Ch ief, Sect ion of Cerebrovascular Su rger y
Van derbilt Un iversit y Medical Cen ter
Barrow Neurological In st it ute
Nashville, Ten n essee
St . Josep h’s Hosp ital an d Medical Cen ter
Ph oen ix, Arizon a
Daniel W Zum o fe n, MD
In tern at ion al Neuroradiology Fellow
Hasan A Zaidi, MD Sect ion of Neuroin ter ven t ion al Radiology
Neu rosu rger y Residen t Depar t m en t of Radiology
Barrow Neurological In st it ute New York Un iversit y Sch ool of Medicin e
St . Josep h’s Hosp ital an d Medical Cen ter New York Un iversit y Langon e Medical Cen ter
Ph oen ix, Arizon a New York, New York

Neurosurgery Books Full


I Development, Anatomy, and Physiology
of the Central Nervous System

Neurosurgery Books Full


Neurosurgery Books Full
1 Development of the Cerebrovasculature
Zam an Mirzadeh and Robert F. Spetzler

Aristotle (384–322 BC) is cited as th e earliest source to describe tion s, fenest rat ions, hypoplasia, rare anastom oses, redun dant vas-
th e com m on effect of com p ression of both carot id ar teries.1 Al- cular supply w ith prom iscuous territories, an d th e respon se of
th ough alm ost 500 years w ou ld p ass before th e Greek p hysician the vasculat ure to diverse int rinsic and extrinsic diseases. Despite
Galen (129–199 AD) est ablish ed th at ar teries con t ain blood an d t h is seem in gly over w h elm in g var iabilit y in t h e en d p rod u ct ,
n ot air,2 Aristotle’s sem in al obser vat ion h ad already suggested t h e h u m an cerebrovascu lat u re h as a com m on origin an d devel-
th at t h e brain dep en d s on th e great vessels in th e n eck to fu n c- opm en tal progression . An un derstan ding of th is developm en tal
t ion . Desp ite th ese early in sigh t s, it w as n ot u n t il th e Eu ropean progression len ds sign ifican ce to th ese an atom ic variat ion s an d
Ren aissan ce (14th to 17th cen t u ries) th at at tem pts w ere m ade to u lt im ately m ay sh ed ligh t on t h e p ath ophysiology of cert ain
delin eate th e st ru ct u ral elem en t s of th e h u m an vascu lar system . cerebrovascular diseases an d lead to n ovel th erapies.
From 1504 to 1506 th e ar t ist an d scien t ist Leon ardo da Vin ci
(1452–1519) produ ced several detailed an atom ic draw ings, in -
clu ding depict ion s of th e carot id ar teries in th e n eck, based on
dissect ion s of an im als an d a rigorou s st u dy of a 100-year-old ■ Evolutionary Perspective on
h um an .1,3 Later, th e an atom ist An dreas Vesaliu s (1514–1564)
provided th e first system at ic st u dy of th e h u m an vascu lar sys-
Cerebrovascular Development
tem based on both an im al an d h u m an dissect ion s in h is m aster- In asm uch as on togeny recapit ulates phylogeny, un derst an ding
w ork, De Hum ani Corporis Fabrica (1543).1 Alth ough th ese an a- cerebrovascu lar d evelop m en t m ay be facilit ated by review ing
tom ic st udies provided an im proved roadm ap for th e vascular th e evolu t ion of th e cerebrovascu lar t ree. Tw o gu iding prin cip les
n et w ork, un derstan ding of blood flow st ill relied on th e galen ic u n derlie m uch of vascular evolu t ion ar y adapt at ion th at occurs
system , w h ich p roposed th at blood w as delivered to th e en d or- as n er vous system com plexit y in creases. First , th e basic blue-
gan s th rough both ar teries an d vein s. prin t of th e n eu rovascu lar n et w ork is on e of t ran sversely ori-
It w as n ot un t il 1628, w h en William Har vey (1578–1657) en ted vessels con n ected by longit u d in al on es.6 Th is p at tern is
pu blish ed h is revolu t ion ar y fin dings in Exercitat io Anatom ic de best appreciated in th e developing n eural t ube an d spin al cord,
Mot u Cardis et Sanguinis in Anim alibus (Anatom ical Essay on the w h ere segm en tal or m et am eric vessels arising from th e dorsal
Mot ion of the Heart and Blood in Anim als), th at ou r m odern u n - aor t a su p p ly adjacen t segm en t s of t h e cord . As d evelop m en t
derstan ding of blood circu lat ion w as establish ed.3,4 Th e accep - pro ceeds, longit u d in al an astom oses are establish ed bet w een ad-
tance of Harvey’s concept of the circulation led to further advances jacen t segm en tal vessels, form ing n ew rost rocau dally orien ted
in th e un derstan ding of vascu lar an atom y. For exam ple, details ch an n els th at p rovide redun dan t sup ply in th e direct ion parallel
regarding th e ou tflow of th e carot id arteries w ere provided by to the neuraxis (e.g., anterior spinal arter y). This developm ental
th e w ork of th e Lon don p hysician Th om as Willis (1621–1675), pat tern dim in ish es th e h em odyn am ic n eed for segm en tal ves-
for w h om th e an astom ot ic circle at th e skull base is n am ed, in h is sels at ever y level an d en ables som e of th ese vessels to regress.
Cerebri Anatom e Nervorum que (1664).3 In terest ingly, Willis w as Secon d, as n ew cerebral territories em erge in evolu t ion , th ere is
n ot th e first to describe th e circle, but he w as th e first to do so in progressive recru it m en t of exist ing vascu lar n et w orks to su pp ly
su ch great det ail. Gabr iel Fallop iu s (1523–1563), after w h om th e em erging territories, rath er th an de n ovo ar terial solu t ion s.5,7
t h e fallopian t u bes are n am ed, h ad provided an in com p lete de- Th is p rin ciple is exem p lified by th e p rogressive ram ificat ion of
script ion in 1561. Giu lio Casserio (1561–1616), after w h om th e cerebral vessels th rough evolut ion from fish to h um an s, as de-
gasserian ganglion is n am ed, w as th e first to draw th e circle. Ger- scribed in detail below (Fig. 1.1).
m an an atom ist Joh an n Vesling (1598–1649) also described th e Fish h ave a prim itive cerebellum , a p rim it ive th ree-layer cor-
circle in 1653, as did Sw iss path ologist Joh an n Jakob Wepfer tex th at is th e predecessor of th e h ippocam pu s, a h igh er m ove-
(1620–1695) in 1658 in h is classic t reat ise on st rokes, Historiae m en t cen ter th at is th e predecessor of th e basal ganglia, an d a
Apoplect icorum .5 Fin ally, th e develop m en t of cerebral angiogra- sm all bu t effect ive olfactor y lobe. Tw o large longit u din al vessels,
phy by Por t ugu ese n eu rologist Egas Mon iz, as d iscu ssed in h is th e carot id ar teries, ascen d in th e n eck an d en ter th e cran ial cav-
classic w ork L’Angiographie Cerebrale (1934), enabled radiographic it y; each gives rise to paired longit udin al vessels th at run th e
evalu at ion of th e carot id ar ter y an d in t racran ial vasculat u re in length of th e brain .5,6 Th e carot id bran ch project ing rost rally,
living p at ien ts.3 Th is revolut ion in cerebrovasculat ure im aging called th e cran ial ram us, is th e predecessor of th e an terior cere-
provided an u nparalleled view of th e vascu lar t ree in act ion . bral (ACA) an d m iddle cerebral (MCA) ar teries. In fish , th e cran ial
More th an any p rior an atom ic st u dy, th e rou t in e use of cere- ram u s h as t w o bran ch es: t h e m ed ial olfactor y ar ter y, w h ich
bral angiography dem on st rated th e t rem en dou s in terin dividual is t h e p red ecessor of th e ACA, an d t h e lateral olfactor y ar ter y,
var iabilit y in t h e cerebrovascu lat u re, in clu d ing vessel d u p lica- w h ich is th e predecessor of th e recurren t ar ter y of Heubn er an d

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4 I Development, Anatomy, and Physiology of the Central Nervous System

Fig. 1.1 Evolution of the cerebrovasculature from fish to hum ans. Pro- choroidal artery); PChA, posterior choroidal artery; RH, recurrent artery of
gressive enlargem ent of the brain, in particular the cerebral hem ispheres Heubner; ACA, anterior cerebral artery; CranR, cranial ram us of ICA; CaudR,
and cerebellum , drive hypertrophy and increased ramification of the cere- caudal ram us of ICA; TA, tectal artery (future PCA, posterior cerebral ar-
bral vessels. The vascular tree has been color-coded according to the origin tery); CbA, cerebellar artery (future SCA, superior cerebellar artery); BA,
of the vessels: the internal carotid artery (ICA) is red, the cranial ram us of basilar artery (fused caudal ram i); PICA, posterior inferior cerebellar artery;
the ICA and its branches are in green, the caudal ram us and its branches are VA, vertebral artery; C-VAn, segmental carotid-vertebral anastom oses; and
in blue, and the vertebral artery system is orange. MOA, m edial olfactory AICA, anterior inferior cerebellar artery. (Adapted with perm ission from
artery; LOA, lateral olfactory artery; LSA, lateral striate artery; LSP, lateral Maksim Shapiro, ht tp://neuroangio.org/neurovascular-evolution/.)
striate perforators; PT, posterior telencephalic artery (future AChA, anterior

an terior ch oroidal ar ter y. Th e carot id bran ch project ing caudally, evolut ion , essen t ially th e en t ire brain , in clu ding th e prosen ceph -
called th e cau dal ram u s, is th e p redecessor of th e p osterior com - alon an d cerebellum , is supp lied by th e carot id ar teries.
m un icat ing arter y (PCoA) an d th e top of th e basilar arter y (BA), In am ph ibian s, th e brain h as grow n larger; th ere is a prim it ive
w h ich is already fu sed at m idlin e. Th e caudal ram us elaborates a h ipp ocam pu s an d en larging basal ganglia as w ell as a larger cer-
tectal ar ter y th at supplies th e posterior top of th e brain stem an d ebellum . Th is in creased dem an d for perfusion result s in hyper-
a cerebellar ar ter y, w h ich is th e p redecessor of th e superior cer- t rop hy of som e bran ch es arising from already exist ing ch an n els
ebellar ar ter y. Im p or tan tly, th ere is n o physiologically sign ifican t and coalescence of sm aller perforators into larger nam ed branches.
an astom osis bet w een t h e cau dal ram u s an d t h e sp in al cord / Th e hyp er t rop h ied lateral olfactor y ar ter y n ow h as t w o m ain
ver tebral arter y system s at th is stage.6 How ever, proxim al to th e bran ch es: th e lateral st riate ar ter y, w h ich is th e predecessor to
bifurcat ion of th e carot id ar ter y in to cran ial an d caudal ram i, th e recu rren t ar ter y of Heu bn er an d th e MCA, an d th e p osterior
th ere are ver y sm all segm en t al an astom oses bet w een th e ca- telencephalic artery, w hich is the predecessor to the anterior cho-
rotid arter y an d th e vertebral system , th e carotid-vertebrobasilar roidal artery.5,6 On th e caudal carot id ram us, th e tectal/cerebellar
an astom oses, w h ich are fu r th er discussed below. At th is st age in com p lex elaborates th e p osterior ch oroidal ar ter y to su pp ly th e

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1 Development of the Cerebrovasculature 5
develop ing ch oroid p lexu s. Th ere are st ill n o sign ifican t an asto- gioblast s, w h ich d evelop in to flat ten ed en d oth elial cells. Th e
m oses bet w een th e cau dal carot id an d ver tebral system s. en doth elial cells join togeth er to form sm all vesicular st r uct ures
In rept iles, t h e lateral st r iate bran ch of t h e an ter ior d ivision called angiocyst s, w h ich in t u rn coalesce in to long t u bes or ves-
p rod u ces m u lt ip le p er forator vessels su p p lying t h e en larging sels called angioblast ic cords. In terest ingly, quail-ch ick ch im era
h em isph ere.5,6 Th ese perforators even t u ally becom e p ar t of th e exp erim en t s in w h ich m esoderm is t ran splan ted from on e re-
MCA. At m idlin e, fu sion of th e m edial olfactor y ar teries is ob - gion in th e qu ail to an oth er region in th e ch ick sh ow th at th e
ser ved in som e rept iles an d rep resen ts th e p rim it ive an terior ch aracterist ic bran ch ing p at tern of blood vessels in each region
com m u n icat ing ar ter y (ACoA). Th e p osterior telen cep h alic ar ter y is determ in ed by cues from th e u n d erlying en doderm an d it s ex-
has also en larged an d supplies the posterior cerebral h em isph ere, t racellu lar m at rix.9 Th at is, th e h ost site determ in es th e bran ch -
w h ich it w ill con t in ue to do un t il late in evolut ion w h en th is ter- ing p at tern of blood vessels form ed from th e don or m esoderm
ritor y is an n exed by th e p osterior cerebral ar ter y (PCA). At th is t issu e, n ot vice versa. Th rough th is p rocess, a pair of longit u di-
st age, th e PCA p redecessor, th e tectal ar ter y, sup plies a sm aller n ally directed ch ann els arises in a param edian locat ion to ult i-
territor y also involved in visual processing. Fin ally, th e en larging m ately becom e th e dorsal aor t ae.
cerebellum , part icularly its caudal verm ian por t ion , is supplied Bet w een E21 an d E25, th e en docardial t ubes fuse in to a prim -
from th e dist al (cau dal) BA (st ill w ith in th e in tern al carot id ar- it ive h eart , an d th e aor t ic sac becom es con n ected to th e dorsal
ter y t ree), by th e h om ologue of th e posterior in ferior cerebellar aor tae.3,9 Su bsequ en tly, em br yon ic folding carries th e en docar-
ar ter y (PICA).6 dial t u bes in to th e ven t ral th ora x, an d th e p aired dorsal aor tae
Th e rise of birds coin cides w ith th e em ergen ce of a d iscrete at tach ed to th e cran ial en ds of th e t u bes are p u lled ven t rally to
MCA from a dom in an t perforator am ong th e lateral st riate ves- for m a pair of d orsoven t ral loop s rep resen t ing t h e first aor t ic
sels, again driven by rap id expan sion of cor t ical volu m e.5,6 A arch es. Du r ing th e fou r t h an d fift h em br yon ic w eeks, fou r ad-
dom in an t p erforator also can be dist ingu ish ed in th e ACA terri- d it ion al pairs of aor t ic arch es (2, 3, 4, an d 6) d evelop in cran io -
tor y, w h ich is an alogous to th e recu rren t ar ter y of Heubn er. The cau dal succession , con n ect ing th e aor t ic sac at th e su p erior en d
posterior telen cep h alic or an terior ch oroidal ar ter y con t in u es to of th e t run cus ar teriosus to th e dorsal aor tae. Th e dorsal aor t ae
be th e dom in an t supply for th e pariet al-occipital region , but it rem ain sep arate in t h e region of t h e aor t ic arch es, bu t d u r ing
n ow h as a fu n ct ion al an astom osis w ith th e tect al ar ter y, w h ich t h e fou r th w eek t h ey fu se toget h er from t h e fou r t h t h oracic
h as exten d ed it s ter r itor y an d w ill u lt im ately acqu ire th e ter- segm en t to th e four th lum bar segm en t to form a single m idlin e
r itor y of th e PCA. Th e vertebral system rem ain s con fin ed to th e dorsal aor ta.9 By E32, five pairs of aor t ic arch es (1, 2, 3, 4, an d 6)
spin al cord w ith ou t fun ct ion al an astom osis to th e carot id sys- have form ed,3 coursing around to vascularize five branchial arches.
tem , w h ich con t in u es to p rovide th e sole sup p ly for th e brain . In h um an s, the fifth bran ch ial arch n ever develops at all or ap -
In th e t ran sit ion from birds to m am m als, th e en larging cere- pears briefly an d th en regresses, explain ing th e absen ce of aor t ic
bellum an d posterior telen ceph alon place in creasing dem ands arch 5.
on th e caudal ram us of th e carot id system . St ill, th e carot id sys- Th e first th ree aor t ic arch es are presen t by E28, bu t th e first
tem m eet s th is in creased dem an d in m am m als as evolut ion arily t w o arch es involu te before form at ion of th e fou r th an d sixth ;
advan ced as sh eep an d dogs, w h ich con t in ue to dem on st rate con sequen tly, n ot all th e arch es are presen t togeth er at any on e
cran iopet al flow in th e BA.5,6 How ever, in fu rth er evolved m am - t im e.10 Sp ecifically, th e secon d aor t ic arch arises in th e secon d
m als, th e carot id system fin ally reach es it s physiological lim it , ph ar yngeal (bran ch ial) arch by E26. Sim u ltan eou sly, th e first pair
an d th e ver tebral system progressively an n exes th e basilar terri- of aor t ic arch es regresses com p letely, except for sm all rem n an t s
tor y, star t ing first w ith th e PICA territor y an d u lt im ately in clu d- th at m ay give rise to por t ion s of th e m axillar y ar teries.8 On E29,
ing th e en t ire brain stem an d cerebellu m . Th is ch ange resu lts in th e secon d p air of arch es regresses except for a sm all rem n an t
a reversal of caudally directed flow in th e BA to th e rost rally di- th at gives rise to par t of th e stapedial ar ter y,8 w h ich supplies th e
rected flow obser ved in m on keys, apes, an d h u m an s.6 prim ordiu m of th e stapes bon e in th e developing ear. Briefly, th e
Hu m an s, in p ar t icu lar, rep resen t t h e fu r t h est an ter ior ex- third aortic arch develops into th e com m on carot id arteries (CCAs)
p an sion of t h e ver tebrobasilar ter r itor y to in clu d e t h e PCA, p re- an d in tern al carot id ar teries (ICAs) (discussed in detail below ).
viou sly kn ow n as th e tectal arter y an d developm en tally com plete Th e fou r th an d sixth arch es u n dergo asym m et ric rem od eling to
w ith in th e carot id ar ter y circu lat ion . In terest ingly, th e presen ce su p ply blood to th e u p per ext rem ities, dorsal aor t a, an d lu ngs.
of a fetal PCoA varian t (u p to 25%of cases) 8 is eviden ce of th e st ill Th e left fou r th arch rem ain s in con t in u it y w ith th e aor t ic sac an d
ten uous acqu isit ion of th e PCA territor y by th e ver tebrobasilar th e m idlin e fu sed d orsal aor t a to form th e defin it ive adu lt aor t ic
system . Th is an d oth er varian ts of th e cerebrovascu lat u re h igh - arch , w h ereas th e righ t fou r th arch loses it s con n ect ion w ith th e
light the im portance of understanding both the phylogenetic and fu sed m id lin e aor t a an d , toget h er w it h p ar t of t h e r igh t d orsal
developm en t al origin s of th e cerebral blood su p ply. aor t a, for m s t h e p roxim al r igh t su bclavian ar ter y. Fin ally, t h e
sixt h arch es con t r ibu te to t h e p u lm on ar y ar ter ies an d d u ct u s
ar teriosus.3,9

■ Development of the Large Vessels


The Carotid Arteries
Aortic Arches and the Great Vessels of the Neck Th e carot id ar teries form as a resu lt of involu t ion of th ree sep a-
In h um an s, vasculogen esis begin s on em br yon ic day 18 (E18) in rate arterial segm en t s: th e first t w o aor t ic arch es an d th e seg-
th e splan ch n op leu ric m esoderm of th e em br yon ic disk.9 In du c- m en t of th e dorsal aorta con n ect ing th e th ird an d fourth aort ic
ing factors secreted by th e u n derlying en doderm cau se som e arch ar teries, called t h e d u ct u s carot id u s.3 In it ially, blood flow
cells of th is prim it ive spongy m esoderm to differen t iate in to an - to th e cran ial region is from t h e ven t ral aort ic sac to th e dorsal

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6 I Development, Anatomy, and Physiology of the Central Nervous System

aor ta th rough th e first t w o aor t ic arch es. How ever, by E29 th e an d p oster ior ch oroidal ar ter ies. Fin ally, t h e ch oroid p lexu s of
first t w o arch es h ave regressed. By E35, th e du ct u s carot icu s h as t h e fu t u re fou r t h ven t r icle is su p p lied by a d om in an t feed er
also regressed. At th is stage, th e cran ial exten sion s of th e dorsal bran ch ing off th e basilar/longit udin al n eural ar teries, w h ich ul-
aor t ae su p p lyin g t h e h ead are p er fu sed en t irely via t h e t h ird t im ately becom e th e PICA.
arch . Th e th ird arch ar teries becom e th e righ t an d left com m on During w eeks 6 an d 7 of em br yon ic developm en t , th e longi-
carot id ar teries an d th e p roxim al p or t ion of th e ICAs, w ith th eir t u d in al n eu ral system con t in u es to m at u re. Th e bilateral lon gi-
dist al p or t ion being der ived from th e cran ial exten sion s of th e t u din al n eu ral ar teries at th e ven t ral rh om ben cep h alon fu se to
dorsal aor tae. form th e m idlin e BA, w h ereas m ore cau dally at th e level of th e
The external carotid artery (ECA) develops from a direct branch sp in al cord , t h ese vessels fu se to form th e an ter ior sp in al ar-
off th e aort ic sac, called th e ven t ral p h ar yngeal ar ter y, w h ich ter y.5,7 Th e ver tebral ar teries (VA) form as lon git u d in al an asto-
perfuses th e first an d secon d ph ar yngeal arch es.3 Rapid descen t m oses bet w een cer vical in tersegm en t al ar teries lateral to th e
of th e h ear t at approxim ately E40 results in th e m igrat ion of th e sp in al cord an d t h en join t h e p roxim al en d of t h e BA an d lon gi-
origin of th e ECA from th e aor t ic sac upw ard for a variable dis- t u din al n eu ral system .9 Subsequ en tly, th e ver tebrobasilar system
tan ce along th e th ird arch . Th is m igrat ion accou n ts for th e site of begins to m eet the dem ands of the brainstem and cerebellum and
th e carot id bifu rcat ion in th e n eck an d for th e th ird arch ser ving progressively an n exes th is vascu lar territor y from th e PCoA.5,11
as p recu rsor to segm en ts of both th e CCAs an d ICAs. Th e fin al an d m ost ten u ou s acqu isit ion of th e posterior circu la-
t ion , as discu ssed above, is th e su pply of th e PCA territor y, w h ich
d evelopm en t ally an d p hylogen et ically is am ong t h e n ew est of
Major Cerebral Arteries
th e cerebral vessels. An app reciat ion for th ese develop m en t al
At E24, t h e p r im ord ia of t h e p oster ior circu lat ion are fou n d in sh ift s in vascu lar ter ritor y is im por t an t for u n derst an ding vas-
a p lexu s of vessels obser ved along t h e ven t ral su r face of t h e cu lar variat ion an d p ath ology, as discu ssed below.
rh om ben cep h alon . Th ese vessels coalesce to form bilateral longi-
t u din al n eu ral ar teries, th e p redecessors of th e BA.3,5,11 Con cur-
Cerebral Venous System
ren tly, a bran ch exten ds off th e dorsal aor ta at th e first aor t ic
arch an d t ravels dorsally to th e region of th e t rigem in al ganglion , In it ially, th e ven ous system appears at E26 to E28 in th e form of
w h ere it form s an an astom osis w ith th e longit udin al n eu ral ar- a t ran sien t m idlin e vessel in th e h in dbrain region .12 By E32, bi-
ter y. Th is bran ch , called th e t rigem in al ar ter y, t ran sien tly p ro- lateral ven ou s ch an n els called th e an terior card in al vein s em erge
vides th e m ain blood su p ply to th e rh om ben cep h alon . Later, as an d provide th e first defin itive drain age system from th e dural
th e cran ial en d of th e dorsal aor t a is in corp orated in to th e dist al cap illar y plexu ses.9,11 Th ree dural plexuses h ave been described
ICA, th e t rigem in al ar ter y becom es a bran ch of th e ICA. Mult ip le at this developm ental stage: the anterior dural plexus drains both
sm aller an astom oses bet w een th e ICA system an d th e longit u di- th e telen cep h alon an d th e m esen ceph alon , t h e m iddle du ral
n al n eu ral ar teries su pp lem en t th e t rigem in al ar ter y, inclu ding p lexu s drain s th e m eten cep h alic region (in clu ding t h e fu t u re
th e first cer vical in tersegm en t al, hyp oglossal, an d ot ic ar teries. cerebellum ), an d th e posterior dural plexu s drain s th e m yelen ce-
Togeth er, th ese an astom oses provide th e prim ar y blood supply ph alic region .12 Th e prim ar y h ead vein s drain ing th ese plexuses
to th e rh om ben cep h alon bet w een E24 an d E29. are t ribut aries of th e an terior cardin al vein s, w h ich later becom e
By E29, th e distal ICA h as divid ed in to cran ial an d cau dal th e in ter n al jugu lar vein s.11 Ot h er associated vein s d evelop ing
bran ch es.3 Th e cau dal bran ch form s th e PCoA, th e P1 segm en t of at th is t im e in clude th e p rim it ive m axillar y vein an d t h e ven t ral
th e PCA, an d p ar t of th e BA. Th e PCoA qu ickly t akes over as th e ph ar yngeal vein , w h ich later becom es th e lingu al, facial, an d ex-
m ain blood su pply to th e rh om ben ceph alon , an d th e t rigem in al tern al jugular vein s.12
ar ter y recedes over th e course of a few days (E29–E32). As a re- Bet w een E35 an d E37, th e an terior du ral plexus becom es as-
su lt , th e cau dal bran ch an n exes th e m idbrain an d h in dbrain ves- sociated w ith a prim it ive m argin al sin u s an d begin s to t ran sform
icles in to it s circu lat ion .5,7 Th e cran ial bran ch , also called t h e in to t h e fu t u re su p er ior sagit t al an d t ran sverse sin u ses.9,11,12
olfactor y ar ter y, perfu ses th e large, developing forebrain vesicle Below t h e telen cep h alic vesicle, a vein su bsequ en t ly id en t ified
an d is th e predecessor of the ACA, th e first an d phylogen et ically as th e superficial m iddle cerebral vein also begin s to em erge. At
oldest telen cep h alic ar ter y. In addit ion to becom ing th e ACA, th is a sim ilar t im e in th e h in dbrain , th e posterior dural plexus join s
vessel su bsequ en tly elaborates m u lt ip le bran ch es to th e rap idly th e p rim ar y h ead vein w h ere th e lat ter drain s in to th e an terior
grow ing telen cep h alon , in clu ding th e an terior ch oroidal ar ter y, cardin al vein (i.e., th e p rim it ive in tern al jugu lar vein ). Th e stem
MCA, an d ACoA. of th e posterior dural plexus, th erefore, con st it utes th e caudal
By 5 w eeks, th e brain h as developed in to a five-vesicle organ , en d of th e fu t u re sigm oid sin u s.
an d th e ch oroid plexus begin s to differen t iate w ith in discrete re- By E43, th e m iddle an d posterior dural plexuses form a sec-
gion s of th e cen t ral can al/ven t ricu lar system .5,11 Met abolically, on dar y an astom osis, w ith a ch ange in ven ous drain age tow ard a
the choroid plexus is very active an d prom otes developm ent of its n ew, dorsally located ch an n el. Th is sh ift in drain age is th e first
ow n vascular supply. As a result, a branch vessel extends from the in dicat ion of th e t ran sverse an d sigm oid sin u ses, w ith th e t ran s-
cran ial ram us to feed th e plexus of th e telen ceph alic vesicle; th is verse sin us represen t ing th e m ost cran ial por t ion of th e an asto-
bran ch is th e fut ure an terior ch oroidal ar ter y. A bran ch from th e m osis an d th e sigm oid sin u s represen t ing th e caudal por t ion .12
cau dal ram u s su p plies th e ch oroid plexu s of th e dien cep h alon By E50 to E52, progressive ch anges con t in ue in th e develop -
an d m esen cep h alon ; th is vessel is th e posterior choroidal ar ter y. m en t of th e cran ial sin uses, w ith th e t ran sverse sin us becom ing
Th e con n ect ion bet w een t h e telen cep h alic an d d ien cep h alic m ore defin it ive an d th e first in dicat ion of a sagit tal sin us in both
vesicles, th e fu t u re foram en of Mon ro, is th erefore an im p or t an t its inferior and superior locations. Despite these ongoing changes,
area w h ere h em odyn am ic balan ce occurs bet w een th e an terior venou s developm en t con t in ues to lag beh in d th at of th e ar terial

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1 Development of the Cerebrovasculature 7

system , w it h t h e sigm oid sin u s being t h e on ly defin it ive sin u s often in adver ten tly rem oved togeth er w ith th e rest of th e m e-
by th e en d of th e em br yon ic p eriod. Th e su perior sagit t al sin u s n inges during h istological t issue preparat ion , leaving th e cere-
em erges m ore defin it ively at E60, as th e cerebral h em isp h eres bral cor t ical surface w ith ou t id en t ifiable vasculat ure.14
en large. Th e p rim it ive st raigh t sin u s an d p rim it ive great cerebral Th e pial an astom ot ic cap illar y plexu s is, in fact , th e in n erm ost
vein of Galen also begin to develop at th is t im e, providing in ter- com pon en t of th e ext racerebral m en ingeal com p ar t m en t . Devel-
n al cerebral drain age.11 Fin ally, cerebellar vein s can also be iden - opm en t of th is com par t m en t begin s aroun d em br yon ic w eek 6
t ified at th is t im e. an d 7 w ith th e establish m en t of th e m en inges. All vascular com -
Cerebral ven ou s drain age ret u rn s to th e developing h ear t via pon en t s of th e m en inges, in clu ding th e du ral ven ou s sin u ses,
th e left an d righ t an terior cardin al vein s. Th e an terior cardin al arach n oidal m ain ar teries an d vein s, an d pial capillar y plexu s,
vein s origin ally drain blood in to th e sin u s h orn s via th e com m on are iden t ifiable in 7-w eek h um an em br yos.15–17 Also eviden t by
cardin al vein s.9 Th is sym m et rical con figu rat ion last s for on ly a em br yon ic w eek 7 is an im p erm eable m em bran e covering th e
sh or t t im e before t h e p roxim al con n ect ion of t h e left an ter ior brain surface (ben eath th e pia). Th e m em bran e is com posed of
cardin al vein w ith th e left sin u s h orn regresses. Th e sm all rem - glial en d feet un ited by t igh t jun ct ion s an d em bedded in basal
n an t of th is form er con n ect ion , w h ich is called th e obliqu e vein lam in a.
of th e left at rium , lies directly on th e h ear t . A m edian an astom o- During early pren at al developm en t , from em br yon ic w eek 7
sis, con n ect ing th e left an d righ t an terior card in al vein s, devel- to 25, t h e en d feet p rod u cing t h is im p er m eable exter n al glial-
ops from thym ic an d thyroid vein s. On ce th e left an terior cardi- lim it ing m em bran e belong to rad ial glial cells. Rad ial glia are
n al vein loses its con n ect ion w ith th e h ear t , all ven ous drain age t h e em br yon ic n eu ral stem cells t h at p rod u ce n eu ron s, ast ro -
from th e left side of th e h ead an d n eck sh u n t s to th e righ t an te- cytes, an d oligoden d rocytes d u r in g em br yon ic brain d evelop -
rior cardin al vein th rough th is n ew con n ect ion . Th e p roxim al left m en t . Th ese elongated, radially orien ted stem cells m ain tain
an ter ior card in al vein also receives d rain age from t h e left su b - th eir cell body in th e ven t ricu lar zon e, n ext to th e w alls of th e
clavian vein , w hich coalesces from th e ven ous plexus of th e left ven t ricles, an d exten d a long basal process to th e pial surface
upper lim b bud. Th e in tercardin al an astom osis th us carries blood w h ere th ey dock th eir en d feet . Post n at ally, radial glia u n dergo a
from th e left u pper lim b an d th e left h ead an d is called th e left term in al t ran sform at ion in to ast rocytes, during w h ich th eir long
brach ioceph alic vein . Th is an astom ot ic vessel join s th e righ t an - process is reeled in as th e cell body ascen ds closer to th e p ial
terior cardin al vein at its jun ct ion w ith th e righ t brach ioceph alic su rface to becom e sp ecialized first-layer ast rocytes p rodu cing
vein . Th e sm all segm en t of th e r igh t an terior cardin al vein be- th e extern al glial-lim it ing m em bran e in th e adult .18,19
t w een t h e ju n ct ion of t h e brach iocep h alic vein s an d th e righ t Th e p ial capillar y plexus is a sh or t-lin ked an astom ot ic plexus
at riu m becom es th e su p erior ven a cava.9 By th e en d of th e em - th at covers th e en t ire cerebral cor t ical su rface th rough ou t d evel-
br yon ic period, th e su perior ven a cava th us drain s blood from opm en t , w ith its in n um erable capillaries separated from th e ex-
both sides of th e h ead an d both u p per lim bs. ternal glial-lim it ing m em bran e below by fibroblasts, m en ingeal
In com parison w ith th e ar terial system , cerebral developm en - cells, an d collagen fibers.14 Th e p lexu s is t h e or igin of t h e p er-
tal ven ou s an om alies are m ore com m on an d th ey are frequ en tly forat ing vessels th at w ill provide th e in tern al vascularizat ion of
en cou n tered on conven t ion al n eu roim aging st u dies.11–13 In th e th e cor tex, w ith th e n u m ber of p er forat ing vessels in creasing
m ajor it y of cases, t h ese lesion s are con sid ered ext rem e an a- accordingly as th e plexu s exp an ds d u ring developm en t . To en ter
tom ic variat ion s of th e cerebral vasculat ure an d follow a ben ign t h e cor tex, t h e p ial cap illar ies p er forate t h rough t h e exter n al
cou rse. At ypical form s, h ow ever, are associated w ith cavern ou s glial-lim it in g m em bran e first in t h e p roxim al (ven t ral) cor t ical
m alform at ion s an d ar terialized developm en t al ven ou s an om a- region in em br yon ic w eek 7 an d progress tow ard th e dist al (dor-
lies th at carr y greater risk for cerebral h em orrh age an d its clin ical sal) region . Th e st riat u m an d pyriform lobe are am ong th e first
sequelae. region s to h ave in ter n al vascu lar izat ion , w it h t h e en t ire cor t i-
cal su rface h aving iden t ifiable p erforat ing vessels by em br yon ic
w eek 8. Not ably, th is ven t ral to dorsal progression parallels th e
arrival of early n euron s an d fibers from ext racor t ical sources.14
Pial cap illar y perforat ion of th e extern al glial-lim it ing m em -
■ Microvascular Development bran e is a com plex developm en tal process th at occurs in four
Th e cerebrovascu lat u re can be divided in to th ree m ajor com - iden t ifiable ph ases, first described u sing rap id Golgi preparat ion
part m en t s: ext racerebral m en ingeal, in t racerebral ext rin sic, an d an d elect ron m icroscopy.20 First , pial cap illaries est ablish direct
in t r in sic m icrovascu lar.14 Th e ext racerebral com p ar t m en t en - con t act w it h t h e exter n al glial-lim it in g m em bran e. Th en , t h e
com p asses t h e m ain ven ou s sin u ses, w it h in d u ral lam ellae, as leading endothelial cells of the external glial-lim iting m em brane-
w ell as th e m ain cerebral ar teries an d vein s, in t h e arach n oidal con t act ing capillaries dem on st rate con siderable m em bran e ac-
lam ellae. Develop m en t of t h e ext racerebral com p ar t m en t h as t ivit y. Th e cells exten d m any filop odia, som e of w h ich perforate
been w ell st udied an d w as discussed earlier. How ever, because th e vascu lar an d cor t ical basal lam in a an d p en et rate th e n eu ral
th ere are n o residen t vascu lar p rogen itor cells in th e n er vou s t issu e. Glial en d feet adjacen t to areas of filopodial in filt rat ion
system , developm en t of th e p erforat ing m icrovascu lat u re n eces- first sw ell an d th en lose their t igh t-jun ct ion at tach m en t s, lead-
sitates th e invasion of th e n eu ral t issu e by th ese ext racerebral ing to th e th ird p h ase, du ring w h ich en t ire en doth elial cells begin
vessels. Developm en tal st udies of th e process of m icrovascular to p en et rate t h e n eu ral t issu e. Fin ally, p roliferat ion an d can ali-
invasion lagged beh in d th ose describing th e larger vessels in th e zat ion of th e invading en doth elial cells resu lt s in th e in sit u for-
ext racerebral com p ar t m en t largely d u e to th e m icroscop ic n a- m at ion of n ew cor t ical cap illar ies. In terest in gly, t h e or igin al
t u re of t h e invad in g vessels. Sp ecifically, th e or igin of th e in - p en et rat ing filopodia are surrou n ded by fused vascu lar an d glial
vad ing vessels is th e pial an astom ot ic capillar y plexus, w h ich is (extern al glial-lim iting m em bran e) basal lam in a. As a result , th e

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8 I Development, Anatomy, and Physiology of the Central Nervous System

n ew ly form ed invading capillaries are surroun ded by a reestab - face of th e capillaries. Alth ough th ere are n o sm ooth m uscle cells
lish ed extern al glial-lim it ing m em bran e.14 A perivascu lar sp ace on th ese capillaries, an abun dan ce of pericytes is located on th e
bet w een th e invading capillaries an d th e extern al glial-lim it ing outer w all an d m ay be respon sible for producing pulsat ile flow.24
m em bran e is con t igu ou s w it h t h e ext racerebral m en in geal in - Furth erm ore, th ere are n o Virch ow -Robin spaces at th e level of
terst it ial sp ace t h at su r rou n d s t h e p ial cap illar y p lexu s. Th ese th e in t rin sic capillaries. In stead, com plex an d in com p letely u n -
perivascu lar sp aces are called Virch ow -Robin sp aces. Th e cor t i- d erstood in teract ion s bet w een en d ot h elial cells an d glial cells
cal cap illar ies su r rou n d ed by t h ese sp aces com p r ise t h e in t ra- produ ce th e blood–brain barrier at th is level. Th e size, den sit y,
cerebral ext rin sic m icrovascu lar com par t m en t .14 an d t h ree-d im en sion al organ izat ion of t h e in t r in sic p lexu ses
During th eir in sit u developm en t , th e pial capillaries of th e rem ain u n ch an ged t h rough ou t p re- an d p ost n at al cor t ical d e-
ext rin sic m icrovascu lat u re perforate th e extern al glial-lim it ing velop m en t , w it h u n ifor m in tercap illar y sp aces m easu r in g 80
m em bran e on ly to en ter bu t n ot to exit th e cortex. Circu lator y to 100 µm in diam eter.14 Th ese spaces are sm aller w ith h igh er
dynam ics later determ in e w h ich vessels w ill en ter ar terioles or vascu lar den sit y in th e gray m at ter, w h ere n euron s occupy th e
exit venules; the final pat tern consists of each exiting venule sur- in tercap illar y spaces. Due to its com plexit y, th e an atom ic an d
roun ded by 8 to 10 en tering ar terioles.14 As th e cor tex exp an ds, fu n ction al developm ent of the cerebral m icrovasculature and, in
new perforating vessels continue to en ter bet w een previous ones particu lar, it s role in th e expan ded h um an cerebral cortex h ave
to m ain tain a con stan t in ter vascular dist an ce of bet w een 400 yet to be fu lly u n derstood an d appreciated.
an d 600 µm at th e brain su rface. Th e in ter vascular distan ce be-
t w een adjacen t p erforators an d th e result ing dim en sion of th e
in t rin sic capillar y p lexu s (discu ssed in det ail below ) represen ts
a m am m alian brain’s physiological con stan t n ecessar y for ade- ■ Molecular Determinants of
qu ate oxygen an d n ut rien t perfu sion .
Th e invading cap illaries of t h e ext rin sic m icrovascu lat u re si-
Cerebrovascular Development
m u lt an eou sly en ter th e n eu ral t issu e at m any locat ion s, m ostly Our curren t un derstan ding of cerebrovascular developm en t is
w ith an orien tat ion perpen dicu lar to th e cor t ical su rface pen e- alm ost en t irely based on descript ive h istological st udies at th e
t rat ing dow n to th e ven t ricu lar zon e. At th e ven t ricu lar zon e, an cellu lar an d t issu e levels. Th e m olecu lar even t s t h at d r ive t h is
in t rin sic cap illar y an astom ot ic p lexu s form s th at in tercon n ects d evelop m en t are less w ell st u d ied bu t rep resen t t h e area of
all perforators in th e zon e. Th is periven t ricu lar plexus is th e first greatest recen t in terest an d fut ure advan ces. As early as 1986, it
of m any in t rin sic cap illar y p lexu ses t h at d evelop in p arallel to w as discovered th at th e cen t ral n er vou s system prod u ced p ro-
th e ascen d ing st rat ificat ion an d in sid e-ou t lam in at ion of t h e angiogen ic factors, in cluding fibroblast grow th factor-1 25 an d
cerebral cor tex.17,21 vascu lar en doth elial grow th factor-A (VEGF-A).26,27 In terest ingly,
A fin al im por tan t fun ct ion of th e ext rin sic capillar y m icrovas- VEGF-A exp ression w as developm en t ally regu lated in th e n eu ral
culat ure relates to th e surroun ding Virch ow -Robin spaces th at t u be.28,29 Gen et ic ablat ion of VEGF-A in th e n eu ral t u be resu lted
accom pany th em . Virch ow -Robin spaces are open to th e m en in - n ot on ly in reduced vessel den sit y an d bran ch ing bu t also in de-
geal in terst it ial spaces an d th ereby provide an exch ange route fect s in the n eu ral t u be itself.30,31
bet w een th is in t racerebral com par t m en t an d th e m en inges. In Th ese early st u dies on VEGF-A fou n d th at m any sign aling
essen ce, t h ese sp aces p rovide a lym ph at ic-equ ivalen t drain age path w ays im p or tan t in vascu lar develop m en t w ere also co-opted
route for t h e brain , w h ich lacks t rue lym ph at ic ch an n els.17,20,22 by t h e d evelop in g n er vou s system . Th ese p ath w ays in clu d e
How ever, th is lym ph at ic system is in efficien t becau se it lacks VEGF/VEGF receptors, sem aphorins/plexin receptors, neuropilin s
feat u res com m on to lym p h at ic ch an n els in oth er organ s, su ch as (co-receptors for both VEGF an d plexin receptors), n et rin s/UNC
valves. On e suggested m ech an ism for th e m ovem en t of fluid an d receptors/DCC receptor, an d slit s/ Robo receptors.32 To u n d er-
debris th rough th ese p erivascu lar sp aces is th e presen ce of regu - st an d t h e sp ecific role of t h ese p at h w ays in vascu lar d evelop -
lar pu lsat ion s of th e perforat ing vessels w ith a single su perficial m en t , exp erim en t s h ad to be devised to sp ecifically delete cell-
m eningeal opening. Content that eventually reaches the m eninges au ton om ou s com p on en t s of t h e p at h w ay eit h er in develop ing
drain s th rough m en ingeal perivascular lym p h at ic ch an n els.14,23 vessels or d evelop in g n eu ral t issu e. In su ch a st u dy an alyzin g
As briefly described above, th e in t rin sic an astom ot ic cap illar y n er vous t issue-specific delet ion of a VEGF-A receptor, flk-1, n o
plexu ses d evelop bet w een adjacen t p erforators of th e ext rin sic deleteriou s effect s w ere n oted in n eu rovascu lar d evelop m en t .
system in a p rogressive in sid e-ou t p at ter n t h at follow s n eu ro - Th e au th ors th erefore con clu ded th at th e d efect s seen w ith prior
n al developm en t in th e cor tex. Th e periven t ricu lar m at rix zon e global VEGF-A delet ion w ere due to a direct effect on en doth elial
is th e first to vascu larize because of its early germ in al act ivit y, cells.30 How ever, t h is fin d in g h as been con t rad icted by ot h er
follow ed in sequ en ce by t h e w h ite m at ter, th e su bp late zon e, st u dies th at h ave repor ted th at VEGF sign aling is im p or t an t for
an d fin ally th e m at uring gray m at ter.14 To in tercon n ect adjacen t n eu ral su r vival an d fun ct ion .33–35
ext r in sic vessels, cap illar ies of t h e in t r in sic system p er forate In addit ion to in sit u cell-auton om ous gen et ic ablat ion , st ud-
t h rough t h e Virch ow -Robin sp aces’ ou ter glial w all an d basal ies u sing gen et ically m odified graft s h ave altern ately dissected
lam in a to en ter th e brain paren chym a in a m an n er sim ilar to th e th e d ifferen t ial effect s of sign aling p ath w ays at th e n eu rovascu -
perforation of the cortex external glial-lim iting m em brane by pial lar in terface. Th ese st u dies are based on th e abilit y of m ouse em -
cap illaries. Em erging cap illaries from n eigh boring ext rin sic ves- br yon ic stem cell-derived em br yoid body grafts to con t ribu te to
sels establish con tacts an d form sh or t-lin ked an astom ot ic plex- angioblasts an d en doth elial cells in th e h ost (quail) perin eural
uses. Intrinsic capillaries are ~ 5 µm in diam eter and consist solely vascu lar plexus. W h en em br yon ic bodies gen et ically ablated for
of en doth elial cells covered by a single basal lam in a of glial an d th e VEGF receptor flk-1 w ere grafted in to qu ail h ost s, th ey w ere
vascu lar origin , w ith glial en d feet docking on th e ablum in al sur- defect ive in angioblast m igrat ion an d perin eu ral vascular plexus

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1 Development of the Cerebrovasculature 9

con t ribu t ion , suggest ing a role for VEGF sign aling in p erin eu ral ten t an astom ot ic ch an n els are u n u su al, w it h an in cid en ce be-
vascu lar p lexu s for m at ion .36 Conversely, t ran sp lan t s of m ou se t w een 0.1%an d 1.2%. Th e p ersisten t t rigem in al ar ter y is th e m ost
n eu ral t u be in to qu ail em br yos led to t h e ectop ic for m at ion of com m on (85%), follow ed by th e hypoglossal ar ter y, w h ereas th e
qu ail-d er ived p er in eu ral vascu lar p lexu s arou n d t h e graft , re- ot ic an d proatlan t al in tersegm en t al ar ter y (persisten t first cer-
vealing th at th e n eural t u be w as th e sou rce of pat tern ing sign als vical in tersegm en t al) are rare.44 Th e persisten t t rigem in al ar ter y
for vessel ingression . Sim ilarly, ex-vivo cocult u re system s w h ere is iden t ified as a p rom in en t bran ch of th e proxim al cavern ous
qu ail n eu ral t u be w as cu lt u red w ith m ou se som it ic m esod erm ICA, coursing posteriorly w ith in th e cavern ou s sin us m edial to
revealed t h at n eu ral-derived VEGF-A w as requ ired for vessel for- th e op h th alm ic division of th e t rigem in al n er ve. Th e vessel fol-
m at ion . Gain -of-fu n ct ion exp er im en t s h ave also su p p or ted t h e low s th e cou rse of th e t rigem in al n er ve or p asses th rough th e
role of VEGF-A in n eu rovascu lar d evelop m en t . Select ive exp res- dorsu m sella to join th e m idbasilar ar ter y. Usu ally, th e VAs an d
sion of th e m ajor VEGF-A isofor m s VEGF165 an d VEGF189 in PCoAs ipsilateral to th e t rigem in al ar ter y are hypoplast ic. Th e
localized places in th e developing n eural t ube via elect ropora- hypoglossal ar ter y is a bran ch of th e distal cer vical ICA, arising
t ion in du ced local ectop ic ingression of th e p erin eu ral vascu lar bet w een C1 an d C3, w h ich cou rses p osteriorly an d su p er iorly
plexus vessels, w ithout significantly affecting neuron al sur vival or to en ter th e skull base th rough th e hypoglossal can al to join th e
pat tern ing.37 Conversely, elect roporat ion of a VEGF inhibitor, th e proxim al BA. Th e proatlantal-intersegm ental arter y connects the
solu ble VEGF receptor sFlt-1, locally blocked vessel ingression . dist al cer vical ICA or ECA to th e VA, cou rsing bet w een th e oc-
Vascular en doth elial grow th factor sign aling does n ot operate cipu t an d C1 arch , w h ereas th e ot ic arter y is an exceedingly rare
alon e in p rom ot in g n eu rovascu lar d evelop m en t . In fact , n eu ro- vessel exten ding m edially from th e pet rou s ICA th rough th e in -
p ilin co-receptors am plify VEGF sign aling an d h ave oth er roles tern al au ditor y can al to th e proxim al basilar ar ter y.11
in n eu rodevelop m en t in depen den t of VEGF. En doth elial-specific Th ere are oth er variat ion s in vascu lar an atom y w ith in each
delet ion of n eu rop ilin -1 resu lts in large u n bran ch ed vessels in region of t h e cerebral circulat ion . For exam ple, th ere are several
th e brain .38 Th is fin ding is con sisten t w ith th e p h en ot yp e ob - varian t s of th e ACA/ACoA com plex. Th e unpaired arrangem en t ,
ser ved w ith global n eu rop ilin -1 d elet ion , w h ere vessels invade called th e azygos ACA, con sist s of a single ar terial t ru n k distal to
th e n eu ral t ube an d m igrate along radial glia bu t fail to form lat- th e ACoA th at su p plies both h em isp h eres. Th e in ciden ce of th e
eral t u rn s at th e ven t ricu lar zon e border.39 In terest ingly, n eu ro- azygos ACA ranges from 0 to 5%.45 Th e bih em isph eric ACA con -
pilin act s also as a co-receptor w ith p lexin s to m odu late sem a- sists of a p ericallosal ar ter y th at sup p lies th e m ed ial p or t ion s of
ph oring sign aling. In a recen t st u dy aim ed at exam in ing p oten t ial both h em isph eres, w ith th e opposite ACA being hypoplast ic an d
crosst alk bet w een th ese sign aling p at h w ays, Sem a/n eu rop ilin on ly supplying th e callosom argin al bran ch es. Th is variat ion is
sign aling in th e develop ing h in dbrain regulated on ly th e n eu ral found in 2 to 7%of an atom ic specim ens.46 Th e t riplicated ACA h as
com par t m en t , n ot th e vascu lar com par t m en t .40 Th is fin ding sug- several n am es, in clu ding th e m edial ACA, th ird A2 ar ter y, an d
gests th at despite poten t ial overlap in sign aling com pon en ts, accessor y ACA.8 Th is vessel, also called th e m edian ar ter y of th e
specific com bin at ion s of co-receptors m ay en able th e segrega- corp u s callosu m , is th ough t to be derived from th e em br yon ic
t ion of sign aling path w ays in d ifferen t cell/t issue t ypes. m edian arter y of th e corp u s callosu m , w h ich is a bran ch of th e
Oth er path w ays w ith less w ell u n derstood roles in cerebro- ACoA t h at r u n s p arallel to an d beh in d t h e n or m al p ericallosal
vascu lar develop m en t in clu de th e n et rin /UNC path w ay, in w h ich ar ter y, w ith blood su pply to th e corpu s callosum , septal n u clei,
con t radictor y loss-of-fu n ct ion st u dies h ave altern ately rep or ted sept u m p ellu cidum , rost ral forn ix, an d p ar ts of th e fron tal lobes.
eit h er excess or lack of vascu lat u re.41,42 Fin ally, an ot h er st u dy Th is vessel becom es p ar t icu larly im p or t an t clin ically as a bran ch
sh ow ed a role for t h e W n t p at h w ay: gen et ic d elet ion of bot h at th e base of ACoA an eur ysm s th at can be difficu lt to iden t ify,
W n t 7a an d W n t 7b in t h e d evelop in g n eu ral t u be’s d isr u pted bu t n eeds to be avoided du ring clip app licat ion .
vessel ingression .43 Our un derstan ding of th e m olecular cu es Fin ally, th ere are several variat ion s in fusion pat tern s of th e
th at guide n eu rovascu lar developm en t is st ill in its in fan cy, an d BA. Th e BA form s from coalescen ce of m u lt iple ch an n els belong-
m any p rovocat ive quest ion s rem ain to be an sw ered. Im por tan tly, ing to th e longit udin al n eural arteries (discussed in det ail above).
th ere are sign ifican t poten t ial th erapeu t ic im p licat ion s of a bet- Variat ion s in th e BA are due to differen ces in th e exten t or com -
ter m olecular understanding of cerebrovascular developm ent, in - pleten ess of th e fu sion , w h ich occu rs in a cau dal to rost ral direc-
clu ding th e developm en t of sm all m olecu le agon ist s/an t agon ist s t ion .5 For exam ple, a sh or t BA is th e result of a lack of fu sion of
for t reat m en t of diverse disease processes such as in t racran ial th e cau dal segm en t , w h ereas an u n fu sed or u n zip ped u pp er BA
ath erosclerosis an d brain t u m or progression . resu lts from lack of fu sion of th e rost ral segm en t . Fin ally, in com -
plete fusion in m idsegm ents results in fenestrated configurations.8

■ Clinical Implications: Variant Anatomy


as a Developmental Vestige ■ Conclusion
Th e processes u n derlying cerebrovascu lar developm en t exp lain Th e em br yon ic n er vou s system does n ot h ave residen t vascu lar
th e varian t vascular an atom y seen in th e clin ical populat ion . For progen itor cells. Cerebrovascular developm ent , th erefore, requires
exam ple, t h e persisten t carot id-ver tebrobasilar an astom oses are an orch est rated series of even ts leading to vessel invasion in to
vest iges of d evelop m en t t h at failed to regress.11 In em br yon ic th e n eu ral t issu e. Vascu lar progen itors from th e m esoderm first
d evelopm en t , before th e VA form s, th ese an astom oses allow th e form th e larger ch an n els, in cluding th e ICAs an d th eir cran ial an d
carot id ar ter y to su pp ly th e p osterior circu lat ion . Th e m ost com - cau dal ram i, w h ich in it ially su p ply th e en t ire developing brain .
m on p ersisten t an astom osis is t h e n or m al PCoA.3 Oth er p ersis- Through subsequent stages of developm ent the longitudinal n eu-

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10 I Developm ent, Anatomy, and Physiology of the Central Nervous System

ral ar teries, w h ich form t h e BA an d con n ect p roxim ally w ith th e even t s dr iving all of t h ese p rocesses are ju st begin n ing to be
VAs, an n ex t h e p osterior circu lat ion . Microvascu lar developm en t d iscovered, w ith great clin ical an d th erapeut ic im plicat ion s. Im -
proceeds w ith invasion of th e n eu ral p aren chym a from th e pial proved u n derstan ding of sign aling path w ays m ay resu lt in n ew
cap illar y plexu s, w h ich u lt im ately form s a h igh ly ram ified an d drug t argets for diverse n eu rologic disorders ranging from st roke
den se in t racerebral in t rin sic capillar y n et w ork. Th e m olecu lar to brain t u m origen esis.

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21. St rong LH. Th e early em br yon ic pat tern of in tern al vascularizat ion of th e gan d s d u ring n eu rovascu lar p at tern ing. Developm en t 2007;134:1833–
m am m alian cerebral cor tex. J Com p Neurol 1964;123:121–138 1843
22. Pile-Spellm an JM, McKusick KA, St rau ss HW, Cooney J, Taveras JM. Experi- 41. Lu X, Le Noble F, Yuan L, et al. Th e n et rin receptor UNC5B m ediates guid-
m en t al in vivo im aging of th e cran ial perineu ral lym ph at ic path w ay. AJNR an ce even t s con t rolling m orphogen esis of th e vascular system . Nat ure
Am J Neuroradiol 1984;5:539–545 2004;432:179–186

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1 Development of the Cerebrovasculature 11

42. Wilson BD, Ii M, Park KW, et al. Net rin s prom ote developm en t al an d th er- 45. Calzolari F, Cer ut i S, Pin n a L, Tam arozzi R. Aneur ysm of th e azygos peri-
ap eu t ic angiogen esis. Scien ce 2006;313:640–644 callosal ar ter y. On e case. J Neu roradiol 1991;18:277–285
43. Sten m an JM, Rajagopal J, Carroll TJ, Ish ibash i M, McMah on J, McMah on 46. Perlm ut ter D, Rh oton AL Jr. Microsurgical an atom y of th e dist al an terior
AP. Can on ical Wn t sign aling regulates organ -specific assem bly an d dif- cerebral ar ter y. J Neurosurg 1978;49:204–228
feren t iat ion of CNS vasculat ure. Scien ce 2008;322:1247–1250
44. Yilm az E, Ilgit E, Tan er D. Prim it ive persisten t carot id-basilar an d carot id-
ver tebral an astom oses: a report of seven cases an d a review of th e litera-
t ure. Clin An at 1995;8:36–43

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2 Microsurgical Anatomy of the Internal
Carotid and Vertebral Arteries
Maria Peris-Celda, Alvaro Cam pero, Pablo Rubino, and Albert L. Rhoton, Jr.

A thorough understan ding of cerebrovascular anatom y is critically n ear t h e ton sil. Th e ICA en ters t h e cran iu m w it h ou t giving off
im por t an t w h en addressing path ology involving th e brain . Th is any bran ch es.
chapter review s th e m icrosurgical anatom y of the in ternal carotid Th e ICA is in it ially su p er ficial to t h e ECA, bu t after 10 to
an d ver tebral ar teries, an d h igh ligh ts im por tan t em br yological 20 m m it t u rn s m edially to pass deeper an d ascen ds tow ard th e
an d path ological con siderat ion s for t reat ing vascular lesion s. carot id foram en in th e sku ll base. Th e ECA first cou rses an tero-
m edially an d th en cur ves back to a superficial posit ion . Based on
its top ograp hy, th e C1 por t ion of th e ICA can be divided in to su-
prahyoid an d p ost-st yloid segm en ts.3,4 Th e p osterior belly of th e
■ Microsurgical Anatomy of the Internal d igast r ic m u scle is t h e referen ce t h at d ivid es th ese t w o p ar t s
Carotid Artery (Fig. 2.2c– e).

Th e in tern al carot id ar ter y (ICA) origin ates in th e n eck w h ere th e


com m on carot id ar ter y (CCA) bifu rcates in to th e ICA an d exter- Suprahyoid Part
n al carot id ar teries (ECAs). Th e ICA can be divided in to four p or- Th e su prahyoid p ar t lies over th e prever tebral p lan e adjoin ing
t ion s from p roxim al to dist al. Th e C1 or cer vical por t ion exten ds posteriorly to th e longu s cap it is m u scle. Th e p h ar yn x lies m edi-
from it s ju n ct ion w it h th e CCA to t h e exter n al or ifice of t h e ally, an d th e superficial cer vical fascia covers th e ICA laterally.
carot id can al. Th e C2, or pet rou s p or t ion , cou rses w ith in th e ca- Th e in tern al jugu lar vein is sligh tly posterior to th e ICA, an d th e
rotid canal and ends w here the artery enters the cavernous sinus. hypoglossal n er ve crosses th e ar ter y laterally im m ediately below
Th e C3, or cavern ou s por t ion , cou rses w ith in th e cavern ou s sin u s th e posterior belly of th e digast ric m u scle. Th e su perior root of
an d en ds w h ere th e ar ter y passes th rough th e dura m ater, form - th e an sa cer vicalis descen ds from th e hypoglossal n er ve an terior
ing th e roof of th e cavern ou s sin u s. Fin ally, th e C4, or sup racli- an d adjacen t to th e ar ter y to join th e in ferior root from th e cer vi-
n oid or in t racran ial por t ion , begin s w h ere th e ar ter y en ters th e cal p lexu s. Th e vagu s n er ve ru n s bet w een th e ICA an d th e jugu lar
su barach n oid sp ace an d ter m in ates at it s bifu rcat ion in to t h e vein in a sligh tly posterior plan e, an d th e sym path et ic ch ain is
an terior cerebral ar teries (ACAs) an d m iddle cerebral ar teries en closed in th e prever tebral fascia p osterior to th e ICA. Th e as-
(MCAs) (Fig. 2.1).1 cen d ing p h ar yngeal ar ter y, a bran ch from th e ECA, is an terior to
th e ICA an d crosses th is vessel directed m edially to th e ph ar yn x.
Th e su perior lar yngeal n er ve, arising from th e vagu s n er ve, is
C1 or Cervical Portion posterior to th e ICA an d crosses th e ar ter y m edially to in n er vate
Th e CCA an d it s bifu rcat ion in to th e ECA an d ICA are located in th e lar yn x. At t h e level of th e digast ric m u scle, th e ICA is crossed
th e carot id t riangle of th e n eck (Fig. 2.2a,b). Th is t riangle, a su b - an teriorly by th e occipital an d posterior auricular arteries, w h ich
division of th e an terior t riangle of th e n eck, is bou n ded by th e are bran ch es of th e ECA.
posterior belly of th e digast ric m u scle su periorly, th e su perior
belly of th e om ohyoid an teriorly, an d th e stern ocleidom astoid
Post-Styloid Part
m uscle posteriorly. Th e bifu rcat ion of th e CCA is u su ally located
in t h e cen ter of a t riangu lar area lim ited by th e in tern al jugular Th e p arap h ar yn geal sp ace lies bet w een t h e p h ar yn geal w all
vein posteriorly, th e thyrolinguofacial ven ou s t run k drain ing in to m edially an d th e m edial pter ygoid m u scle an d p arot id fascia lat-
th e jugu lar vein an teriorly, an d th e hyp oglossal n er ve su periorly erally. Th e space is divided by th e st yloid diap h ragm in to pre-
(Farabeu f’s t riangle) (Fig. 2.2b). st yloid and post-st yloid parts (infrapetrous space). The ICA passes
Th e level of th e bifu rcat ion varies con siderably. In on e st udy, beh in d th e digast ric an d st yloid m uscles to en ter th e post-st yloid
it occu rred at th e sup erior border of th e thyroid cart ilage in space. It is form ed posteriorly by th e prever tebral plan e, m edi-
48.3% of cases, in 25% of w h ich it w as opposite th e hyoid bon e, ally by th e ph ar yn x, an d an terolaterally by th e st yloid plan e
an d it occu rred at t h e level bet w een t h e t hyroid car t ilage an d form ed by th e st yloid m u scles an d st yloid fascia. Th e ECA passes
th e hyoid bon e in 18.3% of cases.2 It occu r red at a level low er bet w een th e st ylohyoid an d st yloglossus m uscle an d rem ain s
th an th e superior border of th e thyroid car t ilage in 5% of cases, lateral. Th e glossop h ar yngeal n er ve crosses th e ICA laterally be-
w h ereas in 3.3% of cases th e bifu rcat ion w as located h igh er th an t w een th is vessel an d th e in tern al jugu lar vein to en ter th e sp ace
th e hyoid bon e. In rare cases, th e ICA m ay arise directly from th e bet w een th e st yloph ar yngeus an d st yloglossus m uscles. Th e ph a-
aor t ic arch . Th e C1 por t ion is t ypically st raigh t , but its course can r yngeal bran ch of th e vagus n er ve reach es th e ph ar yn x m edial to
be tor t uous w h en it lies closer to th e ph ar yn x th an usual, ver y th e ICA.

12

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 13
Fig. 2.1a–c The internal carotid artery (ICA). (a) Lateral (left) and anterior
views (right) of the ICA portions as well as the segm ents of the supraclinoid
(C4) portion of the ICA (insets A1 and A2). The ICA is divided into four por-
tions, from proxim al to distal: C1, cervical; C2, petrous; C3, cavernous; and
C4, supraclinoid. (b,c) The C4 portion of the ICA: (b) anterior and (c) infe-
rior views. The C4 portion of the ICA is divided into three segm ents based
on the origin of its m ain branches: the ophthalm ic segm ent from the origin
of the ophthalm ic artery to the origin of the PCoA (C4-Op., dark blue), the
com m unicating segment from the origin of the PCoA to the origin of the
anterior choroidal artery (C4-Co., light green), and the choroidal segm ent
from the origin of the anterior choroidal artery to the bifurcation of the ICA
into the anterior and m iddle cerebral arteries (C4-Ch., dark green). Be-
t ween 8 and 12 perforating arteries can arise from the C4 portion. A, artery;
ACA, anterior cerebral artery; AChA, anterior choroidal artery; Ant., ante-
rior; BA, basilar artery; Ch., choroidal; Cin., cinereum ; Co., com m unicating;
Diaph., diaphragm; Fr., frontal; Gyr., gyrus; Hyp., hypophyseal; Infund., infun-
dibulum ; Mam ., m am illary; MCA, m iddle cerebral artery; N., nerve; O.Ch.,
optic chiasm ; Olf., olfactory; O.N., optic nerve; Op., ophthalm ic; Ophth.,
ophthalm ic; O.Tr., optic tract; PCA, posterior cerebral artery; PCoA, pos-
terior com m unicating artery; Perf., perforating; Subst., substance; Sup.,
superior. (Reprinted with perm ission from Rhoton AL Jr. The supratentorial
arteries. Neurosurgery 2002;51(Suppl):S53–120.)

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14 I Developm ent, Anatomy, and Physiology of the Central Nervous System

c e

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 15
Fig. 2.2a–e (opposite) C1 or cervical portion of the ICA. (a) The com m on at the level of the digastric tendon in the suprahyoid part and CN IX supe-
carotid artery (CCA) and its bifurcation into the ECA and ICA are located rior to it in the post-st yloid com partm ent). (d) The sternocleidom astoid
within the lim its of the carotid triangle whose boundaries are the sterno- m uscle and the m andible have been rem oved to expose the bifurcation of
cleidom astoid m uscle posteriorly, posterior belly of the digastric m uscle the CCA. The ECA passes bet ween the st ylohyoid and st yloglossus m uscles,
superiorly, and superior belly of the om ohyoid m uscle anteriorly. The whereas the ICA continues its ascending course behind the st yloid m uscles
super ficial lobe of the parotid gland has been elevated to show the facial and diaphragm in the post-st yloid space. (e) View of the ICA passing be-
nerve and the cervical and m arginal m andibular branches of the facial hind the lateral pterygoid m uscle (Ext. Pterygoid M.) after resection of the
nerve superficial to the CCA bifurcation. (b) Anatom ic structures related to st yloid muscles. CNs IX and XII cross the artery laterally. A., artery; Basophar.,
the carotid artery bifurcation are the hypoglossal nerve (CN XII) superiorly, basopharyngeal; Bifurc., bifurcation; Br., branch; Car., carotid; CN, cranial
the jugular vein posteriorly, and the thyrolinguofacial venous trunk anteri- nerve; Com m ., com m on; Cond., condyle; ECA, external carotid artery; Ext.,
orly. The lat ter is retracted laterally in the photograph. These three structures external; Gang., ganglion; ICA, internal carotid artery; Int., internal; Jug.,
form Farabeuf’s triangle. (c) Posterior view of the ICA and its parapharyn- jugular; Lar., laryngeal; M., m uscle; Marg., m arginal; Mand., m andibular;
geal relationships after rem oval of the cervical spine. CNs IX, X, XI, and XII Max., m axillary; N., nerve; Occip., occipital; Sig., sigm oid; Sternocl., sterno-
exit the skull base posterior to the artery. CN X is directed inferiorly; CN XI cleidom astoid; Subm and., subm andibular; Sup., superior; Symp., sympa-
is directed laterally to reach the sternocleidomastoid and trapezius m us- thetic; Thyroling., thyrolinguofacial; Tr., trunk; V., vein.
cles; and CNs IX and XII cross the artery laterally to becom e anterior (CN XII

Near th e sku ll base, th e relat ion sh ip bet w een th e ICA an d ac- Th e h orizon t al segm en t is su rrou n ded by a ven ou s p lexu s an d
cessor y n er ve varies. Th e n er ve can be located posterior to th e th e carot id au ton om ic p lexu s, derived from th e in tern al carot id
in tern al jugu lar vein or bet w een th e vein an d th e ICA to reach bran ch of th e superior cer vical ganglion . At th e level of th e an te-
th e stern ocleidom astoid m u scle. At th e level of th e sku ll base, rior gen u , th is p lexu s divides in th e deep pet rosal n er ve. Th e
th e in tern al jugu lar vein an d ICA sep arate to en ter th e jugu lar deep p et rosal n er ve join s th e greater su p erficial pet rosal n er ve
foram en an d carot id foram en , resp ect ively, for m in g t h e carot i- to form th e vidian n er ve an d carot id n er ve, w h ich follow th e ICA
cojugu lar angle. Bet w een th e carot id can al an d th e jugular bulb, superiorly. Th e greater p et rosal n er ve lies in th e m iddle fossa im -
t w o t iny foram in a carr y th e t ym pan ic bran ch (Jacobson’s) of th e m ediately su perior an d p arallel to th e h orizon t al segm en t of th e
glossoph ar yngeal n er ve an d th e auricular bran ch (Arn old’s) of ICA. After join ing th e deep p et rosal n er ve to form th e vidian
th e vagu s n er ve. At th is level th e glossoph ar yngeal, vagu s, acces- n er ve at th e level of th e an terior gen u , th e greater pet rosal n er ve
sor y, an d hypoglossal n er ves lie bet w een th e ICA an d th e in ter- passes m edially along th e u p p er su rface of th e h orizon t al seg-
n al jugular vein . m en t of th e p et rous ICA to en ter th e vidian can al.
Th e p resen ce of t h e pter ygoid ar ter y or vid ian ar ter y is in -
con sisten t . W h en p resen t , it en ters th e pter ygoid can al w ith th e
C2 or Petrous Portion n er ve of th e sam e n am e an d an astom oses w ith a (recu r ren t )
Th e p et rou s por t ion of th e ICA st ar t s w h ere th e ar ter y en ters th e bran ch of t h e greater p alat in e ar ter y. Th e vid ian ar ter y u su ally
carot id can al th rough th e carot id foram en in th e sku ll base an d arises from th e m a xillar y ar ter y, a bran ch of th e ECA, in th e pter-
en d s w h en th e ar ter y leaves th e can al to en ter th e cavern ou s ygopalat in e fossa. In 45% of cases, h ow ever, a separate vidian ar-
sin us p assing m edial to th e p et rolingu al ligam en t above th e car- ter y arises from th e p et rous carot id ar ter y. Most of th ese cases
t ilage th at fills th e foram en laceru m (Fig. 2.3). It h as a posterior arise from the horizontal segm ent of the ICA, but som e arise from
ver t ical segm en t , a h orizon tal segm en t , an d an an terior ver t ical th e an terior gen u .7
segm en t . A posterior gen u is located bet w een th e p osterior ver- Tw o in con stan t ar terial bran ch es—th e stapedial an d perios-
t ical an d h or izon t al segm en t s, an d an an ter ior gen u is located teal ar teries—are associated w ith th e C2 por t ion of th e ICA. Th e
bet w een th e h orizon t al an d an terior ver t ical segm en ts. st ap edial ar ter y rarely p ersist s in to adu lth ood. It is a secon dar y
Th e p osterior ver t ical segm en t of th e ICA, an terom edial to th e bran ch of th e em br yon ic carot id arter y, an d its n am e reflects
st yloid p rocess, lies p osterior to th e eu st ach ian t u be at it s ju n c- th at it t raverses th e p rim ordiu m of th e cr u s of th e st apes. Th e
t ion bet w een it s osseou s an d car t ilagin ou s p or t ion s, an d an te- periosteal ar ter y arises from th e p et rou s port ion of th e ICA in 8%
r ior to both t h e coch lea an d t ym p an ic cavit y. Th e p oster ior ver- of specim en s.8,9
t ical segm en t is sep arated from t h e t ym p an ic cavit y an d t h e
eu st ach ian t u be by a t h in , bony lam ella t h at is cr ibr ifor m in
th e young an d partially absorbed in th e elderly.5 The carot ico-
C3 or Cavernous Portion
t ym pan ic arter y bran ch es from th is segm en t. The sm all, occa- Th e ICA exit s th e carot id can al above th e foram en lacer u m an d
sion ally d ou ble carot icot ym p an ic vessel en ters th e t ym p an ic lateral to th e d orsu m sellae w h ere it passes u n der th e pet rolin -
cavit y th rough a foram en in th e carot id can al. It an astom oses gual ligam en t . It th en t urn s abruptly for w ard to course along th e
w ith th e an terior t ym pan ic bran ch of th e m axillar y ar ter y an d carot id su lcu s an d lateral p ar t of th e body of th e sp h en oid. It
th e st ylom astoid ar ter y. form s a ver t ical posterior ben d, passes for w ard in a h orizon t al
Th e su p erom edial aspect of th e h orizon t al p et rou s segm en t d irect ion for ~ 2 cm , an d for m s a h or izon t al an ter ior ben d . It
of th e ICA is often un roofed in relat ion to th e t rigem in al n er ve in term in ates by passing upw ard along th e m edial side to th e an te-
Meckel’s cave. Th e u n roofed asp ect is lateral to Meckel’s cave rior clinoid process and posterior surface of the optic strut, w h ere
in 72.5%of sku lls, in th e m idd le p ort ion of Meckel’s cave in 17.5%, it pen et rates th e roof of th e cavern ou s sin us. Th e clin oid seg-
an d com pletely covered by th e pet rolingual ligam en t in 10%. Th e m en t of th e carot id arter y is t igh tly surroun ded by th e an terior
h or izon t al segm en t is p oster ior to t h e ten sor t ym p an i m u scle clin oid process laterally, th e opt ic st r u t an teriorly, an d th e ca-
an d eu st ach ian t u be, w h ich slop e dow nw ard as t h ey p roceed rot id sulcu s m edially. On ly a n arrow space is left bet w een th e
m edially.6 bon e an d ar ter y.

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16 I Developm ent, Anatomy, and Physiology of the Central Nervous System

a b

e d

Fig. 2.3a–e Petrous (C2) and cavernous (C3) portions of the internal ca- passing m edial to the petrolingual ligam ent, the ICA describes an anterior
rotid artery (ICA). (a) Petrous segm ent in a lateral view. The temporal bone genu and enters the cavernous sinus. (d) View of the C3 portion of the ICA
has been drilled to expose the relationships of the C2 portion to the t ym - from above. The clinoidal segm ent of the ICA bet ween the proxim al and
panic cavit y posteriorly and the eustachian tube anteriorly. The posterior distal dural rings is intracavernous. (e) Sagit tal section of a specim en, dis-
bend is located at the level of the t ympanic m em brane. The ICA is sepa- section of the lateral wall of the sphenoid sinus. The C3 portion can be
rated from the t ympanic cavit y and the eustachian tube by a thin osseous completely visualized, the inferolateral trunk is located m edial to the tri-
lamella that is cribriform in the young and partly absorbed in the elderly. gem inal ganglion and lateral to the ICA. A., artery; Cav., cavernous; Clin.,
(b) C3 segm ent after dissection of the left cavernous sinus. The cavernous clinoid; CN, cranial nerve; Eust., eustachian; Gr. Pet. N., greater petrosal
siphon is visualized and the distal dural ring at the superior lim it of C3. The nerve; Inf. Hyp. A., inferior hypophyseal artery; Lig., ligam ent; Max., m ax-
meningohypophyseal trunk, one of the branches of the cavernous portion, illary; Mem b., m em brane; Men. Hyp. A., meningohypophyseal artery; N.,
can be identified and usually found in Parkinson’s triangle. (c) Horizontal nerve; Ophth., ophthalm ic; Pit., pituitary; Seg., segm ent; Tr., trunk; Tymp.,
part of C2. Typically, a segm ent of C2 is unroofed in its m edial aspect below t ympanic, t ympani. (Reprinted with perm ission from Rhoton AL Jr. The su-
Meckel’s cave. The trigem inal nerve has been incised and retracted. After pratentorial arteries. Neurosurgery 2002;51(Suppl):S53–120.)

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 17
Th e du ra lin ing th e su rface of th ese osseou s st ru ct u res facing m iddle clinoid processes join in a caroticoclinoid bony ring around
th e clin oid segm en t form s th e carot id collar arou n d th e clin oid th e ar ter y.
segm en t . In 19 of 20 p araclin oid areas, a carot id cave h as been Th e ocu lom otor, t roch lear, oph th alm ic, an d abd u cen s n er ves
foun d as an in t radural pouch th at exten ds below th e level of th e are lateral to th e ICA. Th e abducen s n er ve is located com pletely
distal d u ral ring bet w een th e w all of th e ICA an d th e du ral collar in sid e th e caver n ou s sin u s, w h ereas t h e ot h ers lie em bed d ed
su rrou n ding th e ICA.10 Th e dist al du ral ring is t igh tly adh eren t to w it h in t h e p er iost ic layer of t h e lateral w all of t h e cavern ou s
th e an terior an d lateral w alls of th e ICA adjacen t to th e an terior sin us on th eir w ay to th e su perior orbital fissure.13
clin oid p rocess an d opt ic st r u t bu t n ot on th e m edial an d poste- Th e in t racavern ou s ICA gives rise to bran ch es th at su pp ly th e
rior sides of th e ar ter y facing th e u p per p ar t of th e carot id su lcu s w alls an d en closed st ru ct u res of th e sella, cavern ou s sin u s, an d
w h ere th e carot id cave is located . tentorium . Th e m en ingohypophyseal t ru n k an d th e in ferolateral
Th e su p erior hyp ophyseal ar ter y frequ en tly arises in th e ca- t run k are th e m ost con sisten t bran ch es of th e in tracavern ou s
rot id cave. Th e d ept h an d circu m feren t ial len gt h of t h e cave ICA. Th ey m ay arise from a single t ru n k in 6% of cavern ou s si-
average 2.4 m m (ran ge, 1.5 to 5 m m ) an d 9.9 m m (range, 4.5 to n uses.14 Th e m en ingohypop hyseal t r u n k is th e largest bran ch of
12 m m ), respect ively. On radiological st u dies, an eu r ysm s arising th e in t racavern ous carot id ar ter y. It arises lateral to th e dorsum
at th e level of th e cave m ay ap pear to exten d below th e level of sellae at or ju st p roxim al to th e ap ex of th e first cu r ve of th e in -
th e u p per edge of th e an terior clin oid. In stead, th ey m ay act u ally t racavern ous ICA. It is about th e sam e size as th e oph th alm ic ar-
exten d in to th e su barach n oid space an d be a sou rce of su barach - ter y. In its m ost com p lete form , it gives rise to th e ten torial (w ith
n oid h em orrh age.11 m edial an d lateral bran ch es), in ferior hypop hyseal, an d dorsal
Th e in t racavern ous ICA is relat ively fixed. W h en view ed from m en ingeal ar teries. Th e in ferolateral t ru n k, also called th e lateral
the lateral direction, th e cavernous (C3) and int racranial (C4) por- m ain stem ar ter y or th e ar ter y of th e in ferior cavern ou s sin u s,
t ion s h ave several cu r ves th at form an S sh ap e. Togeth er, th ese arises from th e lateral side of th e m idpor t ion of th e h orizon tal
por t ion s are called t h e carot id sip h on (Fig. 2.3). Th e low er h alf segm en t of th e in t racavern ou s ICA, 5 to 8 m m dist al to th e origin
of th e S, form ed p redom in an t ly by th e in t racavern ou s por t ion , of th e m en ingohypophyseal t r un k. Th ese bran ch es can arise sep -
is convex an teriorly. Th e u p p er h alf, form ed by th e supraclin oid arately from th e ICA or in differen t com bin at ion s.15 All bran ch es
port ion , is convex posteriorly.12 In 1.5%of cases, th e an terior an d an d th eir areas of vascularizat ion are sum m arized in Table 2.1.

Table 2.1 Cavernous Carotid (C3) Artery Branches, Vascular Supply, and Prevalence

Artery Vascular Supply Location and Prevalence

Recurrent artery of foramen Periosteal lining of foramen lacerum and dura of carotid Foramen lacerum; frequently absent
lacerum canal, wall of carotid artery, pericarotid sympathetic
plexus, lower edge of trigeminal ganglion
Meningohypophyseal trunk Parkinson’s triangle; origin lateral to dorsum sellae
at or just proximal to apex of first curve of
intra cavernous ICA
Medial tentorial artery Transdural segm ent of CN III and IV, roof of cavernous Roof of cavernous sinus and free edge of tentorium
(Bernasconi-Cassinari) sinus, medial third of tentorium , and posterior (tentorial branch 100% present)
at tachment of falx cerebri
Lateral tentorial artery Lateral third of tentorium at its at tachment to petrous Roof of cavernous sinus and tentorium (tentorial
bone branch 100% present)
Dorsal meningeal artery CN VI into Dorello’s canal, dura over dorsum sellae and Passes posteriorly through cavernous sinus with
clivus (medial branch); tentorial at tachment to the CN VI (90% present)
petrous bone (lateral branch)
Inferior hypophyseal Pituitary gland; dura over the posterior sellar floor Passes inferiorly to reach sellar floor (80% present)
artery (hypophyseal arterial circle); dura of posterior clinoid
and medial wall of cavernous sinus (m edial clival
artery)
Medial clival artery Dura over posterior clinoid, dorsum sellae, and medial Posterior clinoid, dorsum sellae; usually a branch of
wall of cavernous sinus inferior hypophyseal artery and less commonly
of cavernous carotid artery
Inferolateral trunk Inferolateral wall of cavernous sinus and adjacent m iddle Lateral side of midportion of horizontal segment of
fossa intracavernous ICA, 5 to 8 m m distal to origin of
Superior division Transdural segm ent of CNs III and IV, roof of cavernous meningohypophyseal trunk (84% present)
sinus, medial third of tentorium , and posterior
at tachment of falx cerebri
Anterior division CNs III, IV, VI and cavernous sinus dura around superior
orbital fissure, V2, dura around foram en rotundum
Posterior division V1, V3,CN VII (petrosal) and dura around gasserian
ganglion
Capsular arteries Dura of floor and anterior m argin of roof of sella Anterior wall and floor of sella; frequently absent
Abbreviations: CN, cranial nerve; ICA, internal carotid artery.

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18 I Developm ent, Anatomy, and Physiology of the Central Nervous System

C4 or Supraclinoid Portion Th e in tradural exposure of C4 and the anterior portion of the


circle of Willis are directed along th e ipsilateral sph en oid ridge or
Th e C4 por t ion begin s w h ere th e ar ter y em erges from th e du ra orbital roof to th e an terior clin oid process. In exposing th e ICA,
m ater form ing th e roof of th e cavern ous sin us. It en ters th e cra- the approach usually proceeds proxim ally to distally, beginn ing
n ial cavit y by passing along th e m edial side of th e an terior cli- w ith the ophthalm ic segm ent and w orking distally tow ard the bi-
n oid p rocess an d below th e opt ic n er ve. It cou rses posteriorly, furcation . The oph th alm ic arter y is difficult to expose because of
sup eriorly, an d sligh tly laterally to reach th e lateral side of th e its short in tradural length an d its locat ion under the optic ner ve.
opt ic ch iasm . Below th e an terior perforated subst an ce at th e m e- W hen exposing C4 beyon d the origin of the oph thalm ic arter y,
dial en d of th e sylvian fissu re, it bifu rcates to give rise to th e ACA the surgeon often sees the an terior choroidal arter y before the
an d MCA (Fig. 2.1). Th e C4 segm en t is defin ed as in cluding th e PCoA, alth ough th e form er arises dist ally to th e lat ter (Fig. 2.4).
crotch from w h ich th e MCA an d ACA arise. Th e bran ch es origi- C4 is divided in to th ree segm en t s based on th e site of origin of
n at ing from th e apex of th e w all bet w een th e origin of th e ACA th e oph th alm ic ar ter y, PCoA, an d an terior ch oroidal ar ter y. Th e
an d MCA are con sidered to be bran ch es of th e ICA, just as an eu- oph th alm ic segm en t exten ds from th e roof of th e cavern ous
r ysm s ar isin g at t h is ap ex are con sid ered to be an eu r ysm s of sin u s an d th e origin of th e op h th alm ic arter y to th e origin of th e
t h e bifu rcat ion of th e ICA. Th e ju n ct ion of th e an teriorly an d pos- PCoA. Th e com m un icat ing segm en t exten ds from th e origin of
ter iorly convex segm en t s p asses along t h e m edial sid e of t h e th e PCoA to th e origin of th e an terior ch oroidal ar ter y, an d th e
an ter ior clin oid p rocess. It s m ajor p rebifu rcat ion bran ch es are ch oroidal segm en t exten ds from th e origin of th e an terior ch o-
the ophthalm ic, anterior choroidal, and posterior com m unicating roidal ar ter y to th e term in al bifurcat ion of th e ICA. Th e oph th al-
ar teries (PCoA). Its perforat ing bran ch es in clu de th e superior hy- m ic segm en t is th e longest , an d th e com m un icat ing segm en t is
pop hyseal ar teries. the shortest.16 An average of eight (range, three to 12) perforating

a b

c d

Fig. 2.4a–j Pterional exposure of the circle of Willis. (a) A left frontotem - laterally above the carotid bifurcation. (c) The basilar bifurcation has been
poral bone flap has been elevated and the dura opened. The left frontal and exposed through the opticocarotid triangle located bet ween the internal
temporal lobes have been retracted to expose the carotid artery entering carotid artery, A1 segm ent of the ACA, and optic nerve. (d) The carotid
the dura m edial to the anterior clinoid process. The carotid bifurcation has bifurcation has been depressed to expose the basilar apex in the interval
been exposed. Lenticulostriate arteries arise from the M1 segm ent of the bet ween the carotid bifurcation and the lower margin of the optic tract.
MCA. The M1 splits in a trifurcation pat tern. (b) The exposure has been Perforating branches crossing the area can m ake the approach hazardous.
extended bet ween the chiasm and frontal lobe to the anterior com m uni- A thalam operforating artery arises from the ipsilateral P1 segm ent of the
cating artery (ACoA) and the contralateral A1 and A2 segm ents of the ante- posterior cerebral artery (PCA).
rior cerebral artery (ACA). A recurrent artery arising near the ACoA passes

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Fig. 2.4a–j (continued ) (e) The temporal pole has been retracted posteri- tomy approach, which increases access to the front of the brainstem and
orly for a pretemporal exposure. The carotid and anterior choroidal arteries the basilar artery. In this case, the labyrinth, including the cochlea and semi-
have been elevated to expose the PCoA, which gives rise to a large perforat- circular canals, and the nerves in the internal acoustic m eatus have been
ing branch referred to as a prem amillary artery. The M1 gives rise to an exposed to show the relationship of these structures to the drilling for the
early branch proxim al to the trifurcation. The P2 segm ent of the PCA ex- anterior petrosectomy. The drilling for an anterior petrosectomy is directed
tends above, and the superior cerebellar artery extends below, the oculo- behind the petrous carotid artery m edial to the labyrinth and proceeds m e-
m otor nerve. (f) Anterior subtemporal view. The temporal pole and the dially to the inferior petrosal sinus and side of the clivus. The abducens nerve
carotid artery have been elevated to expose the origin of the norm al-sized (CN VI) and the internal carotid artery are in the lower m argin of the expo-
PCoA. The anterior choroidal artery passes backward along the medial edge sure. A., artery, arteries; AChA, anterior choroidal artery; ACoA, anterior
of the uncus. A large m edial posterior choroidal artery arises from the P1 communicating artery; AICA, anteroinferior cerebellar artery; Ant., anterior;
and loops downward as it passes to the quadrigem inal cistern. (g ) The an- Bas., basilar; Br., branch; Car., carotid; Clin., clinoid; CN, cranial nerve; Con-
terior choroidal artery has been elevated to expose a large perforating tra., contralateral; Front., frontal; Gr., greater; Ipsi., ipsilateral; Lent. Str.,
branch of the PCoA called a prem am illary artery. (h) The PCoA has been lenticulostriate; MCA, middle cerebral artery; MPChA, medial posterior cho-
elevated to provide an excellent exposure of the basilar apex and the P1s. roidal artery; N., nerve; Olf., olfactory; PCoA, posterior com m unicating ar-
The ipsilateral superior cerebellar artery arises as duplicate arteries. (i) The tery; Pet., petrosal, petrous; Post., posterior; Prem am ., premam illary; Rec.,
tentorium has been divided behind where the trochlear nerve enters the recurrent; SCA, superior cerebellar artery; Seg., segm ent; Sem icirc., sem i-
edge. This increases the length of basilar artery exposure. The trunks of circular; Temp., temporal; Tent., tentorial; Thal. Perf., thalamoperforating;
duplicate superior cerebellar arteries loop down toward the trigeminal nerve. Tr., tract; Trifurc., trifurcation. (Reprinted with perm ission from Rhoton AL
(j) The petrous apex has been rem oved to complete an anterior petrosec- Jr. The supratentorial arteries. Neurosurgery 2002;51(Suppl):S53–120.)

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20 I Developm ent, Anatomy, and Physiology of the Central Nervous System

ar teries (exclu ding th e oph th alm ic, PCoA, an d an terior ch oroidal m en t lateral to th e opt ic n er ve before it en ters th e opt ic can al. It s
ar ter y) arise from C4 (Fig. 2.1). origin varies from as far as 5 m m an terior to 7 m m posterior to
th e t ip of th e an terior clin oid process an d bet w een 2 an d 10 m m
m edial to th e clin oid p rocess.19 Most op h th alm ic ar teries arise
Ophthalmic Segment
an terior to th e t ip of th e an terior clin oid process ~ 5 m m m edial
Th e oph th alm ic ar ter y is th e first bran ch of C4 (Fig. 2.5). Most to th e an terior clin oid.
oph th alm ic ar teries arise below th e opt ic n er ve in th e supracli- Th e in t racran ial segm en t of th e oph th alm ic ar ter y is u su ally
n oid area above th e dural roof of th e cavern ous sin u s an d pass ver y sh or t . In a previous st udy from our laborator y,19,20 14% of
an terolaterally below th e opt ic n er ve to en ter th e opt ic can al an d th e segm en t s exited th e ICA an d im m ediately en tered t h e opt ic
orbit . Eigh t percen t of oph th alm ic ar teries origin ate w ith in th e can al. In t h e rem ain in g 86%, t h e m a xim u m len gth of t h e p refo -
cavern ous sin u s. Rarely, th ey arise from th e clin oid segm en t of ram in al segm en t w as 7 m m an d t h e m ean len gt h w as 3 m m .
th e ICA located on th e m ed ial side of th e an terior clin oid p rocess Th e in t racran ial segm en t u su ally arises from th e m edial th ird of
or from the m iddle m eningeal arter y.1,17,18 They are rarely absent. th e su perior su rface of th e op h th alm ic segm en t u n der th e opt ic
The oph thalm ic arteries occasionally give rise to intracranial per- n er ve an d com m on ly en ters th e opt ic foram en w ith in 1 to 2 m m
forat ing bran ch es. If presen t , th ese bran ches r un posteriorly an d of its origin . Th e exposure of th e oph th alm ic ar ter y is facilitated
are dist ributed to th e ven t ral aspect of the opt ic n er ve an d ch i- by rem oving th e an terior clin oid process an d roof of the opt ic
asm an d th e p it u itar y st alk. can al an d by in cising th e falciform p rocess, a th in fold of du ra
Th e op h th alm ic ar ter y u su ally arises from th e m edial th ird of m ater that extends m edially from the anterior clinoid process and
th e su p erior su rface of C4 im m ediately dist al to th e cavern ou s covers a 0.5- to 11-m m (average 3.5 m m ) segm en t of th e opt ic
sin u s in th e area below th e opt ic n er ve. In on e st udy, it arose n er ve im m ediately proxim al to th e opt ic foram en .
above th e m edial th ird of th e superior surface of th e C4 in 78%of An average of four (range, on e to seven ) perforat ing ar teries
h em isph eres an d above th e m iddle th ird of th e superior surface arise from th e oph th alm ic segm en t (Fig. 2.1). Most arise from
in 22%.16 Non e arose from t h e lateral th ird of th e su perior su r- th e posterior or m edial asp ect of th e ar ter y. Th ese bran ch es are
face. It can kin k laterally, in frequ en tly presen t ing a sh or t seg- m ost often dist ributed to th e in fun dibulum (stalk) of the pit u-

Fig. 2.5a–c Ophthalm ic artery. (a) Superior dissection of the left anterior
and m iddle cranial fossae and orbit. The ophthalm ic artery arises from the
supraclinoidal or intracranial segment of the ICA in m ost cases. It enters the
orbit below the optic nerve through the optic canal. (b) Surgical view after an
orbitozygom atic approach; the anterior clinoid has been rem oved and the
optic canal unroofed. The dura mater of the m iddle fossa has been partially
rem oved. The ophthalm ic artery can be visualized bet ween the optic nerve
and ICA above the distal dural ring (resected). (c) Lateral view of the ICA in
the cavernous sinus and lateral aspect of the orbit showing the intracranial
and intraorbital segm ent of the ophthalm ic artery. A., artery; Cav., cavern-
ous; Clin., Clinoidal; CN, cranial nerve; Fiss., fissure; ICA, internal carotid
artery; Int., internal; Lat. Lateral; Less., lesser; M., Muscle; Max., maxillary; N.,
nerve; Ophth., ophthalmic; Orb., orbital; Pet., petrosal; Pit., pituitary; Pteryg.,
pterygoid; Pterygopal., pterygopalatine; Seg., segment; Sphen., sphenoid;
Sup., superior; Tent., tentorial. (b,c: Reprinted with permission from Rhoton
AL Jr. The supratentorial arteries. Neurosurgery 2002;51(Suppl):S53–120.) c

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 21

itar y glan d an d opt ic ch iasm , an d, less com m on ly, in descen ding itar y stalk an d an terior lobe. Th e in ferior hypophyseal bran ch of
order of frequen cy, to th e opt ic n er ve, prem am illar y p or t ion of the m eningohypophyseal trunk of the intracavernous ICA perfuses
th e floor of th e th ird ven t ricle, an d opt ic t ract . A few vessels ter- the posterior lobe. The capsular arteries also arise from the intra-
m in ate in th e dura m ater covering th e an terior clin oid process, cavernous ICA an d supply th e capsule of the pit uitar y gland.19
sella t u rcica, an d t u bercu lu m sellae. Th e ar teries th at arise from Th is circu m in fu n d ibu lar plexu s gives rise to ascen ding an d
th is segm en t an d p ass to th e in fu n dibu lu m of th e pit u it ar y glan d descen ding ar teries. Th e descen ding ar teries in clu de sh or t-stalk
are called t h e “su p erior hyp op hyseal ar teries.”16,20 Rarely, t h e an d superficial ar teries. Th e sh or t-stalk ar teries pen et rate th e
su perior hypop hyseal ar ter y origin ates from t h e in t racavern ous in fun dibu lu m an d form capillaries th at lead in to sin u soids run -
por t ion of th e ICA.8 Th ey are a grou p of sm all bran ch es (average, n ing dow n th e stalk. Th e su perficial ar teries course in feriorly on
t w o; range, on e to five) th at term in ate on th e p it u itar y stalk an d th e ou t side of th e stalk in th e subarach n oid space an d pen et rate
glan d, but th ey also sen d bran ch es to th e opt ic n er ves an d ch i- th e an terior lobe. Th e ascen ding ar teries su p p ly th e t u ber cin e-
asm an d to t h e floor of t h e t h ird ven t r icle. Th e largest of t h e reu m , m edian em in en ce, an d in ferior su rface of th e opt ic ch iasm .
bran ch es is often referred to as th e su p erior hyp ophyseal ar ter y. Th e su perior hypop hyseal ar teries also sen d bran ch es to th e ch i-
Most of th e bran ch es arise from th e p osterom edial, m edial, or asm an d proxim al port ion s of th e opt ic n er ves.
posterior aspects of th e ar ter y. Th e prem am illar y ar ter y is th e largest bran ch th at arises from
th e PCoA. It en ters th e floor of th e th ird ven t ricle in fron t of or
beside th e m am illar y body bet w een th e m am illar y body an d
Communicating Segment
optic t ract (Fig. 2.6f). Th e prem am illar y ar ter y h as also been re-
Th e PCoA, w h ich form s th e lateral bou n dar y of th e circle of Wil- ferred to as th e an terior th alam operforat ing ar ter y. Th e pre-
lis, arises from th e posterom edial su rface of C4 abou t m idw ay m am illar y arter y m ost com m on ly origin ates on th e m iddle th ird
bet w een th e origin of th e oph th alm ic ar ter y an d th e term in al of th e com m u n icat ing ar ter y, bu t it can also arise on th e an terior
bifurcat ion . It sw eeps backw ard an d m edially below th e t uber or posterior th ird. It su pplies th e posterior hypoth alam us, an te-
cin ereum , above th e sella t urcica, an d sligh tly above an d m edial rior thalam us, posterior lim b of the internal capsule, and subth al-
to the oculom otor ner ve to join the posterior cerebral arter y (PCA). am us. Th e an terior group of PCoA perforat ing bran ch es su pplies
In th e em br yo, th e PCoA con t in ues as th e PCA, but in th e adult th e hypoth alam u s, ven t ral th alam u s, an terior th ird of th e opt ic
th e PCA is an n exed by th e basilar system . If th e PCoA rem ain s th e t ract , an d p oster ior lim b of t h e in ter n al cap su le. Th e p oster ior
m ajor origin of th e PCA, th e con figurat ion is term ed “fet al.” If th e grou p reach es th e posterior perforated su bst an ce an d su bth a-
size of t h e PCoA is sm all or n or m al, it cou rses p osterom ed ially lam ic n ucleu s. Occlu sion of t h e bran ch es to th e subth alam ic n u-
to join th e PCA above an d m edial to th e oculom otor n er ve. A fet al cleus leads to con t ralateral h em iballism .
PCA cou rses fur th er laterally above or lateral to th e oculom otor In m ore th an h alf of st u died h em isph eres, n o perforat ing
n er ve (Figs. 2.4 an d 2.6). Th e PCoA u su ally arises from th e pos- bran ch es arise from th e com m u n icat ing segm en t . If presen t , on ly
terom edial or p oster ior asp ect of t h e C4. Th e d iam eter at th e on e to th ree are fou n d. Th e bran ch es are often st retch ed aroun d
carot id origin is sligh tly larger th an at its ju n ct ion w ith th e PCA, th e n eck of PCoA an eu r ysm s.
bu t th e differen ce is seldom m ore th an 1 m m .
Dilat ion s of th e origin of th e PCoA from C4, kn ow n as “fun c-
Choroidal Segment
t ion al dilatat ion ” or “in fu n dibu lar w iden ing,” are fou n d in ~ 6%of
h em isph eres. Such dilat ion m ay be difficult to dist inguish from Th e an terior ch oroidal arter y u su ally arises from C4 as a single
an an eur ysm . Som e au th ors regard it as an early stage of an eu - ar ter y. Th e m ajorit y arises closer to th e origin of th e PCoA th an
r ysm form at ion because of its h istological appearan ce, w h ich is to th e carot id bifurcat ion (Figs. 2.4 an d 2.7). In frequen tly, it m ay
iden t ical to th e app earan ce of an eu r ysm s. Based on h istological arise from C4 as t w o separate ar teries or as a single ar ter y th at
tech n iques, oth ers h ave con cluded th at th e jun ct ion al dilat ion s divides im m ed iately in to t w o t ru n ks (47% of h em isp h eres).23,24
are n eith er an eur ysm al n or p rean eu r ysm al.21,22 Origin s occu rring in few er th an 1% in clude th e MCA an d PCoA.
An average of eigh t (range, four to 14) perforat ing bran ch es Th e origin of th e an terior ch oroidal ar ter y is sim ilar in diam eter
arise from th e PCoA, m ostly from th e superior an d lateral sur- to th at of th e oph th alm ic ar ter y but sm aller th an th at of th e
faces. Th e bran ch es cou rse superiorly to pen et rate, in decreasing PCoA un less th e PCoA is sm all or hypoplast ic. Th e origin of a fetal
order of frequ en cy, th e t u ber cin ereu m an d p rem am illar y par t of t ype PCoA m ay be m ore t h an t w ice th e diam eter of th e an terior
the floor of the third ventricle, the posterior perforated substance ch oroidal ar ter y. Th e an terior ch oroidal ar ter y is th e first bran ch
an d in terpedun cular fossa, th e opt ic t ract , th e pit uit ar y stalk, on C4 distal to th e PCoA in t w o-th irds of h em isph eres, an d th e
an d th e opt ic ch iasm . Th ese bran ch es also su pply th e th alam u s, secon d, th ird, or even fou r th bran ch follow ing on e or m ore p er-
hypoth alam us, subth alam us, an d in tern al capsule.23 Bran ch ori- forat ing bran ch es in d escen d ing ord er of frequ en cy in t h e re-
gin s are dist ributed relat ively even ly along th e course of th e ar- m ain d er. Th e p er forat in g bran ch es ar isin g bet w een t h e PCoA
ter y. Th e in fu n dibu lar ar teries are a grou p of ar teries th at origi- and anterior choroidal arter y t ypically term inate in the optic tract,
n ate from th e PCoA an d are dist ributed to th e in fun dibulum . m edial tem poral lobe, an d posterior perforated substan ce.
Th ere are few er in fu n d ibu lar ar teries th an su p erior hypop hyseal Th e in it ial segm en t of th e an terior ch oroidal ar ter y is directed
ar teries. On e quar ter of h em isph eres h ave on e or t w o in fun dibu- posterom edially beh in d th e ICA. On an terop osterior angiogram s,
lar ar teries, an d th e rem ain d er h ave n on e. th e in it ial segm en t of th e an terior ch oroidal ar ter y is seen m e-
Th e su perior hypop hyseal an d in fu n dibu lar ar teries p ass m e- dial to th e ICA. Th e origin of th e an terior ch oroidal ar ter y is lat-
dially below th e ch iasm to reach th e t u ber cin ereu m . Th ey in ter- eral to th e opt ic t ract , bu t th e in it ial segm en t crosses from th e
m ingle an d form a fin e an astom ot ic p lexu s arou n d t h e p it u it ar y lateral to th e m edial side of th e opt ic t ract in m any h em isph eres.
st alk called th e circu m in fu n dibu lar an astom osis. Th ese ar teries It seld om rem ain s lateral to th e opt ic t ract th rough ou t it s cou rse.
an d th e circum in fun dibu lar plexus are dist ributed to th e pit u - It passes below or along th e m edial side of th e opt ic t ract to reach
(text cont inues on page 25)

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a b

c d

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Fig. 2.6a–f Variations in the posterior circle of Willis include differing the oculomotor nerve. The left PCoA and P1 are of approximately equal size,
lengths and diam eters of the PCoAs or the P1 segm ents of the posterior but the left P1 is short. The junction of the PCoAs and the P2s are sharply
cerebral artery. (a) Superior view. The left PCoA is hypoplastic and the right angulated on both sides. (e) Inferior view. The left P1 is hypoplastic and the
is larger than its corresponding P1. The left PCoA is straight and short and left P2 arises m ainly from the PCoA. The right PCA arises predom inantly
the right is long and convex m edially. The right P2 segm ent is a direct con- from the basilar artery. (f) Large tortuous PCoAs alm ost touch in the m id-
tinuation of the PCoA. A m edial posterior choroidal artery courses medial line. The P2s arise predominantly from the large PCoAs, which are larger
to the left P2. Thalam operforating branches arise at the basilar bifurcation. than the P1 segm ents. Prem am illary perforating branches of the PCoA
(b) Both P1s arise predom inantly from the basilar artery. The hypoplastic arise on both sides. A., artery; AChA, anterior choroidal artery; Bas., basilar;
PCoAs course above and m edial to the oculom otor nerves. (c) The right Car., carotid; CN, cranial nerve; MPChA, medial posterior choroidal artery;
PCoA and P1 are of approxim ately equal size, and the junction of the PCoA PCoA, posterior com m unicating artery; Prem am ., prem am illary; SCA, su-
and the P2 is sharply angulated. The left P1 is directed anterior before join- perior cerebellar artery; Thal. Perf., thalam operforating. (Reprinted with
ing the junction of the P2 and the PCoA. The right PCoA is m uch longer perm ission from Rhoton AL Jr. The supratentorial arteries. Neurosurgery
than the left. (d) The right P1 arises predominantly from the PCoA. The 2002;51(Suppl):S53–120.)
right P1 segm ent is sm all and short, being only long enough to reach above

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Fig. 2.7a–j Anterior choroidal artery. Inferior views. (a) The right AChA enters the temporal horn by passing through the choroidal fissure located
arises from the posterior wall of the ICA above the origin of the PCoA and bet ween the thalam us above and the fim bria of the fornix below. The lat-
passes backward below the optic tract and lateral to the PCA. It ascends eral geniculate body form s the part of the thalam us above where the artery
around the medial surface of the uncus as it travels posteriorly. (b) The enters the choroidal fissure. The dentate gyrus is located at the lower edge
m edial part of the parahippocampal gyrus has been rem oved. The AChA of the fim bria. (d) The floor of the temporal horn and the fim bria have been
courses backward m edial to the anterior segm ent of the uncus to reach the rem oved to expose the AChA entering the choroid plexus of the temporal
uncal apex located at the junction of the anterior and posterior uncal seg- horn by passing through the choroidal fissure just behind the posterior
m ents where it turns laterally along the upper m argin of the posterior uncal segm ent of the uncus. The lower end of the choroidal fissure and the site
segm ent to reach the choroidal fissure. (c) The posterior uncal segment has where the artery passes through the fissure are called the inferior choroidal
been retracted. The AChA passes above the posterior uncal segm ent and point. (continued on page 24)

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g h

i j

Fig . 2.7a–j (continued ) (e ) Inferior view of the AChA. The lower part sella to the medial aspect of the internal carotid artery, uncus, and the ori-
of the right temporal pole has been rem oved to expose the AChA, which gin of the AChA. The AChA passes around the uncus to reach the lower end
passes backward to reach the m edial side of the optic tract where it turns of the choroidal fissure. (j) Medial view of another temporal lobe. The AChA
laterally, passing again below the optic tract and around the uncus to enter pursues an angulated course, descending along the anterior segm ent of
the temporal horn. (f) Lateral view. The right AChA arises above the origin the uncus, but at the uncal apex it turns sharply upward, reaching the
of the PCoA and passes upward and backward around the uncus to reach upper part of the posterior uncal segm ent before entering the temporal
the temporal horn. (g) Medial side of the right uncus. The AChA passes horn. A., artery; ACA, anterior cerebral artery; AChA, anterior choroidal ar-
around the m edial aspect of the uncus to reach the lower end of the choroi- tery; Ant., anterior; Bas., basilar; Car., carotid; Cist., cistern; Chor., choroid,
dal fissure where it enters the temporal horn. The PCA courses along the choroidal; CN, cranial nerve; Dent., dentate; Fiss., fissure; Gen., geniculate;
posterior aspect of the uncus. (h) The PCA has been rem oved. The AChA Gyr., gyrus; Hippo., hippocampus; Lat., lateral; LPChA, lateral posterior
ascends along the anterior segm ent of the uncus to reach the uncal apex choroidal artery; Lent. Str., lenticulostriate; MCA, m iddle cerebral artery;
where it turns laterally above the posterior uncal segm ent to enter the in- MPChA, m edial posterior choroidal artery; Olf., olfactory; PCA, posterior
ferior choroidal point at the lower end of the choroidal fissure located just cerebral artery; PCoA, posterior com m unicating artery; Parahippo., para-
behind the posterior uncal segm ent and the head of the hippocampus. The hippocampal; Plex., plexus; Post., posterior; SCA, superior cerebellar ar-
anterior uncal segm ent contains the amygdala and the posterior segment tery; Seg., segm ent; Temp., temporal; Tr., tract; V., vein; Vent., ventricle.
is form ed predom inantly by the head of the hippocampus. (i) Medial view (Reprinted with perm ission from Rhoton AL Jr. The supratentorial arteries.
of the right AChA in another specim en. The cross section extends through Neurosurgery 2002;51(Suppl):S53–120.)
the m idline of the sella. The view is directed laterally over the top of the

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 25

th e lateral m argin of th e cerebral p edu n cle. Th e ar ter y follow s gen u an d an terior th ird of th e in tern al capsule. If th e an terior
th e opt ic t ract for an average of 12 m m (range, 5 to 25 m m ).24 At ch oroidal ar ter y is sm all, t h e field of su p p ly of t h e PCoA m ay
th e an terior m argin of th e lateral gen icu late body, th e an terior en large to in clu de th e greater p ar t of t h e p osterior lim b of th e
ch oroidal ar ter y again crosses th e opt ic t ract m edially to laterally in tern al cap su le.25 Su ch inverse relat ion sh ip s, in w h ich on e ar-
an d passes posterolaterally th rough th e crural cistern , w h ich is ter y’s field of supply en larges as th e oth er ar ter y’s field con t ract s,
located bet w een th e cerebral p edu n cle an d u n cu s. It arrives su - occu r bet w een t h e PCA an d an ter ior ch oroidal ar ter y in ter m s
perom edially to th e u n cu s, w h ere it p asses th rough th e ch oroidal of th eir su pp ly to th e cerebral p edu n cle, su bst an t ia n igra, red
fissure to en ter th e ch oroid plexu s w ith in th e tem poral h orn. It n ucleus, subth alam ic n ucleus, opt ic t ract , an d lateral gen iculate
cou rses along th e m edial border of th e ch oroid p lexu s in close body. A large an terior ch oroidal ar ter y is usually associated w ith
relat ion to th e lateral posterior ch oroidal bran ch es of th e PCA. It a sm all PCoA on that side.
can p ass dorsally along th e m edial border of th e p lexu s, reach ing Th e p lexal segm en t u su ally origin ates as a single bran ch of
th e foram en of Mon ro in som e cases. the anterior choroidal arter y, w hich passes through th e choroidal
Th e an terior ch oroidal ar ter y is divided in to cistern al an d fissure. Addit ion al sm aller bran ch es to th e ch oroid plexus m ay
plexal segm en t s.24 Th e cistern al segm en t exten d s from th e ori- arise proxim al to the choroid fissure. These plexal branches divide
gin to th e ch oroidal fissu re an d is divided at th e an terior m argin and enter the m edial border of the choroid plexus of the tem poral
of th e lateral gen iculate body in to a proxim al an d dist al por t ion . horn to course in close relation to and often to anastom ose w ith
Th e p lexal segm en t is com p osed of on e or m ore bran ch es th at branches of the lateral posterior choroidal arteries. Som e branches
pass th rough th e ch oroidal fissu re to bran ch an d en ter th e ch o- of th e an terior ch oroidal ar ter y pass posterior in to th e ch oroid
roid p lexus of th e tem poral h orn . From its origin to its p assage plexus in th e at rium and then forw ard above the thalam us to sup -
th rough th e ch oroidal fissu re, it averages 2.4 cm long (range, 20 ply th e ch oroid plexus as far for w ard as th e foram en of Mon ro.
to 34 m m ). If th ere is a d ou ble ar ter y, th e distal bran ch usu ally Alm ost h alf of th e h em isph eres st udied h ave h ad an astom o-
term in ates in th e tem poral lobe. Th e proxim al bran ch n ou rish es ses bet w een th e PCA an d an terior ch oroidal ar ter y. Th e rich est
th e rem ain ing an terior ch oroidal ar ter y field. anastom oses are located on the surface of the choroid plexus w ith
Th e bran ch es, w h ich average n in e in n u m ber (range, fou r to th e lateral posterior ch oroidal bran ch es of th e PCA. An astom oses
18), are divided on th e basis of w h eth er th ey arise from th e cis- bet w een th e an terior ch oroidal ar ter y an d PCA are also foun d on
tern al or plexal segm en t . Th e bran ch es from th e cistern al seg- th e lateral su rface of th e lateral gen icu late body an d on th e tem -
m en t p en et rate, in decreasing order of frequ en cy, th e opt ic t ract , poral lobe near the un cus. These com plex and variable anastom o-
un cu s, cerebral p edu n cle, tem p oral h orn , lateral gen iculate body, ses m ake it difficu lt to pred ict th e effects of occlu sion of a single
h ippocam pu s, den tate gyru s an d forn ix, an d an terior perforated an terior ch oroidal arter y an d explain som e of th e in con sisten t
su bstan ce. Th ese bran ch es u su ally su pp ly th e opt ic t ract , lateral ou tcom es associated w ith an terior ch oroidal ar ter y occlusion .
par t of th e gen icu late body, p osterior t w o-th irds of th e posterior An average of fou r (range, on e to n in e) perforat ing bran ch es
lim b of th e in tern al cap su le, m ost of th e globu s pallidu s, th e ori- arise from th e ch oroidal segm en t . Most arise from th e posterior
gin of th e opt ic radiat ion s, an d th e m iddle th ird of th e cerebral h alf of th e ar ter ial w all an d ter m in ate, in d escen d in g ord er of
pedun cle. Less com m on ly, th e bran ch es sup ply p ar t of th e h ead frequen cy, in th e an terior p erforated substan ce, opt ic t ract , an d
of th e caudate n ucleus, pyriform cor tex, un cus, posterior m edial u n cus.
p ar t of t h e am ygdaloid n u cleu s, su bst an t ia n igra, red n u cleu s,
su bth alam ic n u cleus, an d su perficial asp ect of th e ven t rolateral
n ucleus of th e th alam us. How ever, n on e of th ese st ruct ures are
alw ays sup plied by th e ar ter y. In abou t t w o-th irds of th e h em i- ■ Microsurgical Anatomy of the
sph eres, th e ar ter y supplies th e m edial par t of th e globus palli- Vertebral Arteries
du s, th e p osterior lim b an d ret rolen t icu lar p ar t of th e in tern al
cap sule, th e opt ic tract , an d th e lateral gen iculate body. No st r u c- Th e p aired ver tebral ar ter ies (VAs) are t h e first an d largest
t ure oth er th an th e ch oroid plexus of th e tem poral h orn receives bran ch es of th e su bclavian ar teries. Th ey arise from th e subcla-
bran ch es in ever y case. In about h alf of th e h em isph eres, th e ar- vian arteries, u sually ascen d th rough th e t ran sverse processes of
ter y su pplies th e lateral par t of th e globus pallidu s an d th e cau- th e u pp er six cer vical ver tebrae, p ass beh in d th e lateral m asses
date t ail. In a th ird of th e h em isp h eres, it su p plies th e th alam u s, of th e atlas, en ter th e dura m ater beh in d th e occipit al con dyles,
hypoth alam u s, an d su bth alam u s. ascen d th rough th e foram en m agn u m to th e fron t of th e m e-
Th ere is a m arked in terch angeabilit y of th e field su pp lied by du lla, an d join th e con t ralateral VA to form th e basilar ar ter y at
th e an terior ch oroidal ar ter y an d t h e n earby bran ch es of C4, PCA, th e p on tom edu llar y ju n ct ion . Each ar ter y is divided in to in t ra-
PCoA, an d MCA. C4 frequ en tly gives rise to sm all ar teries dist rib - du ral an d ext radu ral p ar t s. Th e ext radu ral par t is d ivided in to
uted to th e areas com m on ly su p plied by th e p roxim al bran ch es th ree segm en t s (V1, V2, an d V3), an d th e in t rad u ral p ar t form s
of th e an terior ch oroidal ar ter y. Th ese ar teries, as m any as fou r, th e V4 segm en t .26
arise from th e posterior w all of th e carot id ar ter y bet w een th e
PCoA an d an terior ch oroidal ar ter y. Th ey also frequ en tly term i-
n ate, in decreasing order of frequ en cy, in th e opt ic t ract , an terior
V1 Segment
perforated su bstan ce, u n cu s, hyp oth alam u s, p it u itar y stalk, an d Th e first segm en t (V1), also called th e ost ial segm en t , ascen ds
cerebral p edu n cle.23 from it s origin in th e su bclavian ar ter y to reach th e C6 t ran sverse
An ot h er exam p le of t h e in terch angeabilit y of field occu rs process (Fig. 2.8a,b). Th e V1 segm en t is easily iden t ified am ong
w ith in t h e in tern al cap su le. If t h e PCoA is sm all, t h e an ter ior th e oth er bran ch es of th e su bclavian arter y an d th e thyrocer vical
ch oroidal ar ter y m ay assu m e it s n orm al area of su pp ly to th e an d th e costocer vical t r un ks because of th e absen ce of proxim al
(text cont inues on page 29)

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26 I Developm ent, Anatomy, and Physiology of the Central Nervous System

a b

c d

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e f g

h j

Fig. 2.8a–l V1 and V2 segm ents of the vertebral artery (VA). (a) Dissec- ond segment of the VA (V2) ascends through the transverse foram ina of
tion of the lower cervical level and cervicothoracic junction, right side. The the upper six cervical vertebrae anterior to the cervical nerve roots. The right
clavicle and subclavian vein have been rem oved. The internal jugular vein V2 is hidden behind the intertransverse m uscles, which have been rem oved
and com m on carotid artery have been divided. The VA is the first branch of on the left side to expose the artery. (e,f) Oblique (e) and posterior (f) view
the subclavian artery, located behind the com m on carotid artery, jugular of the V2 and V3 segm ents of the VA and its relationship to the atlas and
vein, and CN X. In this specim en, its origin can be seen behind the inferior axis. The V3 portion passes behind the lateral m ass of the atlas before en-
thyroid artery. The phrenic nerve is lateral to the VA. (b) Close view of the tering the dura m ater of the posterior fossa. Other classifications consider
sam e dissection. The inferior thyroid artery has been retracted m edially to the portion bet ween the transverse foram ina of C2 and C1 as part of V3
show the V1 segm ent of the VA, which comprises the trajectory from the segm ent. (g ) The VA is anterior to the cervical nerve root. (h,i) Dissection
origin at the subclavian artery to the entrance into the transverse foram ina. of the VA lateral view. The VA deviates laterally and anteriorly to reach the
The m ost comm on entry point is the sixth cervical vertebra, although it is transverse foramen of C1. The ram i of the cervical roots course posterior to
variable. The V1 is encountered in the VA triangle bet ween the m edial the VA. (j) Superior view of the spinal canal at the level of the atlas. The V3
aspect of the anterior scalene m uscle, the lateral aspect of the longus colli segm ent passes m edially along the upper surface of the posterior arch of
m uscle, and the subclavian artery. In this specim en, the inferior thyroid ar- the atlas to reach the dura. The m uscular branches of the VA supply the
tery arises as an independent artery instead of arising from the thyrocervi- deep muscles of the neck, near the lateral mass of the atlas, and anastomose
cal trunk. (c) Cervical vertebrae and articulated dry skull. The VA has been with branches of the occipital, ascending pharyngeal, and cervical arteries.
represented with m olding m aterial to show its V2 segm ent passing through (continued on page 28)
the transverse foram ina. (d) Cervical spine and VA, anterior view. The sec-

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k

Fig. 2.8a–l (continued ) (k) Craniocervical junction, posterior view. The V3 artery; Ant., anterior; Art., arterial; Artic., articular; Asc., ascending; Atl., at-
extends from the foram en in the transverse process of the atlas to the site lanto.; Br., branch; Cap., capitis; Car., carotid; Com m ., com m on; CN, cranial
of passage through the dura m ater and is intim ately related to the foram en nerve; Dent., dentate; Dors., dorsal; ECA, external carotid artery; Gang.,
m agnum and craniovertebral junction. (l) Enlarged view. The V3 segment ganglion; Horiz., horizontal; ICA, internal carotid artery; Inf., inferior; Int.,
is divided in three portions: a vertical portion just above the transverse pro- internal; Jug., jugular; Lat., lateralis; Lig., ligam ent; M., m uscle; Men., m en-
cess of C1; a horizontal portion in the groove of the posterior arch of the ingeal; Musc., muscular; N., nerve; Occip., occipital; PICA, posterior inferior
atlas; and an oblique portion extending from the m edial edge of the groove cerebellar artery; Post., posterior; Proc., process; Rec., rectus; Sup., supe-
in the upper surface of the atlas to the dural entrance. The upper at tach- rior; Tr., trunk; Transv., transverse; V., vein; Vent., ventral; Vert., vertical.
m ent of the dentate ligam ent and the spinal portion of the accessory nerve (d,h–l: Reprinted with perm ission from Campero A, Rubio PA, Rhoton AL.
ascend behind the V4. The rootlets of the hypoglossal nerve pass laterally Anatomy of the vertebral artery. In: George B, Bruneau M, Spet zler R, eds.
behind the V4. The posterior spinal artery gives rise to branches that as- Pathology and Surgery Around the Vertebral Artery. Paris: Springer-Verlag
cend and descend along the posterolateral aspect of the spinal cord. A., France; 2011.)

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 29

bran ch es. Th e V1 segm en t m ost often origin ates from th e cran ial C3-C6 level, th e ar ter y can be fou n d ~ 13 m m lateral to th e m id-
or posterior aspect of th e subclavian ar ter y an d less frequen tly por t ion of th e ver tebral body. At th e C3- C6 levels th e dist an ce is
from its an terior asp ect . sh or ter th an at th e C2 level becau se th e VA follow s a m ore lateral
Th e first segm en t exten ds from th e origin at th e su bclavian cou rse as it ascen d s to reach th e t ran sverse foram in a of atlas. If
ar ter y to it s en t ran ce in to th e low est t ran sverse foram en , usually th e u n cin ate p rocess at th e C3- C6 level is th e lan dm ark, th e VA
at th e C6 ver tebral level. Som et im es, h ow ever, it can en ter th e can be fou n d alm ost 2 m m laterally.31–33
t ran sverse foram in a at th e level of th e fifth , fou r th , or seven th
cer vical ver tebrae. In a st udy of 700 VAs, th e ar ter y en tered th e
C6 t ran sverse p rocess in 94.9% of th e specim en s.27 An abn orm al
V3 Segment
VA en t ran ce w as obser ved in 5.1% of th e sp ecim en s w it h en - Th e th ird segm en t (V3) of th e VA is in t im ately related to th e fora-
t ran ce in to t h e C4, C5, or C7 t ran sverse foram en in 1.6%, 3.3%, m en m agn u m an d cran iovertebral jun ct ion . It exten ds from th e
an d 0.3% of th e sp ecim en s, resp ect ively. foram en in th e t ran sverse process of th e atlas to th e site of pas-
Th e first segm en t is sit u ated in a t riangle, th e t riangle of th e sage th rough th e du ra m ater (Figs. 2.8, 2.9, 2.10).34–37 Oth er au -
VA, bou n d by th e lateral edge of th e longu s colli m uscle, th e m e- th ors con sider th e V3 segm en t to exten d from th e t ran sverse
dial edge of th e an terior scalen e m u scle, an d th e first par t of th e foram en of C2 to th e dura m ater of th e foram en m agnu m .37 Th e
su bclavian ar ter y. In t w o of 36 cases (5.6%) w ith an abn orm al VA V3 segm en t , w h ich h as a com p lex cou rse du e to th e m obile bon e
en t ran ce, th e ext raosseou s VA form ed an u n u su al m edial loop, st r u ct u res th rough w h ich it passes, preser ves vascular flow du r-
an d th e cen ter of th e VA w as posit ion ed m edial to th e longus ing rot at ion of th e n eck. Th e C2 t ran sverse p rocess h as an obliqu e
colli m u scle.27 Th is t riangle h ouses th e first por t ion of th e VA as lateral an d in ferior orien tat ion as opp osed to all oth er cer vical
w ell as th e vertebral vein , w h ich is p osit ion ed m ore an teriorly. t ran sverse processes, w h ich are h orizon t al an d perpen dicu lar to
Th e V1 segm en t is sit u ated beh in d th e in tern al jugu lar an d ver- th e ver tebral bodies. Th erefore, to reach th e C2 t ran sverse pro-
tebral vein s, beh in d th e CCA an d vagu s n er ve, bet w een th e lon - cess from C3, th e VA m u st ascen d laterally.
gus colli an d an terior scalen e m uscles, an d just an terior to th e V3 is d ivid ed in to t h ree p or t ion s: a ver t ical p or t ion t h at as-
t ran sverse p rocess of th e seven th cer vical ver tebra. cends through the transverse processes of C1, a horizontal portion
Th e V1 segm en t is crossed an teriorly by th e in ferior thyroid th at cou rses in th e groove on th e u pp er su rface of th e p osterior
ar ter y, th e th oracic du ct on th e left side an d righ t lym ph at ic du ct arch of th e atlas, an d an oblique por t ion th at pen et rates th e dura
on th e righ t side, an d th e an sa su bclavia from th e sym path et ic m ater (Fig. 2.8l). After passing th rough th e t ran sverse p rocess of
ch ain . Th e in ferior thyroid ar ter y crosses th e an terior su rface of th e atlas, th e ar ter y is located on th e m edial side of th e rect u s
th e su p erior par t of th e V1 segm en t . Th e t h oracic du ct , as it as- capitis lateralis m uscle. The third segm ent passes m edially behin d
cen ds from th e posterior m ediast in um to th e CCA before flow ing th e lateral m ass of th e at las an d atlan tooccip it al join t (Figs. 2.8,
in to th e jugular su bclavian ven ou s ju n ct ion , crosses th e an terior 2.9, 2.10) an d is pressed in to th e groove on th e upper surface of
su rface of th e left V1 segm en t . Th e righ t lym p h at ic du ct does th e th e lateral p ar t of th e posterior arch of th e atlas. Th ere, it courses
sam e on t h e righ t sid e. Th e in ferior cer vical ganglion is fu sed along th e floor of th e suboccipital t riangle form ed by th e rect us
w ith th e first th oracic ganglion to form th e stellate ganglion at capitis posterior m ajor and th e superior and inferior oblique m us-
th e m edial border of th e VA at th e level of th e first costover tebral cles an d is p ar t ially covered by t h e p oster ior at lan to -occip it al
ju n ct ion . Th e an sa su bclavia, w h ich p asses arou n d th e su bcla- m em bran e an d sem isp in alis cap it is m u scle (Fig. 2.10).38 It is
vian ar ter y to for m a loop con n ect in g t h e m id d le an d in fer ior su r roun ded by a ven ous plexus form ed by an astom oses bet w een
cer vical ganglia, crosses th e VA an teriorly (Fig. 2.8a,b). th e deep cer vical an d epid ural vein s.
Th e V1 segm en t is u nprotected by bony st ru ct u res an d at risk Th e VA en ters th e ver tebral can al by passing an terior to th e
of inju r y w h en t h e m u scles arou n d it are d ivid ed . Th u s, recog- lateral border of th e atlan to-occipit al m em bran e. Th e C1 ner ve
n izing th e variat ion s in w h ere it en ters th e t ran sverse foram en root passes th rough th e dura m ater on t h e low er surface of t h e
on preoperat ive invest igat ion s is im por tan t to avoid in adver ten t VA bet w een th e ar ter y an d th e groove on th e p osterior arch of
dam age. On com p u ted tom ograp hy (CT), an em pt y t ran sverse th e atlas. Th is bony groove on th e u p per su rface of th e p osterior
foram en is sm all or absen t . In su ch a case, t h e d ifferen t ial d iag- arch of th e atlas is frequ en tly t ran sform ed in to a bony can al th at
n osis w it h an at ret ic or a hyp op last ic VA m ay be resolved by com p letely su r rou n d s a sh or t segm en t of t h e ar ter y. In a p revi-
contrast-enhanced CT, m agnetic resonance (MR) im aging, and CT ou s st u dy of 50 ar ter ies,39 24 (48%) ar ter ies w ere in a sh allow
or MR angiograp hy.28–30 groove; 12 (24%) w ere p ar t ially, but in com pletely, surroun ded by
bon e; an d 14 (28%) cou rsed th rough a bony ring th at com p letely
surrou n ded th e ar ter y. Th e term in al ext radu ral segm en t of th e
V2 Segment VA gives rise to th e p osterior m en ingeal an d posterior sp in al ar-
Th e secon d segm en t (V2) of th e VA ascen ds th rough th e t ran s- teries, bran ch es to th e deep cer vical m uscu lat ure, an d occasion -
verse foram in a of th e u p p er six cer vical ver tebrae in fron t of th e ally th e posterior in ferior cerebellar ar ter y (PICA).39 Th e dist an ce
cer vical n er ve root s (Fig. 2.8c,d). In th ese foram in a, th e ar ter y is bet w een th e posterior m idlin e an d th e site of th e dural en t ran ce
covered by th e in ter t ran sverse m u scles. It is accom pan ied by a is ~ 12 m m .
plexu s of n er ves from th e in ferior sym p ath et ic ganglion an d is
su rrou n ded by a ven ou s p lexu s, w h ich u n ites to form th e ver te-
bral vein . Th is segm en t deviates laterally just above th e axis to
V4 Segment
reach th e m ore laterally placed t ran sverse foram en of th e atlas Th e in t rad u ral segm en t of th e VA (V4) begin s at th e du ral foram -
(Fig. 2.8). Th e relat ion ship bet w een th is segm en t an d som e an a- in a just in ferior to th e lateral edge of th e foram en m agn u m (Figs.
tom ic lan dm arks can be useful during a surgical exposure. At th e 2.9 and 2.10). In this region the dura is m uch thicker than in other
(text cont inues on page 32)

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30 I Developm ent, Anatomy, and Physiology of the Central Nervous System

a b

c d

Fig. 2.9a–h Posterior view. (a) The V3 passes m edially behind the lateral view. The m edulla has been rem oved. The C1 nerve roots penetrate the
m ass of the atlas and atlanto-occipital joint. The posterior inferior cere- dura with the VA. The V4 and the dura lining the anterior m argin of the fo-
bellar arteries (PICAs) arise from the intradural segm ent (V4) of the VA. ram en m agnum have been rem oved to expose the tectorial mem brane, a
(b) Foramen m agnum , posterior view. The posterior spinal arteries usually rostral extension of the posterior longitudinal ligam ent, and the vertebral
arise from the posterom edial surface of the V3, just outside the dura m ater. venous plexus, which courses just outside the dura. (h) The tectorial mem -
The left PICA arises just outside the dura. (c) Enlarged view. The V4 begins brane has been rem oved to expose the cruciform and alar ligam ents. The
at the dural foram ina located just below the lateral edge of the foram en horizontal portion of the cruciform ligament, called the transverse ligament
m agnum . The dura in this region is m uch thicker where it form s a funnel- of the atlas, extends laterally to at tach to the m edial edges of the lateral
shaped foram en around a 4 to 6 m m length of the artery. The left PICA m asses of the atlas, and the vertical portion ascends to at tach to the ante-
arises just outside the dura from the V3 and penetrates the dura with the rior m argin of the foram en m agnum deep to the tectorial m em brane. The
VA. The upper at tachm ent of the dentate ligam ent and the accessory nerve alar ligam ents pass upward and laterally from the dens and at tach to the
ascend behind the VA. (d) The right PICA arises just outside the dura from lateral edges of the foram en m agnum . The anterior m eningeal arteries
the V3. (e –h) Stepwise posterior dissection. (e ) Enlarged view of left half course along the dura and ligam entous structures in the anterior spinal
of the foram en m agnum . The VA passes behind and below the atlanto- canal. A., artery; AICA, anterior inferior cerebellar artery; Ant., anterior; Asc.,
occipital joint, penetrates the dura, and passes in front of the dentate liga- ascending; Atl., atlanto; Bas., basilar; Br., branch; Cap., capitis; CN, cranial
m ent, accessory nerve, and rootlets form ing the C1 nerve. The rostral end nerve; Cond., condylar, condyle; Cruc., cruciform ; Dent., dentate; Desc.,
of the dentate ligam ent at taches to the dura at the level of the foramen descending; Gang., ganglion; Horiz., horizontal; Inf., inferior; Lat., lateralis;
magnum. The C1 nerve penetrates the dura with the VA and posterior spinal Lig., ligam ent; M., m uscle; Mem b., m em brane; Men., meningeal; Musc.,
artery. The hypoglossal rootlets pass behind the V4 and are separated into m uscular; Obl., oblique; Occip., occipital; PICA, posterior inferior cerebellar
several bundles as they penetrate the dura to reach the hypoglossal canal. artery; Plex., plexus; Post., posterior; Rec., rectus; SCA, superior cerebellar
The posterior spinal artery arises as the VA enters the dura and gives rise to artery; Trans., transverse; V., vein; VA, vertebral artery; Vert., vertebral, ver-
ascending and descending branches. Several bundles of hypoglossal root- tical. (Reprinted with permission from Campero A, Rubio PA, Rhoton AL.
lets penetrate the dura at different sites. (f) The right half of the medulla Anatomy of the vertebral artery. In: George B, Bruneau M, Spet zler R, eds.
has been removed to expose the vertebrobasilar junction, and the origin of Pathology and Surgery Around the Vertebral Artery. Paris: Springer-Verlag
the anterior spinal artery. The anterior spinal artery arises predom inantly France; 2011.)
from the left V4 with a small contribution from the right V4. (g) Enlarged

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e f

g h

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32 I Developm ent, Anatomy, and Physiology of the Central Nervous System

areas, an d it form s a fun n el-sh aped foram en aroun d a 4 to 6 m m var y su lcu s. Th e an terior m ed u llar y segm en t begin s at th e preo-
length of th e ar ter y (Fig. 2.10). Th e first cer vical n er ve exit s th e livar y su lcus, cou rses in fron t of or bet w een th e hypoglossal
spinal canal, and the posterior spinal arter y enters the spinal canal rootlets, an d crosses th e pyram id to join th e oth er VA at or n ear
th rough th is du ral foram en w ith th e VA. Fibrou s du ral ban ds t h e p on tom ed u llar y su lcu s to for m t h e basilar ar ter y. As t h ey
bin d these th ree st ru ct ures togeth er at th e foram en . Th e in it ial ascen d, th e an terior an d lateral su rfaces of th e lateral m edullar y
in t radural segm en t of th e VA p asses ju st su perior to th e dorsal segm en t s face t h e occip it al con dyles, hyp oglossal can als, an d
an d vent ral root s of th e first cer vical n er ve an d just an terior to jugu lar t u bercles. Th e an terior m edu llar y segm en t s rest on th e
th e posterior sp in al ar ter y, den tate ligam en t , an d spin al p or t ion clivu s (Fig. 2.9).40
of th e accessor y n er ve.
On ce in side th e du ra m ater, th e VA ascen ds from th e low er
lateral to th e u p per an terior su rface of th e m edu lla (Figs. 2.9 an d
VA Branches
2.10). Th e in t radural par t of th e ar ter y is divided in to lateral an d Bran ch es arising from th e VA can be divided in to t w o grou ps.
an terior m edullar y segm en ts. Th e lateral m edu llar y segm en t be- Th e cer vicosp in al grou p in clu des th e lateral sp in al an d m u scu lar
gin s at th e dural foram en an d passes an terior an d su perior along ar teries. Th e cran ial group located in th e region of th e foram en
th e lateral m edu llar y su rface to term in ate lateral to th e p reoli- m agn um an d th e cran iovertebral jun ct ion in cludes th e posterior

a b

c d

Fig. 2.10a–h Exposure of the V3 in the suboccipital triangle. (a) The su- minor m uscle have been reflected inferior and m edially. The superior and
perficial m uscles have been reflected to expose the suboccipital triangles inferior oblique m uscles have been reflected downward. The V3 passes be-
form ed by the superior and inferior oblique and rectus capitis posterior hind the atlantal condyle, gives rise to a posterior m eningeal branch, and
m ajor m uscles. The superior oblique m uscle extends from the occipital penetrates the posterior atlanto-occipital m em brane to enter the dura. The
bone to the transverse process of C1; the inferior oblique m uscle extends rectus capitis lateralis m uscle extends from the transverse process of C1
from the transverse process of C1 to the spinous process of C2; and the to the occipital bone behind the jugular foram en. (d) The m uscles form ing
rectus capitis posterior m ajor m uscle extends from the occipital bone to the margins of another right suboccipital triangle and the venous plexus
the spinous process of C2. The V3 passes m edially across the upper surface around the V3 have been rem oved. The V3 gives rise to the posterior m en-
of the posterior arch of C1 in the depths of the suboccipital triangle, where ingeal artery, which ascends through the foram en m agnum and along the
it is em bedded in a venous plexus. (b) Posterolateral view. The occipital occipital dura. A V3 m uscular branch has been divided. The C1 nerve
artery passes behind the superior oblique m uscle. (c) The rectus capitis courses bet ween the VA and the posterior arch of the atlas.
posterior major muscle and the adjacent part of the rectus capitis posterior

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e f

Fig. 2.10a–h (continued ) (e) A suboccipital craniotomy has been com - clivus. The dentate ligam ent and accessory nerve ascend through the fora-
pleted and the posterior arch of the atlas has been rem oved. The V3 passes m en m agnum and behind the V4. The rostral at tachment of the dentate
behind and partially hides the atlanto-occipital joint. The PICA arises just ligam ent is at the level of the foram en m agnum . (h) The m edial part of the
outside the dura and penetrates the dura with the VA. The dentate liga- right occipital condyle and the posterior arch of C1 have been rem oved.
m ent and spinal accessory nerve ascend behind the V4. The rootlets of the The V3, which norm ally courses above the C1 nerve root, has been m obi-
hypoglossal nerve are stretched around the posterior surface of the V4. The lized and retracted below the level of the C1 nerve root. The right V4 has
rostral at tachment of the dentate ligam ent is at the level of the foram en been retracted posteriorly to provide access to the cervicom edullary re-
m agnum . CNs IX, X, and XI pass behind the V4 to enter the jugular fora- gion. The contralateral V4 is exposed anterior to the medulla. Hypoglossal
m en. (f) The dural incision completely encircles the junction of the V3 and rootlets pass behind the VA. The condylar drilling has provided wide access
V4, leaving a narrow dural cuff on the artery and therefore allowing the to the lower clivus and to the lateral and anterior surfaces of the m edulla.
artery to be m obilized. The drilling in the supracondylar area exposes the A., artery; Atl., atlanto.; Br., branch; Cap., capitis; CN, cranial nerve; Cond.,
hypoglossal nerve in the hypoglossal canal and can be extended extradu- condylar, condyle; Dent., dentate; Dors., dorsal; Flocc., flocculus; Inf., infe-
rally to the level of the jugular tubercles to increase access to the front of rior; Int., internal; Jug., jugular; Lat., lateralis; Lev., levator; Lig., ligam ent;
the brainstem and clivus. (g) Comparison of the far-lateral and transcondy- M., m uscle; Mem b., m em brane; Men., m eningeal; Musc., m uscular; Obl.,
lar exposure. The far-lateral exposure on the right side extends to the pos- oblique; Occip., occipital; PICA, posterior inferior cerebellar artery; Plex.,
terior edge of the m edial m argin of the atlantal and occipital condyles and plexus; Post., posterior; Proc., process; Rec., rectus; Scap., scapula; Sig.,
the atlanto-occipital joint. The prom inence of the condyles on the right sigmoid; Suboccip., suboccipital; Sup., superior; Triang., triangle; Transv.,
side lim its the exposure along the anterolateral m argin of the foram en transverse; Tuber., tubercle; V., vein; Vent., ventral, ventricle; VA, vertebral
m agnum . On the left side, a transcondylar exposure has been completed artery. (Reprinted with permission from Campero A, Rubio PA, Rhoton AL.
by rem oving the upper part of the occipital condyle. The dura can be re- Anatomy of the vertebral artery. In: George B, Bruneau M, Spet zler R, eds.
flected further laterally with the transcondylar approach than with the far Pathology and Surgery Around the Vertebral Artery. Paris: Springer-Verlag
lateral approach. The condylar drilling provides an increased angle of view France; 2011.)
and additional space for exposure and dissection along the brainstem and

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34 I Developm ent, Anatomy, and Physiology of the Central Nervous System

an d anterior spin al ar teries, an terior an d posterior m en ingeal an d p5, cor t ical.43 Each segm en t m ay be form ed by m ore th an
ar teries, an d th e PICAs. on e t r un k, depen ding on th e level of bifu rcat ion of th e ar ter y.
Th e p 1 segm en t lies an terior to th e m edu lla. It begin s at th e
origin of th e PICA an terior to th e m edulla an d exten ds backw ard
Cervicospinal Group
p ast t h e hyp oglossal root let s to t h e level of a rost rocau dal lin e
Th e lateral sp in al bran ch es en ter th e sp in al can al th rough th e t h rough t h e m ost p rom in en t p ar t of t h e in fer ior olive, w h ich
in ter ver tebral foram in a an d divide in to bran ch es th at pass along m arks th e bou n dar y bet w een th e an terior an d lateral su rfaces of
th e dorsal an d ven t ral n er ve root s to reach an d su pp ly th e su r- th e m ed u lla. Th e p2 segm en t begin s w h ere th e ar ter y p asses th e
roun ding p ar t of th e sp in al cord an d it s m em bran es. Th ey an as- m ost lateral p rom in en ce of th e olive an d en ds at th e level of th e
tom ose w ith ar teries from adjacen t levels. Th ese bran ch es also origin of the glossophar yngeal, vagus, and accessor y rootlets. This
d ivid e in to ascen d ing an d d escen d ing bran ch es t h at an asto - segm en t is p resen t in m ost PICAs. Th e p 3 segm en t begin s w h ere
m ose w ith ascen ding an d descen ding bran ch es from adjacen t th e PICA passes p osterior to th e glossoph ar yngeal, vagu s, an d ac-
levels (Fig. 2.9e ). Th e lateral spin al bran ch es also give rise to cessor y n er ves an d exten ds m edially across th e posterior aspect
sm all bran ch es n ear th e at tach m en t of th e p edicles. Th ese sm all of th e m edulla n ear th e cau dal h alf of th e ton sil.
bran ch es supply th e vertebral body an d periosteu m an d join sim - Th e p 4 segm en t is th e m ost com p lex of th e segm en t s. It be-
ilar bran ch es from th e con t ralateral side to create a cen t ral an as- gin s at th e m idport ion of w h ere th e PICAs ascen d along th e m e-
tom ot ic ch ain on th e p osterior su rface of th e ver tebral body.5 dial su rface of th e ton sil tow ard th e roof of th e fou r th ven t ricle.
Mu scu lar bran ch es su p ply th e deep m u scles of th e n eck, n ear It en ds w h ere it exit s th e fissures bet w een th e verm is, ton sil, an d
th e lateral m ass of t h e atlas, an d an astom ose w ith t h e occipit al, h em isphere to reach the suboccipital surface. This segm ent form s
ascen ding ph ar yngeal, an d cer vical ar teries (Figs. 2.8 an d 2.9). a loop w ith a convex rost ral cur ve, called th e cran ial loop. Th e
apex of th e cran ial loop usually cou rses bet w een th e cran ial pole
of th e ton sil an d the cen t ral part of th e in ferior m edullar y velum .
Cranial Group
Th is segm en t gives rise to bran ch es th at su pp ly th e tela ch oroi-
Th e p osterior sp in al ar ter y u su ally arises from th e posterom e- dea an d ch oroid plexu s of th e fou r th ven t ricle. Th e p 5 segm en t
dial su rface of th e VA, ju st ou tside th e du ra m ater (Fig. 2.8k,l). It begin s w h ere th e trun ks an d bran ch es leave th e groove bet w een
can also arise from th e in it ial in t radu ral part of th e VA or from th e verm is m edially an d th e ton sil an d th e h em isph ere laterally.
th e PICA. W h en th e du ra is op en ed, care sh ou ld be taken to pre- It in cludes th e term in al cor t ical bran ch es.
ser ve th e p osterior sp in al ar ter y becau se it m ay be in corp orated Most PICAs bifu rcate in to a sm aller m edial an d a larger lateral
in to th e du ral cuff aroun d th e VA. As th e p osterior sp in al arter y t ru n k. Th e m edial t r u n k su p p lies th e verm is an d adjacen t p ar t of
passes th rough th e du ra m ater, it is su rrou n d ed by th e sam e fi- th e h em isph ere, an d th e lateral t ru n k su p p lies m ost of th e h em i-
brous t un n el as th e VA an d th e first cer vical n er ve root . In th e sph eric an d ton sillar par ts of th e suboccipital surface. Th e PICA
su barach n oid space, it cou rses m edially beh in d th e rost ral-m ost an d its t run ks give rise to perforat ing bran ch es to th e m edu lla,
at t ach m en t s of t h e d en t ate ligam en t . On reach ing t h e low er ch oroidal ar teries th at su p ply th e tela ch oroidea an d ch oroid
m edu lla it divides in to ascen ding an d descen ding bran ch es. Th e plexu s, an d cor t ical ar teries. Th e cor t ical ar teries form ing th e p5
ascen ding bran ch courses th rough th e foram en m agn um an d segm en t are divided in to m edian an d p aram edian verm ian , ton -
sup plies th e rest iform body, gracile an d cu n eate t u bercles, root- sillar, and m edial, in term ediate, an d lateral h em isph eric arteries.
let s of th e accessor y n er ve, an d th e ch oroid p lexu s. Th e descen d- Th e perforat ing ar teries are sm all ar teries th at arise from th e
ing bran ch p asses dow nw ard bet w een th e dorsal rootlet s an d th ree m edu llar y segm en t s an d term in ate in th e brain stem . Th ey
th e den t ate ligam en t on th e p osterolateral su rface of th e sp in al are divided in to direct an d circum flex t ypes. Th e direct t ype pur-
cord . Th is bran ch su p plies th e su p erficial par t of th e dorsal h alf su es a st raigh t cou rse to en ter th e brain stem . Th e circu m flex
of th e cer vical spin al cord. It an astom oses w ith th e posterior t ype passes arou n d th e brain stem before term in at ing in it .
bran ch es of th e radicular ar teries en tering th e ver tebral foram en Th e an terior sp in al arter y is form ed by t h e u n ion of t h e paired
at low er levels.35,37 an terior spin al ar teries, w h ich origin ate from th e an terior m ed-
Th e PICA, th e largest bran ch of th e VA (Figs. 2.9, 2.10, 2.11), u llar y segm en t of th e VA n ear th e origin of th e basilar arter y (Fig.
usually origin ates w ith in th e d u ra m ater. In frequen tly, it origi- 2.9). In m ost brain stem s t h e ju n ct ion of t h e an ter ior sp in al ar-
n ates from th e term in al ext radural par t of th e VA (Fig. 2.9).39,40 It ter ies is located above th e level of th e foram en m agn um n ear th e
usu ally arises from th e VA n ear th e in ferior olive an d passes pos- low er en d of th e olives.
teriorly aroun d th e m edulla. At th e an terolateral m argin of the Th e m en ingeal ar teries, plu s th e an terior m en ingeal bran ch of
m edu lla, it passes rost ral or caudal to or bet w een th e rootlet s of m en ingohypop hyseal t ru n k an d th e m en ingeal bran ch es of th e
th e hyp oglossal n er ve. At th e p osterolateral m argin of th e m e- ascen ding ph ar yngeal an d occipit al arteries, supply all of th e du ra
dulla, it courses rost ral to or bet w een th e fila of the glossopharyn- lin ing th e posterior cran ial fossa bran ch es. Th e an terior m en in -
geal, vagus, an d accessor y n er ves. After passing th e lat ter n er ves, geal branch of the VA arises from the m edial surfaces of the extra-
it cou rses arou n d th e cerebellar ton sil an d en ters th e cerebello- du ral p ar t of th e VA im m ediately above th e t ran sverse foram en
m edu llar y fissure an d passes posterior to th e low er h alf of the of the third cer vical vertebra. This branch supplies the dura m ater
roof of th e fou rth ven t ricle. On exit ing th e cerebellom edullary in th e region of the clivus an d th e an terior part of th e foram en
fissure, its branches are distributed to the verm is and hem isphere m agn um an d u pp er spin al can al (Fig. 2.8h).
of t h e su boccip it al su r face. Bran ch es from PICA in clu d e p er fo- Th e posterior m en ingeal ar ter y arises from th e p osterosu pe-
rat ing, ch oroidal, an d cor t ical ar teries. Th e cor t ical ar teries are rior su rface of th e VA as it cou rses arou n d th e lateral m ass of th e
divided in to verm ian , ton sillar, an d h em isp h eric group s.41,42 Th e atlas (Fig. 2.10c,d), above th e posterior arch or ju st before it pen -
PICA is divided in to five segm en ts: p 1, an terior m ed u llar y; p 2, et rates th e dura. How ever, if it h as an in t radural origin , it pen e-
lateral m edu llar y; p 3, ton sillom ed u llar y; p4, teloveloton sillar; t rates th e arach n oid to reach th e du ra.35,37,40

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2 Microsurgical Anatomy of the Internal Carotid and Vertebral Arteries 35

a b

Fig. 2.11a–d Relationships of the V4. (a) Posterior view. Once inside the
dura mater, the V4 ascends from the lower lateral to the upper anterior
surface of the m edulla and joins its m ate of the opposite side near the pon-
tom edullary junction to form the basilar artery. The intradural part of the
V4 is divided, based on its relationship to the m edulla, into lateral and an-
terior medullary segm ents. The artery ascends anterior to CNs IX, X, XI, and
XII. The PICA usually arises from the V4 and the AICA from the basilar ar-
tery. (b) Anterior view of another specim en. The distal V4s com m only devi-
ate from the m idline toward or into one cerebellopontine (CP) angle. In this
case, the distal V4s have deviated into the left CP angle. (c) Anterior view.
The anterior arch of the atlas has been rem oved and the clivus opened. The
V4s deviate toward the left CP angle and join near the pontomedullary
c junction to form the basilar artery. The right PICA arises in front of the me-
dulla and the left PICA arises at the anterior part of the lateral edge of the
medulla. The C1 nerve exits the dura along the lower margin of the junction
of the V3 and V4. The m ost rostral dentate ligament at taches to the dura
posterior to the V4. (d) Endoscopic view through the transnasal approach.
These V4s join near the pontom edullary junction to form the basilar artery.
The abducens nerve arises in the m edial part of the pontomedullary junc-
tion. A., artery; AICA, anterior inferior cerebellar artery; Ant., anterior; Bas.,
basilar; Car., carotid; CN, cranial nerve; Dent., dent ate; Lat., lateral; Lig.,
ligam ent ; Med., m edial; N., nerve; Pet., petrous; PICA, posterior inferior
cerebellar artery; Proc., process; SCA, superior cerebellar artery; Seg., seg-
ment; Transv., transverse. (Reprinted with perm ission from Campero A,
Rubio PA, Rhoton AL. Anatomy of the vertebral artery. In: George B, Bru-
neau M, Spetzler R, eds. Pathology and Surgery Around the Vertebral Artery.
Paris: Springer-Verlag France; 2011.)

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36 I Developm ent, Anatomy, and Physiology of the Central Nervous System

an d Ch apters 3 an d 4, on th e an atom y of t h e an ter ior an d p os-


■ Conclusion terior circu lat ion , are essen t ial for pract it ion ers an d t rain ees.
Th e t reat m en t of cerebrovascu lar path ology dep en d s on a solid Master y of cerebrovascular an atom y en ables th e safe, precise,
u n derst an ding of n orm al, varian t , an d abn orm al an atom y of th e an d effect ive t reat m en t of in t racran ial p ath ologies.
blood vessels of th e brain an d surroun ding t issues. Th is ch apter

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carot id collar. Neurosurger y 2002;51(4, Suppl):S375–S410 process, in tert ran sverse space, an d vertebral arter y in an terior approach es
11. Joo W, Fun aki T, Yosh ioka F, Rh oton AL Jr. Microsurgical an atom y of th e to the lower cervical spine. J Neurosurg 2003;98(2, Suppl):188–194
carotid cave. Neurosurger y 2012;70(2, Suppl Operative):300–311, discus- 33. Russo VM, Grazian o F, Peris- Celda M, Russo A, Ulm AJ. Th e V(2) segm en t
sion 311–312 of th e ver tebral ar ter y: an atom ical con siderat ion s an d surgical im plica-
12. Rhoton AL Jr. The supratentorial arteries. Neurosurgery 2002;51(4, Suppl): t ion s. J Neurosu rg Spin e 2011;15:610–619
S53–S120 34. Br un eau M, Corn elius JF, George B. An tero-lateral approach to th e V3 seg-
13. Cam pero A, Cam pero AA, Mar t in s C, Yasuda A, Rhoton AL Jr. Surgical an at- m ent of th e ver tebral ar ter y. Neurosurger y 2006;58(1, Suppl):ONS29–
om y of th e du ral w alls of th e cavern ous sin us. J Clin Neu rosci 2010;17: ONS35, discu ssion ONS29–ONS35
746–750 35. Rh oton AL Jr. Th e foram en m agn u m . Neu rosu rger y 2000;47(3, Su p p l)
14. In ou e T, Rh oton AL Jr, Th eele D, Bar r y ME. Su rgical ap p roach es to t h e S155–S193
caver n ou s sin u s: a m icrosu rgical st u dy. Neu rosu rger y 1990;26:903– 36. Rh oton AL, de Oliverira E. An atom ical basis of surgical approach es to th e
932 region of th e foram en m agnum . In : Dickm an CA, Spetzler RF, Son ntag VKH,
15. Martins C, Yasuda A, Cam pero A, Ulm AJ, Tan riover N, Rh oton A Jr. Micro- eds. Surger y of th e Cran iover tebral Jun ct ion . New York: Th iem e Medical
su rgical an atom y of th e dural arteries. Neu rosurger y 2005;56(2, Suppl): Publish ers; 1998:13–57
211–251, discu ssion 211–251 37. Wen HT, Rh oton AL Jr, Kat sut a T, de Oliveira E. Microsu rgical an atom y of
16. Gibo H, Len key C, Rh oton AL Jr. Microsurgical an atom y of th e supraclin oid th e t ran scon dylar, su pracon dylar, an d p aracon dylar exten sion s of th e far-
portion of the internal carotid artery. J Neurosurg 1981;55:560–574 lateral approach . J Neu rosurg 1997;87:555–585
17. Liu Q, Rh oton AL Jr. Middle m en ingeal origin of th e oph th alm ic ar ter y. 38. Gupt a T. Quan t it at ive an atom y of ver tebral ar ter y groove on th e posterior
Neurosu rger y 2001;49:401–406, discu ssion 406–407 arch of at las in relat ion to sp in al su rgical p rocedu res. Su rg Radiol An at
18. Ren n W H, Rh oton AL Jr. Microsu rgical an atom y of th e sellar region . J Neu- 2008;30:239–242
rosurg 1975;43:288–298 39. Fin e AD, Cardoso A, Rhoton AL Jr. Microsu rgical an atom y of th e ext racra-
19. Harris F, Rh oton AL Jr. Microsu rgical anatom y of the cavernou s sin us. Su rg n ial-ext radural origin of th e posterior in ferior cerebellar ar ter y. J Neuro-
Foru m 1975;26:462–463 surg 1999;91:645–652
20. Fujii K, Len key C, Rh oton AL Jr. Microsurgical an atom y of th e choroidal 40. de Oliveira E, Rh oton AL Jr, Peace D. Microsurgical an atom y of the region
arteries: lateral and third ventricles. J Neurosurg 1980;52:165–188 of th e foram en m agn u m . Su rg Neu rol 1985;24:293–352
21. Epstein F, Ran soh off J, Bu dzilovich GN. Th e clin ical sign ifican ce of jun c- 41. Lister JR, Rh oton AL Jr, Mat su shim a T, Peace DA. Microsurgical an atom y of
t ion al d ilat at ion of t h e p oster ior com m u n icat in g ar ter y. J Neu rosu rg th e posterior in ferior cerebellar ar ter y. Neu rosurger y 1982;10:170–199
1970;33:529–531 42. Mat sush im a T, Rh oton AL Jr, Len key C. Microsu rger y of th e fou r th ven t ri-
22. Hassler O, Salt zm an GF. Histologic ch an ges in in fu n d ibu lar w id en ing of cle: Part 1. Microsurgical anatom y. Neurosurgery 1982;11:631–667
t h e p oster ior com m u n icat ing ar ter y. A p relim in ar y rep or t . Act a Pat h ol 43. Rodríguez-Hern án dez A, Rh oton AL Jr, Law ton MT. Segm en t al an atom y
Microbiol Scan d 1959;46:305–312 of cerebellar ar teries: a proposed n om en clat ure. Laborator y invest igat ion .
23. Saeki N, Rh oton AL Jr. Microsurgical an atom y of th e upper basilar arter y J Neu rosu rg 2011;115:387–397
an d th e posterior circle of Willis. J Neurosurg 1977;46:563–578

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3 Cranial Vascular Anatomy of the
Anterior Circulation
João Paulo C. de Alm eida, Feres Chaddad, Albert L. Rhoton, Jr., and Evandro de Oliveira

Vascular n eurosurger y is on e of th e m ost com plex areas in th e cur ves posterosu periorly at th e lim en in su la, form ing th e gen u of
field of n eurologic surger y. It requ ires exten sive laborator y t rain - th e MCA, to reach th e in su la surface (Fig. 3.2).
ing, several years of clin ical an d su rgical pract ice, an d acqu iring Th en , it m ay follow a superior or in ferior t rajector y, depen d-
an d m astering profou n d kn ow ledge of brain an atom y. It is also ing on th e level of th e carot id bifurcat ion .4 W h en th e bifurcat ion
vit al for m icrosu rgeon s to h ave sou n d kn ow ledge of th e m icro- is h igh because th e su praclin oid ICA is long, t h e arter y m ust
an atom y of th e brain circulat ion an d it s n eurovascular relat ion - cou rse in feriorly from th e an terior p erforated su bst an ce to pass
sh ip s.1 Com p reh en sive u n derst an ding of th e vascular an atom y, laterally below th e lim en in su la. W h en th e carot id bifu rcat ion is
in clu ding th e direct ion of th e vessels, an atom ic variat ion s, an as- low, th e MCA h as an ascen ding course.
tom ot ic an d collateral vessels, an atom y of th e perforators, an d Th e length of th e su p raclin oid ICA is im por t an t for plan n ing
areas of irrigat ion for each specific vascular t r un k is relevan t for surger y for an eur ysm s of th e carot id bifurcat ion , proxim al MCA,
th e t reat m en t of an eu r ysm s an d vascu lar m alform at ion s. Un d er- or proxim al ACA. In cases w ith a h igh carotid bifurcat ion , a m ore
st an ding th e m icroan atom y of th e cerebral vessels h elps su r- basal view th an th e on e provided th rough th e classic pterion al
geon s select th e m ost appropriate m icrosurgical or en dovascu lar approach is useful. In such cases, th e orbitozygom at ic approach
t reat m en t for pat ien ts. m ay h elp red u ce ret ract ion over th e fron t al lobe an d p rovide th e
Th is ch apter p resen t s th e m icrosu rgical an atom y of th e an te- addit ion al view required. At th e periph er y of th e in su la, th e MCA
rior circu lat ion , w ith em ph asis on th e an terior an d m iddle cere- bran ches pass to the m edial surface of the opercula of the frontal,
bral arteries an d th e an terior perforat ing bran ch es. Th e n euro- tem poral, an d parietal lobes. Th ey th en course arou n d th e oper-
vascu lar relat ion sh ip of th ese vessels an d an atom ic con siderat ion s cula to reach th e lateral port ion of th e in ferior su rfaces of th e
related to su rger y of an terior circu lat ion an eu r ysm s are an alyzed cerebral h em isph eres.
in detail.
Th e an ter ior circu lat ion (or t h e d ist r ibu t ion of t h e in ter n al
carot id arter y [ICA]) involves th e grou p of ar teries th at carries Sylvian Fissure
blood origin at ing from bot h ICAs. It in clu d es t h e ICA an d it s
Com preh en sion of th e an atom y of th e MCA requ ires u n derstan d-
bran ches, th e an terior cerebral ar teries (ACAs) an d m iddle cere-
ing th e st ru ct ure of th e sylvian fissu re. According to Gibo et al,2
bral ar teries (MCAs), an d th e perforators an d collateral vessels to
th e sylvian fissu re h as both a superficial an d a deep segm en t .
th e con t ralateral side an d to th e p osterior circu lat ion . Th e an at-
Th e su p erficial segm en t h as a stem an d th ree ram i: th e an te-
om y of th e posterior circu lat ion an d of th e ICA an d it s bran ch es
r ior h or izon t al, an ter ior ascen d ing, an d p oster ior ram i. Th e an -
are described in Ch apters 2 an d 4.
terior horizon tal an d th e an terior ascen ding ram i delim it the pars
t riangu laris of th e in ferior fron tal gyru s. Th e orbitalis por t ion of
th e in ferior fron tal gyrus is located an terior to th e an terior h ori-
zon t al ram u s. Th e op ercu lar p or t ion of in fer ior fron t al gyr u s is
■ Middle Cerebral Artery located p osterior to th e an terior ascen ding ram u s. Th e posterior
Th e MCA is th e largest term in al bran ch of th e ICA an d th e m ost ram us exten ds backw ard bet w een th e fron t al an d pariet al lobes
com p lex vessel of th e an terior circu lat ion . In th e p ast , su rgical above an d th e tem poral lobe below. Below th e pars t riangularis,
in terest in th e MCA h as been directed at avoiding dam age to its th e t h ree ram i m eet at th e lateral su rface of th e h em isp h ere. Th e
bran ch es du ring su rger y p erform ed w ith in it s territor y. Micro- su p erficial sylvian fissu re is larger at th is level becau se of sligh t
surgical tech n iques h ave m ade recon st ru ct ion an d byp ass to th e ret ract ion from th e pars t riangularis.4 Th erefore, t h is site is u su -
MCA, su rgical app roach es to MCA an eu r ysm s, an d resect ion of ally th e easiest at w h ich to begin dissect ion of th e sylvian fissure.
ar terioven ous m alform at ion s (AVMs) related to MCA bran ch es From th is point, the dissect ion m ay proceed an teriorly and deeper
com m on procedures in vascu lar n eu rosu rger y.2,3 or posteriorly if n ecessar y.
Th e origin of th e MCA is located at t h e carot id cistern at th e Th e deep (cistern al) segm en t of th e fissu re is divided in t w o
m edial en d of th e deep port ion of sylvian fissure, below th e an - por t ion s: an an terior por t ion called th e sp h en oidal segm en t , an d
terior perforated substan ce, lateral to th e opt ic ch iasm , an d pos- a posterior por t ion called th e operculoin sular com par t m en t . Th e
terior to th e olfactor y t ract division in to th e lateral an d m edial sph en oidal com par t m en t arises in th e region of th e lim en in su-
olfactor y st riae (Fig. 3.1). Th e diam eter of th e MCA at its origin lae at t h e lateral m argin of t h e an ter ior p er forated su bst an ce. It
ranges from 2.4 to 4.6 m m , alm ost t w ice th at of th e ACA.2 Th e is a n ar row sp ace p oster ior to t h e sp h en oid r idge bet w een t h e
MCA ru n s laterally from its origin , parallel to th e lesser sph en oi- fron t al an d tem p oral lobes an d com m u n icates m ed ially w it h
dal w ing an d ~ 1 cm p oster ior to sp h en oidal r idge. Th e ar ter y t h e carotid cistern . Th e operculoin sular com partm en t is located

37

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38 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 3.1 Surgical view of a left pretemporal


approach. The frontal lobe has been retracted
superiorly to show the bifurcation of the left in-
ternal carotid artery (2) into the m iddle cerebral
artery (MCA, 3), anterior cerebral artery (ACA,
4) and the ACA–anterior comm unicating artery
(ACoA) complex (6). The ACA runs m edially,
joins its contralateral m ate (5) through the an-
terior com m unicating artery above the optic
chiasm (1), and follows a superior and posterior
course within the interhem ispheric fissure. The
proxim al segm ent of the MCA (M1 segm ent)
runs laterally into the sylvian fissure and gives
rise to the m edial, interm ediate, and distal len-
ticulostriate arteries, which irrigate the basal
ganglia and internal capsule. 1, optic chiasm ; 2,
internal carotid artery bifurcation; 3, left MCA;
4, left ACA; 5, right ACA; 6, ACoA; and 7, olfac-
tory tract.

deep to th e su p erficial ram i of th e sylvian fissu re on th e lateral Th e sp h en oidal segm en t (M1) ru n s from th e origin of th e
su rface.5 It is form ed by t w o n arrow clefts: th e opercu lar cleft MCA at th e carot id bifurcat ion to th e lim en in sula. Th is segm en t
bet w een th e opposing lips of th e fron topariet al an d tem poral cou rses laterally in th e d eep par t of th e sylvian fissu re, ~ 1 cm
opercu la, an d th e in sular cleft bet w een th e in sula an d opercula. posterior to th e sp h en oidal ridge, crossing th e carot id an d syl-
Th e in sular cleft h as a su p erior lim b located bet w een th e in su la vian cistern s. An terior to th e lim en in sula, it m akes a 90-degree
an d frontoparietal operculum an d an in ferior lim b located be- t urn referred to as th e gen u of th e MCA. Th e M1 segm en t can be
t w een th e in sula an d tem poral op ercu lu m . An teriorly, th e sup e- divided in to t w o p or t ion s: th e prebifu rcat ion an d postbifu rca-
rior lim b h as m ore ver t ical h eigh t th an th e in ferior lim b, bu t t ion . Th e prebifu rcat ion p or t ion of M1 ru n s from th e origin of
posteriorly the height of the inferior lim b equals or is greater than th e MCA to th e bifu rcat ion of it s m ain t ru n k. Th e postbifu rcat ion
th e h eigh t of th e su p erior lim b.2 port ion is com p osed of th e bran ch es origin at ing from th e bifu r-
cat ion of th e MCA to th e gen u . In 86%of th e cases, th e bifu rcat ion
of th e MCA is proxim al to th e gen u (Fig. 3.3).2
Segments of the Middle Cerebral Artery Th e in su lar segm en t (M2) is com posed of th e t r u n ks an d
Classically, th e MCA is divided in fou r an atom ic segm en ts: M1, bran ch es of th e MCA th at lie on an d supply th e in sula. It begin s
th e sp h en oidal segm en t; M2, th e in su lar segm en t; M3, t h e op er- at th e gen u an d term in ates at th e circu lar su lcu s of th e in su la.
cu lar segm en t; an d M4, th e cor t ical segm en t .4 Th e M2 segm en t u su ally h as t w o m ain t ru n ks: an in ferior an d a

Fig. 3.2 Inferior view of the M1 segm ent (3),


carotid bifurcation (2), and anterior cerebral
artery–anterior com m unicating artery complex
(4, 11). 1, optic chiasm ; 2, internal carotid ar-
tery bifurcation; 3, right M1 segment; 4, right
anterior cerebral artery; 5, right olfactory tract;
6, posterior orbital gyrus; 7, genu of the right
m iddle cerebral artery; 8, lenticulostriate arter-
ies; 9, left M1 segm ent; 10, interhemispheric
fissure; and 11, anterior com m unicating artery.

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3 Cranial Vascular Anatomy of the Anterior Circulation 39
Fig. 3.3 Anterior view of the left m iddle cere-
bral artery (MCA) after resection of the anterior
portion of the right and left hem ispheres. The
origin of the left MCA is observed lateral to the
optic chiasm below the anterior perforated sub-
stance. The M1 segment (2) follows a lateral
course parallel to the lesser sphenoidal wing to
the lim en insula (5), where it curves 90 degrees
(genu of the MCA) toward the lateral surface of
the insula, giving rise to the M2 segm ent (6, 7).
In m ost cases, the MCA bifurcates proxim al to
the genu of the MCA. The perforating branches
(3) from the MCA can be observed in the photo-
graph running toward the anterior perforated
subst ance to irrigate the basal ganglia (11).
1, supraclinoidal internal carotid artery; 2, M1
segm ent; 3, lenticulostriate arteries; 4, bifurca-
tion of the MCA; 5, lim en insula; 6, superior
trunk of the MCA; 7, inferior trunk of the MCA;
8, anterior cerebral artery (A1); 9, anterior com -
m unicating artery; 10, insula; and 11, lentiform
nucleus.

su p erior t ru n k. In m ost cases, th e in ferior t ru n k is dom in an t , h as Perforating Branches of the Middle


a larger diam eter th an th e superior t ru n k, an d is respon sible for Cerebral Artery
irrigat ion of th e tem poral an d p arietal lobes. Th e greatest bran ch -
ing of th e MCA occu rs dist al to th e gen u at th e an terior port ion A group of t w o to 15 ar teries th at arises from th e proxim al MCA
of th e in sula. Th e cou rse of th e bran ch es directed to th e fron t al com p oses th e so-called len t icu lost riate ar teries. At th eir origin ,
an d tem poral lobes is relat ively sh or t . Th ey usually cross on ly th e th ese vessels form vascu lar loop s an d cou rse in to th e lateral t w o-
sh or t gyri of th e in su la. How ever, th e bran ch es to th e posterior th irds of th e an terior p erforated su bst an ce. App roxim ately 80%
por t ion of th e p ariet al lobe an d angu lar gyru s cross th e sh or t of th e len t iculost riate bran ch es arise from th e prebifurcat ion
gyri, cen t ral sulcus of th e in sula, an d long gyri before leaving th e por t ion of M1. Th e p ostbifu rcat ion segm en t is th e site of origin
in sular su rface (Fig. 3.4). of m ost of th e rem ain ing bran ch es; h ow ever, som e bran ch es also
Th e op ercu lar segm en t (M3) begin s at th e circu lar su lcu s of m ay arise from th e proxim al M2 segm en t . In t raoperat ive in spec-
th e in su la an d term in ates at th e su rface of th e sylvian fissu re. tion of such bran ches, an im portan t step in the surgical treat m ent
Th e M3 bran ch es are closely related to th e fron top ariet al an d of proxim al MCA an d carot id bifurcat ion an eur ysm s, requires
tem poral opercula, w h ich are crossed by th e ar terial bran ch es so gen tle ret ract ion of th e M1 segm en t because such bran ch es orig-
th at t h e su perficial por t ion of sylvian fissu re can be reach ed. Th e in ate at th e in ferior w all of th e proxim al MCA.
bran ch es to th e fron t al an d parietal lobes un dergo a double flex- According to Yaşargil,1 th e origin of th e len ticu lost riate ar ter-
ion to reach th e h em isph ere su rface.6 Th e first 180-degree t urn ies occurs in th ree pat tern s. Th e m ost com m on p at tern con sist s
or th e first loop is located at th e circular sulcus of th e in sula, of a single stem t run k origin at ing from th e in ferior w all of th e
w h ere th ose bran ch es t urn in feriorly over th e fron toparietal M1 segm en t . After 2 to 10 m m , th e vessel d ivides in to m u lt ip le
operculum to reach the convexit y of the brain . The second loop is perforat ing bran ch es (40% of th e cases). A secon d p at tern con -
sit uated at the surface of th e sylvian fissure w here those branches sists of t w o large parallel t r u n ks th at divide to form th e st riate
t urn superiorly tow ard th e lateral surface of th e parietal an d ar teries (30% of t h e cases). Th e t h ird p at tern is st riate ar teries
fron t al lobes. Th e first loop occu rs at th e an terior circu lar su lcu s. th at ar ise directly from th e in fer ior w all of th e proxim al MCA
On angiograph ic st udies, th e m ost posterior an d m edial loop, lo- (30% of th e cases).
cated in th e posterior p or t ion of th e in su la, is called th e sylvian Th e len t icu lost riate ar teries are d ivid ed in to m edial, in term e-
poin t . It is closely related to th e m ed ial en d of th e an terior t ran s- diate, an d lateral grou p s. In term s of it s com p osit ion , dist ribu -
verse tem poral gyrus (Hesch l’s gyr us). It is lateral to th e lateral tion, and m orphology, each group has unique characteristics. Th e
w all of th e at riu m of th e lateral ven tricles an d rep resen ts th e m ed ial grou p (th e least con st an t of th e t h ree grou p s) con sist s
posterior lim it of th e sylvian fissu re.5 Th e bran ch es directed to of on e to five bran ch es th at origin ate at th e posteroin ferior w all
th e tem p oral lobe follow a m ore regu lar cou rse. Th ey ru n along of th e m edial por t ion of th e prebifurcat ion M1 segm en t . Th ose
th e in ferior circu m feren ce of th e circu lar su lcu s of th e in su la an d bran ch es follow a relat ively direct course to th e an terior perfo-
then t urn upw ardly an d laterally on the m edial surface of the tem - rated subst an ce, pen et rat ing it just lateral to th e bran ch es origi-
poral op ercu lu m . On ce at th e su rface of th e sylvian fissu re, th ey n at ing from th e supraclinoid ICA an d en tering th e lateral zon e of
t urn in feriorly an d posteriorly tow ard th e lateral surface of th e th e an terior perforated subst an ce.
tem p oral lobe (Fig. 3.5). Th e in ter m ed iate grou p is obser ved in ~ 90% of t h e h em i-
Th e fin al segm en t of t h e MCA, t h e cor t ical segm en t (M4), sp h eres. It in clu d es at least on e m ajor ar ter y from w h ich or igi-
begin s at th e su rface of th e sylvian fissure an d exten ds over th e n ate as m any as 30 perforat ing bran ch es. On ly a few perforat ing
cort ical su rface of th e fron tal, tem poral, an d parietal lobes. bran ch es origin ate directly from th e MCA. Th is group arises from

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40 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 3.4a,b (a) Lateral view of the M2 seg-


m ent after retraction of the frontoparietal (4)
and temporal (5) opercula. The M2 segm ent (6)
begins at the genu and terminates at the circu-
lar sulcus of the insula. The superior and inferior
trunks of the m iddle cerebral artery are ob-
served crossing the lateral surface of the insula.
The branches directed to the frontal and tem -
poral lobes usually have a shorter course than
the branches to the parietal lobe. (b) Close up
of lateral view shown in part a. 1, short gyrus;
2, central sulcus of the insula; 3, long gyrus;
4, frontoparietal operculum ; 5, temporal oper-
culum ; and 6, M2 segm ent.

th e posterior or p osterosu perior w all of t h e prebifu rcat ion M1 or less from th e M1 bifurcat ion . Th erefore, careful in spect ion of
segm en t or from its early bran ch es an d ru n s tow ard th e an terior th ese ar teries an d th eir origin is recom m en ded before an d after
perforated subst an ce to p en et rate its lateral zon e. an eur ysm s are clipped at th is site.2
Th e lateral grou p is presen t in alm ost all cases. It is com posed
of an average of five len t icu lost riate bran ch es th at give rise to as
Middle Cerebral Artery Bifurcation
m any as 20 perforating arteries before they penetrate the postero-
lateral aspect of th e an terior perforated su bstan ce. Th is grou p of Th e MCA bifu rcat ion occu rs at th e h igh est p oin t of t h e lim en in -
ar teries m igh t origin ate from th e pre- or postbifurcat ion M1 seg- su la,1 proxim al to th e gen u of th e MCA in 86% of th e cases.2 As
m en t or from M2. Th ose bran ch es u su ally arise from th e poste- described, distal to th e bifu rcat ion , th e su p erior an d in ferior
rior aspect of th e MCA an d develop m u lt iple loops on th eir w ay t ru n ks t u rn posterosu p eriorly to reach th e su rface of th e in su la.
to th e an terior perforated su bst an ce.4 From th em origin ates th e gen u of th e MCA. Classically, th e bifu r-
Th e in t raop erat ive evalu at ion of th e relat ion sh ip bet w een th e cat ion region also m ay be described as form ing an “om ega” pat-
lateral len t iculost riate ar teries an d th e bifu rcat ion of th e MCA is ter n becau se of t h e in it ial d ivergen t bu t t h en convergen t rou te
crucial to con sider in th e t reat m en t of an eur ysm s involving th e of th e t run ks of th e MCA. Usually, th e diam eters of th e ar terial
MCA bifu rcat ion . Alm ost 30% of t h e lateral len t icu lost r iate ar- bran ch es n ear th e bifurcat ion are sim ilar to th ose of th e m ain
teries origin ate from th e pre- or postbifurcat ion t r un ks 2.0 m m t ru n ks. Con sequ en tly, it can app ear as if p seu dot rifurcat ion s or

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3 Cranial Vascular Anatomy of the Anterior Circulation 41
Fig. 3.5 Segm ents of the m iddle cerebral ar-
tery (MCA) shown in an anterior view of the an-
terior cerebral artery– anterior com municating
artery complex (2, 9) and MCAs after rem oval
of the anterior portion of the right and left cere-
bral hem ispheres. The MCA is divided into four
segm ents: M1 (from the origin of the artery
at the carotid bifurcation to the genu of MCA)
(1, 4, 5), M2 (from the genu of the MCA to the
circular sulcus of the insula) (6), M3 (from the
circular sulcus to the lateral surface of the hem i-
spheres) (7), and M4 (cortical branches) (8).
1, left M1 segm ent (prebifurcation part); 2, an-
terior cerebral artery (A1 segm ent); 3, recurrent
artery of Heubner; 4, right M1 segm ent; 5, left
M1 segm ent (postbifurcation part); 6, left M2
segm ent ; 7, left M3 segm ent; 8, cortical
branches of the MCA (M4); 9, anterior com m u-
nicating artery; 10, lim en insula; 11, right inter-
nal capsule; and 12, globus pallidus.

p seu d oqu ad r ifu rcat ion s are p resen t . How ever, a real t r ifu rca- are usually the branches selected for a superficial tem poral artery-
t ion of th e MCA occu rs in on ly 12% of th e h em isp h eres, an d to-MCA byp ass.4
m u lt ip le bran ch es h ave been seen in on ly 10% of t h e cases.2
Based on t h e sam e st u dy, t h e su p er ior t r u n k is d om in an t in
28% of cases, th e in ferior t ru n k is larger in 32%, both t run ks are Early Branches
of equal caliber in 18%, an d m ult iple t r un ks of various sizes are Early bran ch es are d efin ed as ar ter ies or igin at in g p roxim al to
fou n d in 22%.2 t h e bifu rcat ion of th e MCA.7 Th ose ar teries u su ally su p p ly th e
orbitofrontal and prefrontal areas in the frontal lobe and the tem -
poropolar an d an terior tem poral area in th e tem poral lobe.
Stem Arteries and Cortical Branches
Th e stem ar teries arise from th e m ain t ru n k of th e MCA or from
th e t ru n ks form ed after th e bifu rcat ion of th e ar ter y. Th e m ost Cortical Area
com m on pat tern is eigh t stem ar teries p er h em isph ere. From Th e cor t ical area su p plied by th e MCA m ay be divided in to 12
each of th ose ar teries origin ates on e to five cor t ical ar teries di- region s based on th e classificat ion proposed by Mich otey et al.8
rected to th e lateral or basal su rface of th e h em isph ere. Tw o stem Th e fron t al lobe is d ivided in to fou r region s: th e orbitofron t al,
ar teries are usually directed to th e fron t al lobe. On e stem gives prefron t al, precen t ral, an d cen t ral. Th e p arietal lobe in clu des th e
rise to th e orbitofron t al, p refron t al, an d p recen t ral ar teries, an d an terior an d posterior pariet al an d th e angu lar areas. Th e tem -
th e oth er stem gives rise to th e cen t ral arter y. Th e p ariet al lobe poral lobe is organ ized in to five areas: tem p oro-occip ital (also
receives t w o stem arteries from th e MCA. On e stem gives rise to su p plies p ar t of th e occip ital lobe); tem p orop olar; an d an terior,
th e an terior an d posterior p ariet al ar teries, an d th e oth er stem m iddle, an d posterior tem poral areas.
gives rise to th e angu lar ar ter y. Th e tem poral lobe h as m ore stem
ar ter ies th an t h e ot h er lobes su p p lied by t h e MCA. It u su ally
receives four bran ch es directed to th e tem poropolar, an terior,
m iddle, an d posterior tem p oral region s. ■ Anterior Cerebral Artery–Anterior
Th e cor t ical bran ch es are resp on sible for th e irrigat ion of th e
lateral an d basal su r face of th e h em isp h ere. From t h e in fer ior
Communicating Artery Complex
trunk of th e MCA originates th e tem poropolar; tem poro-occipital; An eur ysm s of th e ACA–an terior com m un icat ing ar ter y (ACoA)
angular; an d an terior, m iddle, an d posterior tem poral ar teries. com p lex are som e of t h e m ost com p lex lesion s in t h e field of
The orbitofrontal, prefrontal, precentral, and central arteries usu- vascu lar n eu rosu rger y. Th e m u lt ip le var iat ion s in t h e an atom y
ally arise from th e su p erior t run k. Th e origin of th e an terior an d of th e region an d th e relat ion sh ip of th e lesion w ith perforat ing
p oster ior p ar iet al ar ter ies is even ly divid ed bet w een t h e t w o vessels are u su ally respon sible for surgical com plicat ion s associ-
t r u n ks, an d th e lat ter u su ally arise from th e dom in an t tr un k. ated w ith clipping ACoA an eur ysm s. Aneur ysm s of th is area proj-
Th e cor t ical bran ch es of th e MCA are frequ en tly u sed du ring ect in d ifferen t d irect ion s t h at m ay obscu re t h e id en t ificat ion
bypass procedures. The largest cortical bran ches are th e tem poro- of th e m ain vessels of th e region an d of th e perforat ing vessels.
occip it al, angu lar, an d p oster ior tem p oral ar ter ies (m in im u m An ot h er cr it ical p oin t d u r ing t h e ap p roach to vascu lar lesion s
length 4 m m ). Therefore, these arteries (m ainly the angular branch) in th is area is iden t ificat ion of th e recurren t ar ter y of Heubn er.

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42 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 3.6 Surgical view of a right pretemporal


approach. The frontal lobe has been retracted
superiorly to show the bifurcation (6) of the left
internal carotid artery into the m iddle cerebral
artery (8) and anterior cerebral artery (ACA, 5)
and the ACA–anterior com m unicating artery
com plex. The proxim al ACA (A1 segm ent, 5)
originates from the internal carotid bifurcation
in the carotid cistern and runs m edially into the
lam ina term inalis cistern passing through a thin
layer of arachnoid m em brane (4). It anastom o-
ses with the contralateral ACA above the optic
chiasm (3). 1, right optic nerve; 2, left optic
nerve; 3, optic chiasm ; 4, arachnoid m em brane
bet ween the carotid and lam ina terminalis cis-
tern; 5, right A1 segm ent; 6, right internal ca-
rotid artery bifurcation; 7, right supraclinoidal
carotid artery; and 8, right M1 segm ent.

Lesion s associated w it h th is vessel h ave been associated w it h su m an d ter m in ates in th e ch oroid p lexu s in th e roof of th e th ird
h em ip aresis an d aph asia. ven t ricle (Fig. 3.7).4
Th e ACA is th e m edial bran ch origin at ing from th e bifu rca-
t ion of th e ICA. It arises in th e carot id cistern , below th e an terior
perforated su bst an ce (Fig. 3.6). Th e ACA cou rses an terom ed ially
Segments of the Anterior Cerebral Artery
in to t h e lam in a term in alis cister n an d over th e opt ic ch iasm to Th e ACA is divided in t w o m ain segm en t s: p roxim al an d dist al.9
en ter th e in terh em isp h er ic fissu re. Over th e opt ic ch iasm , th e Th e proxim al segm en t (A1) origin ates in th e carot id cistern , th e
ar ter y join s t h e con t ralateral ACA t h rough t h e ACoA before it sm allest bran ch th at origin ates from th e bifu rcat ion of th e ICA.
ascen ds in fron t of t h e lam in a ter m in alis to p ass in t h e lon gi- Th e diam eter of th e A1 segm en t ranges from 0.9 to 4.0 m m (aver-
t u din al fissu re bet w een th e cerebral h em isph eres. In th is par t age, 2.6 m m ) an d its length varies from 7.2 to 18.0 m m (average,
of it s cou rse, u su ally on e d ist al ACA lies in t h e con cavit y of th e 12.7 m m ). Th is segm en t r un s an terom edially tow ard th e lam in a
oth er. Beyon d th e lam in a ter m in alis, th e ar teries cu r ve arou n d term in alis cistern an d term in ates over th e opt ic ch iasm at th e
th e genu of th e cor pu s callosu m an d cou rse posteriorly above jun ct ion w ith th e con t ralateral A1 th rough th e ACoA. Longer A1
th e body of th e cor p u s callosu m in th e p er icallosal cister n . Th e segm en t s m ay h ave a m ore an terior cou rse an d m eet at th e level
ACA r u n s p osteriorly arou n d t h e sp len iu m of t h e corp u s callo- of th e opt ic n er ves (30%of th e cases). Both A1 segm en ts are u su-

Fig. 3.7 Sagit tal view of the m edial surface of


the right hem isphere shows the segm ents of
the distal anterior cerebral artery and its course
artery. The A2 (infracallosal) segment (1) begins
at the anterior com m unicating artery, passes
anterior to the lam ina terminalis, and term i-
nates at the junction of the rostrum (9) and
genu (10) of the corpus callosum . The A3 (pre-
callosal) segm ent (2) extends around the genu
of the corpus callosum and term inates where
the artery turns sharply posterior above the
genu. The A4 (supracallosal, 3) and A5 (postcal-
losal, 4) segm ents are located above the corpus
callosum and are separated into an anterior
(A4) and posterior (A5) portions by a point bi-
sected in the lateral view close behind the coro-
nal suture. 1, A2 segment; 2, A3 segment; 3, A4
segm ent; 4, A5 segm ent; 5, superior frontal
gyrus; 6, paracentral lobule; 7, cuneus; 8, pre-
cuneus; 9, rostrum of the corpus callosum ; 10,
genu; 11, body of the corpus callosum; 12, sple-
nium; and 13, callosom arginal artery.

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3 Cranial Vascular Anatomy of the Anterior Circulation 43

ally con n ected by a single ACoA, alth ough doubling or even t ri- Above th e lam in a term in alis, th e in fracallosal (A2) segm en t
pling of th is ar ter y m ay occur.9 describes a convex cu r ve orien ted an teriorly w ith in th e para-
In a n orm al ACA–ACoA com plex, th e ACoA con n ects A1s of olfactor y region . Th e n ext cur ve is aroun d th e rost r um an d h as a
alm ost equal size, an d both A1s an d th e ACoA are sufficien tly dorsal convexit y. A th ird cu r ve is convex an teriorly at th e low er
large to allow circu lat ion bet w een th e t w o carot id arteries an d aspect of th e gen u of th e corpus callosum . Th e ar ter y follow s a
th rough th e an terior circle of Willis.4 Th e diam eter of th e ACoA posterior cou rse to th e sp len iu m an d, in som e cases, to th e roof
averages 1 m m less th an th at of th e A1. A1 segm en t s w ith a di- of th e th ird ven t ricle.
am eter less th an 1.5 m m are con sidered hypoplast ic. Based on
th is criterion , 10% of all A1 segm en t s are hyp op last ic. A hypo-
plast ic A1 is associated w ith a h igh rate of an eu r ysm s; A1 is hy- Branches of the Anterior Cerebral Artery
pop last ic in 85% of cases w ith an ACoA an eu r ysm .10 Th e size of
Recurrent Artery of Heubner
th e ACoA is directly related to th e differen ce in size bet w een
th e A1 segm en ts. For exam ple, w h en th e diam eter of an ACoA is In m ost h em isph eres th e recu rren t ar ter y of Heubn er is th e larg-
large, th e diam eters of th e righ t an d left A1 differ con siderably. est ar ter y arising from th e A1 or from th e proxim al 0.5 m m of
Object ively, th e m ean diam eter of th e ACoA w as 1.2 m m in a th e A2. It t ypically arises from A2. Th e diam eter of th e recu rren t
group of brain s in w h ich th e differen ce in diam eter bet w een th e ar ter y is usually less th an th at of A1. How ever, in cases of hypo-
righ t an d left A1s w as 0.5 m m or less an d 2.5 m m if th e differ- plast ic A1 segm en t s, th is bran ch m ay be as large as or larger th an
en ce w as m ore th an 0.5 m m .9 th e diam eter of A1.9
Th e ACoA is n ot easily dem on st rated on angiograp h ic st u dies. Th e cou rse of th e recu rren t ar ter y of Heu bn er is u n iqu e in
It is u su ally or ien ted in an obliqu e or st raigh t an terop oster ior th at it d ou bles back on it s paren t ACA an d p asses above th e ca-
plan e. Th e A2 segm en ts are seldom side by side, m aking obliqu e rot id bifu rcat ion an d MCA in to t h e m ed ial p ar t of t h e sylvian
im aging n ecessar y to visu alize th e ACoA. fissu re before it en ters t h e an terior perforated su bst an ce (Fig.
Th e dist al segm en t of th e ACA is divided in to fou r por t ion s: 3.8). Th e recu rren t ar teries u su ally cou rse an terior to A1 an d are
A2, in fracallosal; A3, precallosal; A4, su p racallosal; an d A5, p os- visible w h en t h e fron t al lobe is elevated before t h e A1 can be
terocallosal. Th e in fracallosal (A2) segm en t begin s at th e ACoA, visualized. Th ey also can cou rse su perior to A1 or bet w een it an d
passes an terior to th e lam in a term in alis, an d term in ates at th e th e an terior perforated su bst an ce, or th ey can loop p osterior to
junct ion of th e rost r um an d gen u of th e corpu s callosum . Th e A1. In th eir t rajector y tow ard th e an terior perforated su bst an ce,
precallosal (A3) segm en t exten d s arou n d th e gen u of th e corp u s th e ar teries r u n above th e carot id bifu rcat ion an d th e p roxim al
callosu m an d term in ates w h ere th e ar ter y t u rn s sh arply p oste- part of MCA.
rior above th e gen u . Th e su p racallosal (A4) an d p ostcallosal (A5) During su rgical clipping of ACoA an eur ysm s, great care m ust
segm en t s are located above th e corp u s callosu m an d are sep a- be exer ted to avoid cu t t ing or occlu d ing t h e recu rren t ar ter y.
rated in to an an terior (A4) an d p osterior (A5) port ion by a poin t Th e vessel su p plies th e an terior cau date n u cleu s; an terior th ird
bisected in a lateral view located close beh in d th e coron al sut ure. of th e putam en ; an terior outer segm en t of th e globus pallidus;
Th e A2 an d A3 segm en t s togeth er an d A4 an d A5 h ave been re- an teroin ferior por t ion of th e an terior lim b of th e in tern al cap -
ferred to as th e ascen ding an d h orizon tal segm en t s, resp ect ively. sule; th e un cin ate fascicu lus; an d, less com m on ly, th e an terior
Th e term pericallosal artery is also u sed to describe th e postcom - hypoth alam us. Con sequen tly, it s occlusion can be associated w ith
m un icat ing, or d ist al, segm en t of th e ACA.4 h em iparesis w ith facial an d brach ial predom in an ce if th e bran ch

Fig. 3.8 Surgical view of a right pterional ap-


proach shows the origin of the recurrent artery
of Heubner (5) at the junction of the right ante-
rior cerebral artery (4) with the anterior com -
municating artery. The recurrent artery doubles
back on its parent anterior cerebral artery and
passes above the carotid bifurcation and m iddle
cerebral artery (3) into the m edial part of the
sylvian fissure before it enters the anterior per-
forated substance. 1, optic chiasm ; 2, right su-
praclinoidal internal carotid artery; 3, right M1
segm ent ; 4, right A1 segm ent ; and 5, right
recurrent artery of Heubner. (Figure reprinted
from Chaddad-Neto F, Campos Filho JM, Dória-
Net to HL, Faria MH, Ribas GC, Oliveira E: The
pterional craniotomy: Tips and Tricks. Arquivos de
Neuro-Psiquiatria, 70(9). 2012.)

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44 I Developm ent, Anatomy, and Physiology of the Central Nervous System

su p plying th e an terior lim b of th e in tern al cap su le is com pro- region (Fig. 3.10).11 Th e diam eter of th e pericallosal ar ter y is re-
m ised, an d w ith ap h asia if th e ar ter y is on th e dom in an t side.4 lated to th e size of the callosom argin al ar ter y. W h en th e calloso-
m argin al arter y is large, th e pericallosal arter y is usually sm aller
th an average.
Basal Perforating Branches
Th e an terior p ort ion of th e falx cerebri is con sisten tly n ar-
Th e an terior perforated su bst an ce, su bfron t al area, dorsal su r- row er th an it s posterior port ion . Th e free m argin of it s an terior
face of the optic chiasm , suprachiasm atic area, hypothalam us, and por t ion lies w ell above th e gen u of th e corp u s callosu m , w h ereas
sylvian fissu re receive basal p erforat ing bran ch es th at origin ate th e free m argin of it s posterior p or t ion is n ear th e sp len iu m . Th e
from A1 an d A2. Most of th ose bran ch es arise from th e lateral en t ire course of th e pericallosal ar ter y, except for its posterior
h alf of th e A1 segm en t (68% of th e basal perforat ing bran ch es), por t ion , is below th e free m argin of th e falx cerebri. Hen ce, th e
m ost ly from t h e su p er ior su r face of t h e vessel.9 Th e m ost im - ar ter y is free to sh ift across th e m idlin e. In con t rast , th e calloso-
p or tan t differen ce in term in at ion of A1 bran ch es com pared w ith m argin al arter y h as on ly it s m ost an terior port ion below th e free
t h ose of t h e recu r ren t ar ter y is t h e lack of recu r ren t ar ter y m argin of th e falx. Th e rem ain der lies above th e free edge, an d its
bran ch es to t h e d orsal su rface of t h e opt ic n er ves an d ch iasm disp lacem en t across th e m idlin e is lim ited by th e rigid it y of th e
an d to th e an terior hyp oth alam us an d th e greater n um ber of re- falx.4
curren t bran ch es en tering th e sylvian fissure. The A2 segm en t
m ay give rise to as m any as fou r basal p erforat ing bran ch es,
Cortical Branches
w h ich usu ally arise from th e lateral an d superior aspect s of th e
vessel an d are prim arily directed to th e gyru s rect us an d in ferior Th e cor t ical bran ch es of th e dist al ACA are p rim arily directed to-
fron tal area. Occasionally, the an terior perforated substance, dor- w ard th e m ed ial an d basal su rfaces of th e fron tal lobe an d m e-
sal opt ic ch iasm , an d su p rach iasm at ic region also are su pp lied by d ial su r face of t h e p ar iet al lobe. On t h e m ed ial su r face, t h e ACA
th e basal bran ch es from A2 (Fig. 3.9). is respon sible for irrigat ion of th e superior fron tal gyrus, cingu -
Th e ACoA sen ds basal p erforat ing bran ch es to t h e dorsal su r- late gyru s, p araolfactor y area, paracen t ral lobu le, an d corp u s cal-
face of th e opt ic ch iasm , su p rach iasm at ic area, and an terior p er- losu m . On t h e basal su r face, t h e ACA su p p lies t h e m ed ial p ar t
forated substan ce. Th ose bran ch es origin ate from th e superior of th e orbital gyri, gyru s rect us, an d olfactor y bulb an d t ract . Fi-
(54%), posterior (36%), an terior (7%), an d in ferior (3%) aspects of nally, the ACA also contributes to irrigation of a sm all cortical area
th e ar ter y.4 in th e lateral su rface of th e fron t al an d p ariet al lobes, in cluding
th e su perior fron t al gyr u s an d su p erior p ar t s of th e p recen t ral,
cen t ral, an d postcen t ral gyri (Figs. 3.11 an d 3.12).9,11
Callosomarginal Artery
Eigh t cor t ical bran ch es usually origin ate from th e ACA: th e
Th e callosom argin al ar ter y is th e m ain bran ch origin at ing from orbitofron tal, fron topolar, an d paracen t ral ar teries; th e in tern al
th e dist al ACA. It r u n s in or n ear th e cingu late su lcu s, alm ost p ar- fron t al grou p (an ter ior, m id d le, an d p oster ior fron t al ar teries);
allel to th e p ericallosal ar ter y. It gives rise to at least t w o cor t ical an d t h e p ar iet al grou p (su p er ior an d in fer ior p ar iet al ar ter ies).
bran ch es to th e m edial surface of th e h em isph eres. Th e calloso- Th e orbitofron t al ar ter y or igin ates from t h e A2 segm en t as a
m argin al arter y can origin ate from anyw h ere bet w een th e proxi- single bran ch or as a com m on t r u n k w ith th e fron topolar ar ter y.
m al port ion of A2 (just distal to th e ACA) an d th e gen u of th e From it s origin , it ru n s tow ard th e floor of th e an terior fossa to
corp u s callosu m , bu t it u su ally arises from th e p recallosal (A3) th e level of th e p lan u m sp h en oidale. It su p plies th e gyru s rect u s,

Fig . 3.9 Basal view of the anterior cerebral


artery (2, 3)–anterior com m unicating artery
(ACoA, 1) complex after retraction of the optic
nerves. The ACA runs m edially to anastom ose
with it s contralateral m ate over the optic chi-
asm . The A2 segm ent follows a superior course
into the hem ispheric fissure to irrigate part of
the m edial surface of the hem ispheres. The per-
forating branches from the A1 course toward
the anterior perforated substance. At the A1–
ACoA junction, the origin of the recurrent ar-
tery (4) is usually observed. This branch runs
laterally toward the anterior perforated sub-
stance to irrigate the caudate, put am en, and
anterior lim b of the internal capsule. 1, ACoA; 2,
A2 segm ent; 3, left A1 segm ent; 4, right recur-
rent artery of Heubner; and 5, left recurrent
artery of Heubner.

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3 Cranial Vascular Anatomy of the Anterior Circulation 45
Fig. 3.10 Midsagit tal view to the level of the
body of the corpus callosum and coronal cut
through the left frontal lobe and insula. In this
case, the distal segm ent of the anterior cerebral
artery gives rise to the callosom arginal artery
at the infracallosal segm ent. Usually, such a
branch arises from the A3 segm ent of the ante-
rior cerebral artery. The callosomarginal artery
then runs in the cingulate sulcus, parallel to the
pericallosal artery. 1, left A1 segm ent; 2, left A2
segm ent; 3, left callosom arginal artery; 4, genu
of the corpus callosum ; 5, cingulate gyrus; and
6, left m iddle cerebral artery.

Fig. 3.11 Anterior view of brain. The anterior


cerebral artery is m ainly responsible for irrigat-
ing the basal and medial frontal and parietal
lobes, whereas the middle cerebral artery (MCA)
is responsible for irrigating m ost of the lateral
surface of the hem ispheres. 1, right A1 seg-
m ent; 2, right frontopolar branch; 3, left in-
ternal frontal branches; 4, orbital gyri; 5, right
MCA; 6, right temporopolar artery; 7, perforat-
ing branches from the left A1 segm ent; 8, optic
chiasm ; 9, left MCA bifurcation; and 10, left syl-
vian fissure.

Fig. 3.12 Sagit tal view of the m edial surface


of the left hem isphere. On the m edial surface,
the anterior cerebral artery is responsible for
irrigating the superior frontal gyrus, cingulate
gyrus, paraolfactory area, paracentral lobule,
and corpus callosum . 1, right A1; 2, left A1;
3, right A2; 4, left A2; 5, right callosom arginal
artery; 6, genu of the corpus callosum ; 7, sep-
tum pellucidum ; 8, falx; 9, frontopolar branch;
and 10, fronto-orbital branch.

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46 I Developm ent, Anatomy, and Physiology of the Central Nervous System

olfactor y bulb an d t ract , an d m edial par t of th e orbital gyri of th e Th e an terior p erforated su bst an ce can be divided both m edio-
fron t al lobe. In 90% of cases, th e fron top olar ar ter y arises from laterally an d an terop osteriorly to classify th e poin t of en t r y of
th e pericallosal ar ter y.11 It ru n s along th e m edial su rface of th e th e perforat ing bran ch es from th e ICA, ACA, an d MCA.12 Th e site
h em isp h eres tow ard t h e fron t al p ole to ir r igate t h e m ed ial an d of pen et rat ion in th e m ediolateral direct ion w as determ in ed in
lateral su rfaces of th e fron t al lobe. relat ion to a lin e passing posteriorly along th e olfactor y t ract .
Th e in tern al fron t al ar teries arise from t h e A3 segm en t an d Th is lin e crosses th e an terior perforated su bst an ce at it s largest
are d irected tow ard t h e m ed ial an d lateral su r faces of t h e su p e- an teroposterior dim en sion an d t ran sects th e opt ic t ract as it
r ior fron t al gyr u s. Th e an ter ior fron t al ar ter y su p p lies t h e an te- passes the cerebral peduncles. The m edial zone includes the space
r ior p or t ion of t h e su p er ior fron t al gyr u s. Th e m id d le fron t al bet w een th e m ediolateral lin e an d in terh em isph eric fissure. Th e
ar ter y su pp lies th e m iddle port ion of th e sup erior fron tal gyr us. lateral zon e exten d s from t h e m ed iolateral lin e to t h e sylvian
Fin ally, th e p osterior fron tal ar ter y su p plies th e p osterior par t of fissu re an d lim en in su la. W h en th e an terior perforated su b -
th e sup erior fron tal gyrus an d par t of th e cingu late gyru s. st an ce is divided in an an teroposterior direct ion , th ree zon es are
Th e p aracen t ral arter y arises from A4 or th e callosom argin al obser ved: an ter ior, m id d le, an d p oster ior. Th ese zon es exten d
ar ter y. It u su ally cou rses an terior to th e m argin al lim b of th e cin - across th e full w idth of th e an terior perforated substance, from
gulate sulcus or in th e paracen t ral sulcu s before it t u rn s vert i- th e in terh em isph eric fissu re to th e lim en in sula.
cally to th e su perior port ion of th e paracen t ral lobu le. Th ere, it
su p plies a port ion of th e p rem otor, m otor, an d som at ic sen sor y
areas. It m ay represen t the term in al por t ion of th e ACA. Th e pa- Perforating Branches from the Internal
riet al ar teries are resp on sible for su p p lying th e area p osterior to Carotid Artery
th e p aracen t ral lobu le. Those vessels arise from A4 or A5, course
Th e an terior perforat ing bran ch es from th e ICA arise exclu sively
n ear th e splen ium of th e corpus callosum , an d sen d bran ch es to
from it s ch oroidal segm en t . On e to n in e bran ch es (average, 3.9)
th e precun eus an d, in som e cases, cu n eu s n u cleu s.
arise from th e posterior w all of th e ar ter y dist al to th e origin of
t h e an ter ior ch oroidal ar ter y.12 Most of t h ose bran ch es origi-
Callosal Branches n ate proxim al to th e carot id bifurcat ion (80%); on ly 20% of th e
perforat ing vessels from th e ICA arise at th e bifu rcat ion . Th e p er-
Th e ACA is th e prin cip al ar ter y t h at su pp lies t h e corpu s callo-
forat ing bran ch es r un in a posterosuperior direct ion tow ard th e
sum . It sen ds bran ch es th at su pp ly th e rost r u m , gen u , body, an d
anterior perforated substance, near the optic tract. A sim ilar num -
splen iu m of th e corpus callosum . Th e bran ch es respon sible for
ber of perforat ing vessels pen et rate th e lateral an d m edial por-
such irrigat ion are th e sh or t an d long callosal ar teries. Th e sh or t
t ion s of th e an terior p erforated su bst an ce. Based on th e an tero-
callosal ar teries arise from th e pericallosal ar ter y an d p en et rate
posterior division , m ost of th e p erforators p en et rate th e p osterior
directly into the corpus callosum . These bran ches supply the cor-
an d m iddle division s; on ly 5% en ter th e an terior perforated sub -
pu s callosu m , an d th ey con t in u e th rough it to su p p ly th e sept u m
st an ce th rough th e an terior division . Th e bran ch es from th e ICA
pellu cidu m , an terior p illars of th e forn ix, an d p ar t of th e an terior
overlap w ith th e perforat ing vessels from oth er arteries, m ain ly
com m issu re. Th e long callosal ar teries arise from th e p ericallosal
w ith th ose from th e an terior ch oroidal ar ter y. Perforators from
ar ter y an d cou rse parallel to it , bet w een th e lateral vessel an d
th e lat ter u su ally p en et rate th e posterior zon e of th e an terior
th e su rface of th e corp u s callosu m , to give rise to callosal p erfo-
perforated su bstan ce. Th ere is n o an astom osis in th e su barach -
rat ing bran ch es. Besides sen ding bran ch es to th e corpus callo-
n oid space bet w een th e perforating bran ch es from th e ICA an d
su m , cor t ical bran ch es m ay su p ply adjacen t cor tex as w ell as th e
vessels origin at ing from oth er arteries.
septal n u clei, sept u m p ellu cidu m , an d u p p er p or t ion s of th e col-
u m n of th e forn ix.4
Perforating Branches from the Anterior
Choroidal Artery
■ Anterior Perforating Arteries The anterior choroidal artery sends one to 10 perforating branches
to th e an terior perforated substan ce (average, 2.2).12,13 Th e per-
The anterior perforating arteries, a group of vessels that originates forat ing bran ch es from th e an terior ch oroidal ar ter y h ave th ree
from th e ICAs, ACAs, an d MCAs, p en et rate th e brain th rough th e possible pat tern s. In th e first p at tern , w h ich is presen t in h alf of
an terior perforated substan ce.12 Th e locat ion of th ose vessels in th e h em isp h eres, on e to th ree perforat ing bran ch es arise w ith
th e basal su rface of th e fron t al lobe, n ear im por t an t sites w h ere th e an terior ch oroidal ar ter y an d sen d bran ch es to t h e an terior
an eur ysm s develop, m akes it crucial to u n derstan d th eir m icro- perforated su bstan ce. In th e secon d pat tern , th e m ain t r u n k of
an atom y. Erron eou s clipping of a perforat ing vessel can be asso- th e an terior ch oroidal ar ter y sen ds bran ch es directly to th e an te-
ciated w ith cat ast rop h ic com plicat ion s. rior perforated substance. In the third pat tern, the superior branch
from th e bifu rcat ion of t h e an terior ch oroidal ar ter y sen ds perfo-
rat ing bran ch es to th e an terior perforated su bst an ce. Most of th e
Anterior Perforated Substance perforat ing bran ch es from th e an terior ch oroidal ar ter y h ave a
Th e an ter ior p er forated su bst an ce is a rh om boid -sh ap ed area posterior, superior, and m edial course or a direct posterosuperior
located deep in th e sylvian fissure. Its lim its are th e m edial an d cou rse tow ard th e an terior p erforated su bst an ce. Th ey u su ally
lateral olfactor y st riae (an terior border), th e lim en in su la (lateral pen et rate th e p osterior an d m edial zon es of th e an terior p erfo-
border), th e opt ic t ract an d tem poral lobe (posterior border), an d rated substan ce, near the optic tract, overlapping extensively w ith
th e opt ic ch iasm /in terh em isp h eric fissu re (m ed ial border). th e bran ch es from th e ICA.

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3 Cranial Vascular Anatomy of the Anterior Circulation 47

Anterior Perforating Branches from the m ediolateral aspect of th e an terior perforated substan ce. How -
Middle Cerebral Artery ever, based on t h e an terop oster ior organ izat ion of t h e an terior
p erforated su bst an ce, m ost of t h e p erforat in g bran ch es from t h e
The perforating branches from the MCA to the anterior perforated recu r ren t ar ter y of Heu bn er pen et rate t h e an ter ior zon e of th e
su bst an ce are called len t icu lost r iate ar ter ies. Th ese bran ch es an terior perforated su bst an ce.
arise from th e M1 an d M2 segm en t s an d are com posed of th ree
to 21 perforat ing vessels per h em isph ere (average, 10.4).12 Most
of th ese bran ch es are derived from th e prebifu rcat ion segm en t Areas of Irrigation of the Anterior
of M1 (80% of th e bran ch es). On ly 17% an d 3%, respect ively, are
Perforating Arteries
sen t by t h e p ost bifu rcat ion segm en t of M1 an d t h e p roxim al
p or t ion of M2. W h en an early bifurcat ion is presen t , th e n um ber Th e an terior p erforat ing ar teries pass th rough par t s of th e cau -
of perforat ing bran ch es origin at ing from th e postbifu rcat ion seg- date n u cleu s, pu t am en , an d in tern al capsu le directly above th e
m en t s is u su ally larger. an terior perforated substan ce an d spread posteriorly to supply
As n oted du ring discu ssion of th e p erforat ing bran ch es of th e larger p or t ion s of th ese st r u ct u res an d adjacen t areas of th e glo-
MCA, th e len t icu lost riate ar teries are divided in to m edial, in ter- bu s p allidu s an d th alam us.
m ediate, an d lateral grou ps. Each group h as un ique ch aracteris- Th e su p raclin oidal ICA bran ch es irrigate th e gen u of th e in ter-
t ics regarding th eir com p osit ion , dist ribu t ion , an d m orph ology. n al capsu le an d th e adjacen t par t of th e globu s pallidus, poste-
rior lim b of th e in tern al capsu le, an d th alam us.
Th e bran ch es from th e an terior ch oroidal ar ter y su p ply th e
Anterior Perforating Branches from the m ed ial segm en t s of t h e globu s p allid u m , t h e p oster ior lim b of
Anterior Cerebral Artery t h e in ter n al cap su le, an d t h e an ter ior an d ven t rolateral n u clei
of th e th alam us.12,13
Th e p erforat ing bran ch es from th e ACA arise from A1 an d th e
Th e m edial len t icu lost riate ar teries irrigate th e lateral p or t ion
recu rren t arter y of Heu bn er (w h ich u su ally origin ates from th e
of th e globus pallidus, th e an terior lim b of th e in tern al capsule,
A2 segm en t). A1 gives rise to on e to 11 perforat ing bran ch es th at
an d th e an terosuperior por t ion of th e h ead of th e caudate n u-
term in ate in th e an terior perforated substan ce (average, 6.4).
cleus. Th e in term ediate an d lateral len t icu lost riate ar teries su p -
Th ose bran ch es divide to yield fou r to 49 vessels as th ey p en e-
ply th e u p per por t ion of th e in tern al cap su le an d th e body an d
t rate th e an terior p erforated su bstan ce.4,12 Most of th e perforat-
h ead of th e cau date n u cleus.2
ing bran ch es derive from th e su p erior or p osterior w all of th e A1
Th e A1 bran ch es su p p ly th e area arou n d th e opt ic ch iasm , an -
segm en t in its lateral por t ion an d ru n p osterosu p eriorly tow ard
terior com m issure, an terior hypoth alam us, gen u of th e in tern al
th e an terior perforated su bst an ce. Most of th ese bran ch es pen e-
capsu le, an d an terior p or t ion of t h e globu s pallidu s. Less com -
t rate m edial, m iddle, an d p osterior zon es of th e an terior p erfo-
m on ly, th ese bran ch es exten d to th e con t iguous por t ion of th e
rated su bst an ce, posterior to th e bran ch es from th e recu rren t
posterior lim b of th e in tern al cap su le an d to th e an terior p or t ion
ar ter y an d an terom edial to th e bran ch es from th e ICA.
of th e th alam us.9
Th e p erforat ing bran ch es from th e recu rren t ar ter y of Heu b -
Perforating Branches from the Recurrent Artery n er con t ribute to th e irrigat ion of th e h ead of th e caudate n u-
of Heubner cleus, pu tam en , an d an terior lim b of th e in tern al capsu le.

Th e recu rren t bran ch of th e ACA is th e largest an d longest of th e


bran ch es directed to th e an terior perforated substan ce. As n oted
earlier, th is ar ter y u sually origin ates n ear th e jun ct ion of th e A1
an d A2 segm en ts an d doubles back on th e ACA in its course to-
■ Conclusion
w ard th e an terior perforated su bst an ce.9 On e to fou r recurren t A detailed un derst an ding of th e an atom y of th e cerebral vessels,
ar teries m ay be presen t per h em isph ere. If t w o recu rren t ar ter- th eir variat ion s, bran ch ing p at tern s, an d an astom oses is crit ical
ies are p resen t , on e or bot h ar ise at t h e ju n ct ion of t h e A1 an d to th e su ccessfu l execut ion of vascu lar surger y. It beh ooves n eu -
A2 segm en t s. A single recurren t bran ch m ay give rise to on e to rosurgeon s to becom e fam iliar w ith th e an atom y out lin ed in th is
28 p erforat ing bran ch es to t h e an terior p erforated su bst an ce an d oth er ch apters on th e vascular an atom y of th e posterior cir-
(average, 9.6 bran ch es).9 Th ose bran ch es diffusely pen et rate th e culat ion an d cerebral vein s.

References
1. Yaşargil MG. Micron eu rosurger y. New York: Th iem e; 1984 5. Wen HT, Rh oton AL Jr, de Oliveira E, Cast ro LH, Figueiredo EG, Teixeira MJ.
2. Gibo H, Car ver CC, Rh oton AL Jr, Len key C, Mitch ell RJ. Microsurgical an at- Microsurgical anatom y of the tem poral lobe: part 2—sylvian fissure region
om y of th e m iddle cerebral ar ter y. J Neurosurg 1981;54:151–169 an d it s clin ical app licat ion . Neu rosurger y 2009;65(6, Suppl):1–35, dis-
3. Kalan i MY, Zabram ski JM, Hu YC, Spet zler RF. Ext racran ial-in t racran ial cu ssion 36
byp ass an d vessel occlu sion for t h e t reat m en t of u n clip p able gian t m id- 6. Lazor t h es G, Gou aze A, Salam on G. Vascu lar isat ion et Circu lat ion de
dle cerebral arter y an eur ysm s. Neurosurger y 2013;72:428–435, discu s- l’En ceph ale. Anatom ie Descript ive et Fon ct ion n elle. Paris: Elsevier: Mas-
sion 435–436 son ; 1976
4. Rhoton AL Jr. Th e supratentorial arteries. Neurosurgery 2002;51(4, Suppl): 7. Tan riover N, Kaw ash im a M, Rh oton AL Jr, Ulm AJ, Mericle RA. Microsu rgi-
S53–S120 cal an atom y of th e early branch es of th e m iddle cerebral arter y: m orph o-

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48 I Developm ent, Anatomy, and Physiology of the Central Nervous System

m et ric an alysis an d classificat ion w ith angiograph ic correlat ion . J Neu ro- 10. Steh ben s W E. An eur ysm s an d an atom ical variat ion of cerebral ar teries.
surg 2003;98:1277–1290 Arch Path ol 1963;75:45–64
8. Mich otey P, Moscow N, Man elfe CL, et al. Th e territor y of th e cor t ical 11. Perlm ut ter D, Rh oton AL Jr. Microsu rgical anatom y of the dist al an terior
bran ch es of th e m iddle cerebral ar ter y. In : Meyer JS, Lechn er H, Reivich M, cerebral ar ter y. J Neu rosu rg 1978;49:204–228
et al. Cerebral Vascular Disease. Berlin : Georg Th iem e Verlag; 1974 12. Rosn er SS, Rh oton AL Jr, On o M, Barr y M. Microsurgical an atom y of th e
9. Perlm u t ter D, Rh oton AL Jr. Microsu rgical an atom y of t h e an ter ior an terior perforat ing ar teries. J Neu rosu rg 1984;61:468–485
cerebral- an terior com m un icat ing-recurren t ar ter y com plex. J Neu rosu rg 13. Rh oton AL Jr, Fujii K, Fradd B. Microsurgical an atom y of th e an terior ch o-
1976;45:259–272 roidal ar ter y. Su rg Neurol 1979;12:171–187

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4 Cranial Vascular Anatomy of the
Posterior Circulation
Michaël Bruneau and Henri-Benjam in Pouleau

Th e cran ial vascu lar an atom y of th e posterior circu lat ion en com - u llar y segm en t exten ds from th e preolivar y sulcu s to in fron t of
passes both ver tebral ar teries (VAs), w h ich fu se togeth er to form (or bet w een ) th e hypoglossal n er ve rootlets an d crosses th e pyr-
th e basilar ar ter y (BA) (Figs. 4.1a an d 4.2). Th e BA th en term i- am id to form th e BA by join ing th e con t ralateral ar ter y.2,4,6 Th e
n ates in to th e posterior cerebral ar teries (PCAs) (Fig. 4.3). Th is an terior m edu llar y segm en t rest s on th e clivu s.2
ch apter det ails th e bran ch es an d an atom ic var iat ion s of th ese
ar teries.
Variations
Defin ing VA dom in an ce as m ore th an a 1-m m differen ce in w idth
bet w een th e VAs, a large st udy foun d th at both VAs w ere equally
■ Vertebral Artery sized in 61.5%, th e left VA w as dom in an t in 21.2%, an d th e righ t
VA w as dom in an t in 17.3%of cadavers.3 VA hypoplasia is defin ed
Th e in t racran ial VA (Fig. 4.1) (diam eter 2.8 to 3 m m , also called
by a relat ively sm all VA diam eter.1 Un equ al VA diam eter an d flow
th e in t radu ral or V4 segm en t) st ar t s at th e du ra m ater at th e
con t ribu te to cu r vat u re of th e BA an d to th e d evelop m en t of p eri-
level of th e foram en m agn u m , ju st in ferior to its lateral edge. At
VBJ in farct s.7 Th e in cid en ce of VA hyp op lasia is h igh ly var iable
its origin , V4 is fixed at th e distal du ral ring; at it s en d, it fu ses
an d depen ds on th e size cutoff an d m eth od of m easurem en t .8
w ith its con t ralateral coun terpar t to form th e BA.1–3 Th e perios-
W h en d efin ed by a VA d iam eter ≤ 2 m m , t h e rates of VA hyp o -
teal sh eath surroun ding th e suboccipital V3 segm ent (an exten -
p lasia on th e left side, righ t side, an d bilaterally are 14.4%, 20.2%,
sion of th e t ran sverse p rocess periosteu m ) join s t igh tly w ith th e
an d 4.8%, respect ively.3
du ra m ater to form a dou ble fu rrow from 1 to 2 m m to 4 to 6 m m
long, located 10 m m from m idlin e.4 Th e venous plexus surround-
ing V3 inside the periosteal sheath is discontinuous, and collage- Branches
n ous fibers of th e du ra act as cram p, pen et rat ing th e adven t it ia
to reach th e m edia an d an ch or in to th e ar terial w all.4 Th e bin d- Th e p oster ior sp in al ar ter y, p oster ior in fer ior cerebellar ar ter y
ing of t h e VA, of th e p osterior sp in al arter y en tering th e du ra, (PICA), an ter ior sp in al ar ter y, an d an ter ior an d p oster ior m en -
an d of th e first cer vical n er ve exit ing th e dura by fibrou s ban ds in geal ar teries bran ch from th e VAs in th e region of th e foram en
th rough t h e fu n n el-sh ap ed foram en 2 p reven t s th e VA from being m agn um .6
separated from th e du ra at th e level of th e dist al ring.5
Paired in t radural VAs ascen d th rough th e foram en m agn u m
Posterior Spinal Artery
in fron t of th e m edu lla, w h ere both arteries fu se to form th e BA
at th e level of th e pon tom edu llar y ju n ct ion (Figs. 4.1 an d 4.2). In Th e p osterior sp in al ar ter y u su ally arises from th e posterom e-
t w o-th irds of cases, th e vertebrobasilar jun ct ion (VBJ) is located dial su rface of th e V3 segm en t ju st ou t side th e du ra. Th e ar ter y
below (m ean 4.34 ± 1.85 m m ) th e bulbopon t in e sulcus; in 20%, passes th rough th e du ra in to th e sam e fibrou s t u n n el as th e VA
the VBJ is located at this level; an d in 12%, the VBJ is located above an d th e first cer vical n er ve root . Surgeries th at open th e dural
th is level (m ean 4.42 ± 2.05 m m ).3 Th e VBJ angle is repor ted to be cuff arou n d th e VA m u st be perform ed cau t iou sly to avoid injur-
52.2 ± 18.2 degrees.3 ing th e posterior sp in al arter y.2,9 Th e p osterior sp in al ar ter y also
Th e V4 segm en t cou rses ju st su perior to th e dorsal an d ven - m ay arise from th e PICA or from th e in it ial port ion of th e in t ra-
t ral roots of th e first cer vical n er ve an d ju st an terior to th e p os- du ral VA. In th e su barach n oid space, th e posterior spin al ar ter y
terior sp in al ar ter y, d en t ate ligam en t , an d sp in al p or t ion of th e run s m edially beh in d th e rost ralm ost at tach m en ts of th e den tate
accessor y n er ve.2 Th e ar ter y ascen d s from t h e low er lateral to ligam en t, dividing in to ascen ding an d descen ding bran ch es w h en
th e up p er an terior su rface of th e m edu lla an d is su bdivided in to it reach es th e low er m edu lla. The first bran ch ascen ds th rough
th e lateral an d an terior m edu llar y segm en t s.2 Th e lateral m edu l- the foram en m agnum and supplies th e rest iform body, gracile and
lar y segm en t st ar ts at th e level of th e du ral foram en an d cou rses cun eate t ubercles, accessor y n erve rootlet s, an d ch oroid plexus.
an terior an d superior along th e lateral m edullar y surface to ter- Th e lat ter bran ch descen ds bet w een th e d orsal rootlet s an d th e
m in ate at th e preolivar y sulcu s.2 It s an terior an d lateral su rfaces den tate ligam en t on th e p osterolateral su rface of th e sp in al cord,
face th e occip it al con dyles, hyp oglossal can als, an d jugu lar t u - su p plying th e su p erficial part of th e dorsal h alf of th e cer vical
bercles.2 Th e V4 segm en t p asses u n der th e arch form ed by th e spin al cord. Th is bran ch an astom oses w ith posterior bran ch es of
first an d secon d den tate ligam en t t ips.4 It crosses th e posterior th e radicu lar arteries en tering th e ver tebral foram en at th e low er
face of th e an terior m edullar y root of th e accessor y n er ve an d levels.2,9 Paired posterior spinal arteries supply th e posterior third
th e sp in al ganglion of th e first cer vical ner ve. Th e an terior m ed- of th e spin al cord. Direct pen et rat ing vessels an d a plexu s of pial

49

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50 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 4.1a–c Anatomic view of the arteries of the posterior circulation. (a) An-
terior view of the vertebral arteries, basilar artery, and branches. 1, vertebral
artery; 2, anterior spinal artery; 3, basilar artery; 4, anterior inferior cerebellar
artery; 5, lateral pontine artery; 6, anterolateral pontine artery; 8, P1 segm ent
of the posterior cerebral artery; 9, posterior com m unicating artery; 10, P2A
segm ent of the posterior cerebral artery; 11, internal carotid artery; 12, optic
nerve; 14, trochlear nerve; 15, trigem inal nerve; 16, abducens nerve; 17, facial
and vestibulocochlear nerves; 18, lower cranial nerves; 19, dist al dural ring.
(b) Lateral view of the upper brainstem and inferior view of the temporal and
occipit al lobes. 1, basilar artery; 2, superior cerebellar artery; 3, long circum -
flex artery; 4, trochlear nerve; 5, P1 segm ent of the posterior cerebral artery;
6, posterior com m unicating artery; 7, P2A segm ent of the posterior cerebral
artery; 8, hippocampal artery; 9, anterior temporal artery; 10, m iddle temporal
artery; 11, posterior temporal artery. (c) Medial view of parieto-occipital lobes.
1, P3 segm ent of the posterior cerebral artery; 2, calcarine artery; 3, location of
the parieto-occipital artery inside the parieto-occipital sulcus.

a c

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4 Cranial Vascular Anatomy of the Posterior Circulation 51

Fig. 4.2 Anterior view illustrating the arterial branches to the brainstem peduncular fossa. penetrating the foram en cecum (14**); 15, anterolateral
and cerebellar arteries. (A) Medulla. (B) Pons. (C) Midbrain. (D) Cerebel- group of pontine arteries; 16, lateral group of pontine arteries originating
lum . Main arterial trunks: 1, vertebral artery; 2, anterior spinal artery; from the superior lateral pontine (16*) and the inferior lateral pontine
3, posterior inferior cerebellar artery; 4, basilar artery; 5, anterior inferior (16**) arteries and from the anterior inferior cerebellar artery; 17, antero-
cerebellar artery; 6, superior cerebellar artery; 7, posterior cerebral artery; medial group of mesencephalic arteries (middle rami of the interpeduncular
8, collicular artery; 9, posterom edial choroidal artery; 10, anterior choroi- fossa); 18, thalam operforating arteries (superior ram i of the interpedun-
dal artery. Arteries of the anterior and lateral aspects of the brainstem : cular fossa); 19, anterolateral group of m idbrain arteries. Arteries of the
11, anterom edial group of m edullary arteries; 12, anterolateral group of anterior aspect of the cerebellum : 20, branches of the superior cerebellar
m edullary arteries; 13, lateral group of m edullar arteries (arteries of the artery; 21, branches of the anterior inferior cerebellar artery; 22, branches
lateral medullary fossa), a, inferior ram i, b, middle ram i, c, superior ram i; of the posterior inferior cerebellar artery. (Redrawn from Tatu et al,34 m odi-
14, anterom edial group of pontine arteries, penetrating the basilar sulcus fied from Duvernoy.38 )
(14), penetrating the interpeduncular fossa (14*) (inferior ram i of the inter-

vessels fed by both posterior spin al ar teries form a rich an asto- w ith su rroun ding st ruct ures (n am ely, th e brain stem , cerebellar
m otic net w ork that explain s the low incidence of posterior spinal p ed u n cles, fissu re bet w een t h e brain stem an d cerebellu m , an d
ar ter y syn drom e.10 cerebellar su r faces). Th ese ar ter ies are also associated w it h a
grou p of cran ial n er ves (CNs III–V, VI–VIII, an d IX–XII). Th e PICA
belongs to th e low er n eurovascular com plex con t ain ing th e m e-
Posterior Inferior Cerebellar Artery
du lla; in ferior cerebellar p edu n cle; cerebellom edu llar y fissu re;
As th e largest bran ch of th e VA, th e PICA h as a com plex cou rse su boccipit al cerebellar su rface; an d th e glossop h ar yngeal, vagu s,
w ith a tor t uous an d variable ch aracter (Fig. 4.4).11 It com m on ly spin al accessor y, an d hypoglossal n er ves.
origin ates 16 or 17 m m proxim al to th e VBJ, w ith m any varia- Th e PICA ar ises from t h e VA close to t h e in fer ior olive an d
t ion s.9 It s ou ter diam eter is 1.7 to 1.8 m m du ring it s cou rse p asses p oster iorly arou n d t h e m ed u lla.11 At th e an terolateral
th rough th e p erim edu llar y cistern an d 1.3 to 1.4 m m just before m edulla m argin , it passes rost ral or caudal to or bet w een th e hy-
it term in ates as a cerebellar h em isp h eric bran ch .12 Th e PICA is poglossal n er ve rootlets. At th e p osterolateral m edu lla m argin ,
present as a single (84%) or double trunk (2.4%), and it arises above it cou rses rost ral to or bet w een th e fila of th e glossoph ar yngeal,
(83.3%) or below (16.7%) th e level of th e foram en m agn u m .13 vagu s, an d accessor y n er ves. It t h en loop s arou n d t h e cerebel-
As elu cidated by Rodrígu ez-Hern án dez et al,11 th e th ree cere- lar ton sil, pen et rates th e cerebellom edullar y fissu re, an d passes
bellar ar teries (su p erior cerebellar ar ter y, an terior in ferior cere- posterior to th e low er h alf of th e roof of th e fou r th ven t ricle. On
bellar ar ter y [AICA], an d PICA) h ave a con sisten t relat ion sh ip exit ing th e cerebellom edu llar y fissu re, m ost PICAs bifu rcate in to

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52 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 4.3 Branches of the posterior cerebral artery. 1, in-


ternal carotid artery; 2, posterior com m unicating artery;
3, basilar artery; 4, superior cerebellar artery; 5, P1 seg-
m ent; 6, P2A segm ent; 7, anterior temporal artery; 8, P2P
segm ent; 9, com m on temporal artery; 10, P3 segm ent;
11, calcarine artery; 12, parieto-occipital artery; 13, long
circum flex artery; 14, hippocampal artery; 15, anterior
choroidal artery; 16, m iddle temporal artery; 17, lateral
posterior choroidal artery; 18, posterior temporal artery.

t w o t run ks th at dist ribu te to th e verm is an d h em isph ere of th e hypoglossal rootlets. How ever, it m ay loop upw ard, dow nw ard,
su boccip ital su rface. Th e m edial t ru n k feeds th e verm is an d th e laterally, or m ed ially before p assin g p oster iorly arou n d or be-
adjacent par t of th e h em isph ere, w h ereas th e lateral t run k vas- t w een th e hypoglossal rootlet s. Th e an terior m edullar y segm en t
cularizes th e cor t ical ton sil su rface an d h em isph ere. cou rses to t h e level of a rost rocau dal lin e t h rough t h e m ost
prom in en t par t of th e in ferior olive, rep resen t ing th e bou n dar y
bet w een th e an terior an d lateral surfaces of th e m edulla.11
Segments
Th e PICA bran ch es in to t h e p er forat in g, ch oroid al, an d cor t ical Lateral Medullary Segment
ar ter ies, w h ich in t u r n are d ivided in to ver m ian , ton sillar, an d Th is segm en t exten ds bet w een th e m ost p rom in en t poin t of th e
h em isph eric grou ps. Th e PICA is divided in to an terior m edullar y, olive an d th e or igin of t h e glossop h ar yngeal, vagu s, an d acces-
lateral m edu llar y, ton sillom edu llar y, teloveloton sillar, an d cor t i- sor y n er ve root let s. It s cou rse m ay var y great ly, w it h several
cal segm en t s (Fig. 4.4), w h ich m ay in clu de m u lt iple t ru n ks, d e- com plex loop s.11
pen ding on th e level of ar terial bifu rcat ion .11 Segm en tal an atom y
of the infratentorial cerebellar arteries has been described through Tonsillomedullary Segment
cadaver ic d issect ion .13 For ed u cat ion al an d p ract ical p u r p oses, Th e ton sillom edu llar y segm en t begin s w h ere th e PICA passes
a n um erical n om en clat ure an alogou s to th e n u m bering system posterior to th e glossop h ar yngeal, vagu s, an d accessor y n er ves.
used for th e cerebral arteries w as est ablish ed for th e cerebellar Th e p roxim al PICA u su ally cou rses n ear t h e lateral recess. It
ar teries.11 t ravels posteriorly to th e in ferior pole of th e ton sil, w h ere it
com m on ly passes m edially to th e m edulla, form ing a cau dal or
Anterior Medullary Segment in fraton sillar loop , before t urn ing rost rally along th e m edial sur-
Th is segm en t is p resen t w h en th e PICA origin ates an terior to th e face of th e ton sil.11 Th e low er en d of th e caudal loop is above,
m edulla but is absen t w h en th e origin is lateral to th e m edulla. below, or at th e level of th e edge of th e foram en m agn um in 88%,
Th is segm en t is m ore likely to be presen t if th e PICA arises from 9.5%, an d 2.5% of cases, resp ect ively.9 If th e PICA ascen ds along
the superior VA because the VA courses from the lateral side of the th e su rface of th e ton sil to reach th e h em isph eric su rface or if t h e
m edulla below th e an terior su rface of th e m edu lla. From it s ori- PICA h as a low origin from th e VA an d ascen ds p osteriorly to th e
gin , th e PICA usu ally exten ds backw ard aroun d or bet w een th e m edu lla to reach th e ton sil, t h en th e cau dal loop m ay be absen t

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4 Cranial Vascular Anatomy of the Posterior Circulation 53

a b

d
c

Fig. 4.4a–d Overview of the segm ental anatomy of infratentorial arteries, as seen in lateral (a), anterior (b), superior (c), and inferior (d) views. AICA,
anterior inferior cerebellar artery; PICA, posterior inferior cerebellar artery; SCA, superior cerebellar artery. (Courtesy of Albert L. Rhoton, Jr.)

w h en th e ar ter y cou rses su p er iorly or in fer iorly to th e cau dal bran ch es th at radiate out w ard from th e superior an d lateral ton -
pole of th e ton sil, passing directly m edial bet w een th e ton sil an d sil borders to th e rest of th e verm is an d h em isph ere.11
m edulla. Th e ton sillom edullar y segm en t en ds w h ere th e arter y
ascen ds to th e m idlevel of th e m edial su rface of th e ton sil.11
Variations
Telovelotonsillar Segment Som e variat ion s of th e PICA in clu de an ext radu ral origin , agen e-
Th e h igh ly com plex teloveloton sillar segm en t begin s at th e m id- sis, dup licate vessels, an d an om alou s origin .
por t ion of th e PICA, w h ich ascen ds along th e m edial su rface of
th e ton sil tow ard th e roof of th e fou rt h ven t ricle. It exit s th e fis- Extradural Posterior Inferior Cerebellar Artery
su res bet w een th e verm is, ton sil, an d h em isp h ere to reach th e Alt h ough an ext rad u ral PICA is com m on (5 to 20% in cid en ce),
su boccip it al su rface.11 In m ost h em isp h eres, th is segm en t form s bilateral ext rad u ral PICAs are rare.14 An ext radu ral PICA m ay
th e cran ial loop , w h ich is a convex rost ral cu r ve located cau dal to st ar t from th e h orizon t al V3 segm en t , ju st ou t side th e du ra or
th e fast igiu m bet w een th e cerebellar ton sil below an d th e low er fu r th er laterally above th e t ran sverse foram en of th e atlas. Th e
h alf of th e four th ven tricular roof form ed by th e tela ch oroidea PICA cou rses ext rad u rally, p arallel to t h e VA an d th e C1 n er ve,
an d th e posterior m edullar y velum above. Bran ch es arising from all th ree of w h ich p en et rate th e du ra togeth er. In t radurally, th e
th is segm en t su p p ly th e tela ch oroidea an d ch oroid p lexu s of th e PICA rem ain s p osterolateral to th e brain stem , su p plying th e pos-
fou r th ven t ricle. terolateral m edulla. W h en an ext radu ral PICA arises in t radurally,
th e first segm en t of th e PICA cou rses an terior to th e m ed u lla an d
Cortical Segment su p plies th e an terior brain stem . An ext radu ral PICA also m ay
Th e PICA often bifu rcates n ear th e origin of th e cor t ical segm en t , arise from th e ver t ical V3 segm en t and pen et rate th e dura be-
w h ich begin s w h ere th e t r un ks an d bran ch es leave th e groove t w een C2 an d C1. With th is un u su al anatom y, th e PICA is at risk
su r rou n d ed by t h e ver m is m ed ially an d t h e ton sil an d h em i- of isch em ia in th e case of V3 dissect ion. If m ist aken for th e m us-
sph ere laterally. Th is segm en t en com passes th e term in al cor t ical cu lar, posterior m en ingeal, or posterior spin al bran ch es du ring a

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54 I Developm ent, Anatomy, and Physiology of the Central Nervous System

posterior app roach to th e cran iover tebral ju n ct ion , th e PICA also Th e “textbook” p at tern of t w o descen ding sym m et ric an terior
m ay be at risk of inju r y. vent ral spin al ar teries join ing to form th e m ain an terior spin al
ar ter y t r un k is en coun tered in on ly 18% of cases. Great variabil-
Posterior Inferior Cerebellar Artery Agenesis it y exists, part icu larly in t h e size an d con t ribu t ion of t h e t w o
A cerebellar ar ter y arising from th e VA m ay be absen t in as m any (t ypically asym m et ric) ram i from th e VA.22,24 Th e an terior ven -
as 16% of cases.13 In th is sit uat ion , th e ipsilateral AICA or th e su- t ral sp in al ar ter y or an terior sp in al ar ter y arises m ain ly from th e
perior cerebellar ar ter y u su ally perfu ses th e low er cerebellu m .15 m edial w all of V4 (43.8% in ciden ce) bu t m ay arise from th e pos-
terom edial (23.8%) or posterior (18.5%) w all, dist al to th e PICA
Anomaly of Origin origin at a m ean distan ce of 6.86 m m (2.86 to 12.38 m m ) from
In t h e case of an an om alou s or igin of t h e PICA, th e vessel t h e VBJ.22,24 Kaw ash im a et al 25 fou n d t h at t h e ju n ct ion of t h e
ar ises from t h e hyp oglossal, p roatlan t al, or p oster ior m en in geal an terior ven t ral spin al ar teries w as above th e foram en m agn um
ar ter y.16–18 n ear th e low er en d of th e olives in 84% of specim en s.
According to Er et al,23 th e origin of th e an terior spin al ar ter y
Bihemispheric Posterior Inferior Cerebellar Artery m ay be categorized in to th ree m ain t yp es an d several su bt yp es.
In th e case of bih em isph eric PICAs (< 0.1% in ciden ce),15 both Type I is ch aracterized by th e presen ce of t w o ram i th at fuse to
PICAs origin ate from a com m on t ru n k of a dom in an t VA. A t ru e form th e an terior spin al ar ter y, t ype II by on e ram us th at con t in -
bih em isph eric PICA supplies both cerebellar h em isph eres from a u es as th e m ain an terior spin al ar ter y, an d t ype III by t w o in de-
single t ru n k. In th e verm ian varian t , a single PICA provid es on ly pen den t t r u n ks th at cou rse dow nw ard sep arately 22,23 an d m ay
bilateral verm ian su pp ly, w ith th e su p erior cerebellar ar ter y or be lin ked by th e an terior spin al com m un icat ing arter y.26 In t yp e
AICA su pp lying th e rest of th e con t ralateral cerebellar su pply. Ia, th e an terior sp in al ar ter y cou rses dow nw ard, w h ereas in t ype
Ib, th e an terior sp in al ar ter y su bdivides in to t w o sep arate an te-
Duplicate Posterior Inferior Cerebellar Artery rior sp in al ar ter y t r u n ks, w h ich m ay arise from a vascu lar arcade
A double origin of the PICA (1.45–2%in cidence) m ay be associated lin king th e t w o VAs (t ype Ic). In t ype IIa, a single an terior spin al
w ith an ext racran ial PICA origin an d th e risk of an in t racran ial ar ter y em erges from th e left or righ t VA. In t ype IIb, there are
an eur ysm .19,20 A dist al PICA resu lts from th e fusion of t w o ch an - t w o ram i: on e w ith a ver y sh or t course an d on e th at su pplies th e
n els. Th e cran ial ch an n el bran ch es from V4. Th e caudal ch an n el spin al cord. In t ype IIc, a dom in an t ram u s cou rses dow nw ard as
t ypically branches from the VA interatlanto-occipital segm ent or, th e m ain an terior spin al ar ter y t r u n k, an d a sm aller ram us join s
less frequen tly, from th e C1–C2 segm en t .21 th e m ain t run k in an en d-to-side fash ion .22,23
Term in al bran ch es t h at arise from t h e an ter ior sp in al ar ter y
in clu de th e p aram edian bran ch es (100% in ciden ce, m ean 14.7
Anterior Spinal Artery
p er brain stem ), sh ort circu m feren t ial bran ch es (100%in ciden ce,
Con t rast -en h an ced , h igh sp at ial resolu t ion , t h ree-d im en sion al m ean 9.4 per brain stem ), an d long circu m feren t ial bran ch es
m agn et ic reson an ce (MR) an giograp hy is t h e m ost sen sit ive (84% in cid en ce, m ean 3.5 p er brain stem ).24 Th e st raigh t p ara-
m et h od for visualizing th e an terior sp in al ar ter y. Its detect ion m edian bran ch es en ter th rough th e ven t ral m edu lla to su pp ly
rate is as h igh as 96%. Mu lt idetector com p u ted tom ograp hy (CT) th e m edial pyram ids. Sh or t circu m feren t ial bran ch es su pp ly th e
angiography visualizes th e an terior spin al ar ter y in on ly h alf of rost ral pyram ids an d olive w ith ou t passing beyon d th e an tero-
th e cases. Conven t ion al angiograp hy is less u sefu l an d m ay n ot lateral (p reolivar y) su lcu s. Long circu m feren t ial bran ch es r u n
visu alize t h e origin of th e an terior sp in al arter y even after selec- beyon d t h e an terolateral su lcu s an d su p p ly t h e olive in 84% of
t ive VA inject ion s.22,23 brain stem s.24
An terior m edullar y segm en t s of th e VAs n ear th e VBJ are at Marin ković et al27 n oted th at perforat ing arteries origin ate
th e origin of p aired an terior ven t ral sp in al ar teries w h ose u n ion from th e VA (54.54% in cid en ce), an terior spin al ar ter y (100% in -
form s th e an terior spin al ar ter y.2 Th e an terior sp in al ar ter y cre- ciden ce), an terior vent ral spin al ar teries (95.45% in ciden ce), or
ates a con t in u ou s ch an n el th at r u n s along th e en t ire length of th e th e an terolateral or lateral m ed u llar y ar teries (circu m flex ar ter-
spin al cord an d is con st it u ted by th e coalescen ce of ascen ding ies, 50%). Perforat ing ar teries of th e VA en ter th e foram en cecum
and descending branches em anating from the radicular arteries.22 an d su perior par t of th e an terior par t of th e m edian m edullar y
Th e an terior spin al ar ter y descen ds th rough t h e foram en m ag- su lcu s to su p p ly th e param edian region of th e u p p er m edu lla,
n um on th e an terior m edu lla an d th e spin al cord in or n ear th e in cluding th e pyram idal bu n dles, m edial lem n iscu s, m edial lon -
an terom edian fissure.2,9 On th e m edulla, th e an terior spin al ar- git udin al fasciculus, cran ial part of th e hypoglossal n ucleus, an d
ter y feeds th e pyram ids an d th eir decussat ion , th e m edial lem - param edian ret icular form at ion .6
n iscus, in terolivar y bu n dles, hypoglossal n uclei an d n er ves, an d Th e an terior sp in al ar ter y su p plies th e an terior t w o-th irds of
p oster ior longit u d in al fascicu lu s.9 Th e size of t h e an astom osis th e spin al cord, an d 75% of th e blood sup ply of th e spin al cord is
w it h t h e an ter ior bran ch es of t h e rad icu lar ar ter ies is inversely from th e an terior spin al ar ter y.22 Before any su rgical an d en do-
related to th e size of th e descen ding ch an n el.9 Th e m ean dist an ce vascu lar procedu re is un der taken, th e su rgeon m ust un derst an d
bet w een th e VBJ an d t h e or igin of th e an terior ven t ral sp in al th e n u m erou s an atom ic variat ion s of th e an terior sp in al ar ter y
ar ter ies or an ter ior sp in al ar ter y is 6.8 to 7.5 m m (range, 0.2 to to m in im ize disast rous isch em ic com plicat ion s. Such kn ow ledge
15 m m ). Mean ar terial size is 0.6 to 0.9 m m .22,24 m ay be h elpful in predict ing toleran ce to occlusion of on e an te-
Th e an ter ior sp in al ar ter y is t yp ically for m ed by on e an te- r ior sp in al ar ter y ram u s. Occlu sion of t h e an ter ior sp in al ar ter y
r ior ven t ral spin al ar ter y from each side (60% of cases). Less fre- at or n ear it s or igin m ay cau se m ed ial m ed u llar y in farct ion .22
qu en tly, th e an terior spin al ar ter y is form ed as a d irect bran ch Sp in al occlu sion of th e an terior spin al ar ter y is associated w ith
from th e left VA (30% of cases), righ t VA (8%), or BA (2%).24 an terior spin al ar ter y syn drom e w ith or w ith out breath ing dis-

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4 Cranial Vascular Anatomy of the Posterior Circulation 55

orders, depen ding on th e involvem en t of th e cer vical m edulla.22 in 70% of cases, at it s level in 20%, an d below th e biclin oid lin e
Th e an terior m edu lla oblongat a an d olive are u su ally ch aracter- (u p to 4.2 m m ) in 10%.32
ized by a rich an astom ot ic n et w ork, w h ich m ay accou n t for th e Th e level of th e basilar bifu rcat ion in flu en ces th e origin an d
rarit y of m edu llar y in farct ion in th e olive region .26 th e locat ion of th e proxim al sup erior cerebellar ar ter y. In th e
presen ce of n orm al-lying BA bifu rcat ion s, th e su perior cerebellar
ar ter y ar ises from t h e BA bifu rcat ion in to th e PCA (h alf of t h e
Meningeal Arteries
cases). In th e p resen ce of h igh BA bifu rcat ion s, th e su p erior cer-
In frequ en tly, th e PICA, p osterior sp in al arter y, an d in t radural ebellar arter y arises as a single vessel from th e BA t r un k, clearly
part of th e VA give rise to m en ingeal bran ch es.9 Usu ally, th e du ra separated from th e PCA (t w o-th irds of cases). W h en th e BA bi-
aroun d th e posterior cran ial fossa an d foram en m agn um is sup - fu rcat ion is located cran ial or cau dal to th e p on tom esen cep h alic
plied by the anterior an d posterior m eningeal branches of the VA, junct ion , th e proxim al superior cerebellar ar ter y is located in th e
m en in geal bran ch es of t h e ascen d in g p h ar yn geal an d occip it al in terpedu n cu lar or prep on t in e cistern , respect ively.33
ar ter ies, an d t h e d orsal m en ingeal bran ch of t h e m en ingohy- The m ean basilar bifurcation angle bet w een the origins of both
pop hyseal t r u n k th at arises from th e in t racavern ou s segm en t of P1 segm en t s is 109 degrees. Th is angle m ay range bet w een 30
th e in tern al carot id ar ter y (ICA).2 and 180 degrees, w ith a subsequently low apex and vertical course
of both P1 segm en t s an d a h igh apex close to th e dien ceph alon
an d h orizon t al cou rse of both P1 segm en ts, respect ively.32 Th e
Perforating Arteries Around the m ean dist an ce bet w een th e basilar apex an d cerebral pedun cles
Vertebrobasilar Junction is sligh tly greater th an 3 m m (range, 2 to 4.4 m m ), an d th e dis-
t an ce to t h e cen ter of th e in ter p edu n cu lar fossa is ~ 10 m m
Gran d et al28 described fou r grou ps of perforat ing ar teries of th e
(range, 5 to 14 m m ).32 To ch oose t h e ap p rop r iate su rgical ap -
low er basilar an d VA region accord ing to th eir p oin t s of en t r y
p roach to t h e basilar apex, to d efin e th e w orking sp ace, an d to
in to th e brainstem .
id en t ify t h e st r u ct u res p reven t in g access, a su rgeon m u st con -
Per forators in grou p I ar ise from t h e p roxim al VA an d or igin
sider th e relat ion sh ip s am ong th e basilar bifu rcat ion an d m am -
of PICA, p en et rat ing th e lateral m edu llar y area ju st cau dal to th e
m illar y bod ies, d orsu m sellae, an d p ed u n cles, as w ell as t h e bi-
posterior olivar y su lcu s an d th e m ost cau dal por t ion of th e pos-
fu rcat ion angle an d locat ion s of th e perforators.32
terior olivar y su lcu s.28 After p en et rat ing th e m edu lla, th ese per-
Differen t classificat ion sch em es h ave been proposed to de-
forators cu r ve sligh t ly d orsally an d su p p ly t h e n u cleu s an d t ract
scribe th e ar teries pen et rat ing th e brain stem (Fig. 4.2). Th e vas-
of t h e t r igem in al n er ve; sp in al t h alam ic an d sp in al cerebellar
cular dist ribu t ion h as been illust rated by Tat u et al34 on slides
t ract s; in ter n al arcu ate fibers; n u cleu s am bigu u s; d orsal m otor
corresp on ding to th e bicom m issu ral p lan e t h at can be com pared
n ucleus of th e vagus n er ve; lateral ret icular n ucleu s; an d, som e-
w ith CT an d MR angiograph ic results (Fig. 4.5). Lazor thes et al35
t im es, p ar t of th e hypoglossal n u cleu s.28
an d Foix an d Hillem an d 36 divided th e superficial ar teries in to
Group II perforators arise from th e lateral m edullar y port ion
an terior an d param edian , lateral an d sh or t circum feren t ial, an d
of th e PICA an d th e lateral aspect of th e dist al VA. Th ey pen et rate
posterior an d long circum feren t ial group s, respect ively, accord-
th e p osterior olivar y su lcu s, su pp lying th e d orsal accessor y olive,
ing to th eir en t r y poin t in to t h e paren chym a. Duvern oy 37,38 sub -
dorsal in ferior olive, n u cleu s am bigu u s, dorsal m otor n u cleu s of
d ivid ed ar ter ies of th e an ter ior grou p in to an terom ed ial an d
th e vagu s n er ve, sp in al t h alam ic t ract s, n u cleu s an d t ract of th e
an terolateral groups, dividing brain stem territories in to antero-
t rigem in al n er ve, solit ar y fascicu lu s, in ferior salivator y n u cleu s,
m edial, an terolateral, lateral, an d posterior arterial groups, based
lateral ret icular n ucleu s, an d low er rest iform body.28
on w h ere th ey pen et rate th e brain stem . Medial bran ch es are also
Th e grou p arising from th e lateral aspect of th e VBJ an d from
called m ed ian or p aram ed ian , an d lateral bran ch es are called
t h e AICA (grou p III) an d t h e grou p ar isin g from t h e VBJ d orsal
t ran sverse or circu m feren t ial.29 Som e bran ch es are su bd ivid ed
su rface t h at p en et rates t h e foram en cecu m (grou p IV) are d e-
in to m edian , in term ediate, lateral, an d posterior groups.28 Th e
scribed w ith th e BA p erforators, below.
BA collaterals are divided in to perforat ing ar teries, large p on t in e
vessels, an d cerebellar ar teries, w h ich , in t u rn , often bran ch in to
th e an terolateral bran ch es.39
Param edian bran ch es term in ate in th e lateral pon s, pedun cle,
■ Basilar Artery an d posterior perforat ing substan ce. Sh or t circum flex ar teries
Th e BA origin ates w ith th e fu sion of both VAs n ear th e p on to- pen et rate th e ven t ral asp ect of th e brain stem lateral to th e para-
m edullar y jun ct ion an d term in ates w ith bifu rcat ion of th e pon - m edian bran ch es. Long circum flex arteries en ter th e dorsal as-
tom esen ceph alic jun ct ion .12,24,29 Its diam eter (range, 3.75 to 4.1 pect of th e brain stem .29 On average, th ere are 11 sh or t an d eigh t
m m ) m ay reach 3.5 m m at th e level of th e su perior cerebellar long circu m flex ar ter ies, w h ich or igin ate from t h e d ist al BA in
ar ter y an d m ay in crease to 4.1 m m at th e bifurcat ion , w iden ing t w o-t h ird s of cases, w it h h alf from th e p oster ior su r face an d
w ith a cobra-like appearan ce in 16% of th e cases.12,29–31 Th e on e-fou r th on each side. Non e arise from t h e an terior BA su r-
m ean length of th e BA is 32 m m (range, 15 to 40 m m ).29 Th e basi- face.12,29 Th u s, th e p roxim al BA rep resen t s th e preferred site for
lar bifurcat ion m ay be as far rost ral as th e m am m illar y bodies occlusion. Several bran ch ing pat tern s are obser ved, w ith vessels
and as far caudal as 1.3 m m below the pontom esencephalic junc- arising as single bran ch es or com m on t r un ks.12 A com plex ar te-
t ion .29 Mean dist an ces of 5 to 10 m m bet w een th e basilar bifu r- rial p lexu s m ay be form ed in the interpeduncular fossa by upper
cat ion an d m am m illar y bodies h ave been rep or ted, w ith overall param edian arteries em erging 2 or 3 m m below th e basilar bifur-
dist an ces ranging from 0 to 20 m m .29,32 Relat ive to th e dorsu m cat ion an d interm ixed w ith th e m edial P1 branches.29 Although
sellae, th e basilar ap ex is above th e biclin oid lin e (u p to 15.3 m m ) anastom oses m ay occu r bet w een th e long circum flex bran ch es
(text cont inues on page 59)

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Fig . 4.5 Dom inant arterial territories of the brainstem and cerebellum substantia nigra; 22, inferior colliculus; 23, trochlear nucleus; 24, colliculus
on axial sections. The sections correspond and can be transposed on MR superior; 25, oculom otor nucleus; 26, red nucleus; 27, m amm illary body;
im ages. 1, corticospinal tract; 2 m edial lem niscus; 2′, m edial longitudinal 28, optic tract; 29, lateral geniculate body; 30, tonsil; 31, biventer lobule;
fasciculus; 3, spinothalam ic tract; 4, spinal trigem inal tract and nuclei; 32, inferior sem ilunar lobule; 33, pyram id of verm is; 34, uvula; 35, superior
5, gracile and cuneate nuclei; 6, nucleus of the solitary tract; 7, dorsal sem ilunar lobule; 36, tuber of verm is; 37, m iddle cerebellar peduncle;
m otor vagal nucleus; 8, hypoglossal nucleus; 9, inferior olivary nucleus; 10, 38, dentate nucleus; 39, folium of verm is; 40, nodulus; 41, flocculus;
inferior cerebellar peduncle; 11, vestibular nucleus; 12, nucleus propositus; 42, declive; 43, simple lobule; 44, culmen; 45, quadrangular lobule; 46, cen-
13, facial nucleus; 14, superior olivary nucleus; 15, abducens nucleus; 16, tral lobule; 47, ala of the central lobule; V, trigem inal nerve; VII, facial nerve;
pontine nuclei; 17, m otor trigem inal nucleus; 18, principal sensory trigemi- VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve. (Redrawn from
nal nucleus; 19, nucleus coeruleus; 20, superior cerebellar peduncle; 21, Tatu et al.34 )

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4 Cranial Vascular Anatomy of the Posterior Circulation 57

Fig. 4.5 (continued ) (continued on page 58)

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58 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 4.5 (continued )

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4 Cranial Vascular Anatomy of the Posterior Circulation 59

an d th e m ajor BA bran ch es, th ey are un usual bet w een th e sh or t 3 to 3.5 per BA).33,39 Th ese sm all perforators prim arily belong
circu m flex an d param edian vessels.12 to th e superior m edial pon t in e (60% of cases), in terpedun cular
(26% of cases), lateral pon t in e (12% of cases), or in ferior m edial
pon t in e grou p (2%).33 Th ey m ay be absen t in 8 to 16% of cases.33
Perforating Arteries In > 90%of cases, on e or t w o of th e p erforat ing vessels arise from
Perforat ing arteries are divided in to cau dal, m iddle, an d rost ral th e BA or th e early su perior cerebellar ar ter y. Less com m on ly,
group s. Cau dal p erforators arise as in dividual vessels or as com - th ey origin ate from th e p osterolateral or an terolateral arter y.39
m on t r u n ks from t h e d orsal BA bet w een t h e early BA an d th e Most ar teries origin ate rost ral to th e su perior cerebellar ar ter y,
or igin of AICA.39 Th ese vessels belong to grou p s III an d IV in th e but th ey m ay arise at th e level of th e superior cerebellar ar ter y
classificat ion of Gran d et al.28 Th ey m ay arise from th e AICA as (41.6%of cases), bet w een th e superior cerebellar ar ter y an d pos-
collateral bran ch es of th e p on tom edu llar y ar ter y or by a com - terolateral ar ter y (on e-t h ird of cases), or from t h e bord er be-
m on stem , by a com m on t runk w ith a perforator from th e m id- t w een th e BA an d PCA (on e-sixth of cases). Th e m ean d ist an ce
dle grou p , or as collateral bran ch es of th e PICA or of a com m on from th e origin of th e perforators to th e su p erior cerebellar ar-
PICA–AICA trunk.39 Caudal perforating arteries descend along the ter y is 1.3 m m (range, 0.7 to 2.1 m m ) an d site is 2.5 m m (range,
basilar su lcu s an d en ter t h e foram en cecu m at t h e ju n ct ion of 0.9 to 3.9 m m ) to th e BA bifurcat ion . An astom oses (m ostly un i-
t h e p on tom edu llar y su lcu s an d th e an terior m edian su lcu s. Th ey lateral) are presen t in m ore th an 40% of brain s, in tercon n ect ing
often give rise to collateral bran ch es (~ 60% of cases), in clu ding th e rost ral p erforators, th alam op erforat ing bran ch es of th e PCA,
the pontom edullar y arter y, anterolateral branch es, branches pen - an d m ain stem of th e superior cerebellar ar ter y.
et rat in g t h e abd u cen t n er ve, pyram idal bran ch es, t w igs to t h e Alth ough several auth ors h ave repor ted th at a few perforators
rost ral par t of th e an terior m edian su lcu s of th e m edu lla, an d arise from th e BA t ip, large st udies h ave n oted th e absen ce of
large bran ch es to th e hyp oglossal n er ve. An astom oses are com - su ch p erforat ing bran ch es.32,40–42 On average, arou n d 2.5 sm all
m on bet w een cau dal perforators an d oth er bran ch es (50% in ci- h orizon t al bran ch es are seen in half of th e cases, supplying th e
den ce), in clu d ing m id d le BA p er forators (33% in cid en ce), VA or low est p ar t of th e p osterior p erforated su bst an ce an d su perior
an terior sp in al ar ter y p er forators (16% in cid en ce), an d con t ra- pon s.32 Th ey origin ate w ith a m ean angle of 93 degrees from th e
lateral cau dal perforators (8% in ciden ce). basilar ap ex (range, 75 to 110 d egrees). Perforat ing bran ch es
Middle p erforat ing ar teries origin ate as a com m on t ru n k or origin ating from th e last 5 m m of th e BA, th e in itial 7 m m of both
in dividu al vessels from th e p osterolateral su rface of th e m iddle superior cerebellar arteries, an d the initial P1 segm ent of the PCA
BA (bet w een th e origin s of th e AICA an d posterolateral ar ter y), pen et rate th rough a sm all space in th e u p per in terpedu n cu lar
w ith th e rost ral- an d cau dal-m ost ar teries ascen ding an d de- fossa.42 Th e an terior t w o-th irds of th is space is occup ied by th e
scen ding, respect ively, along th e basilar su lcu s.39 Th e bran ch es posterior perforated substance, and the posterior on e-third is th e
t ravel radially an d t ypically en ter th e edges of th e basilar sulcu s. pen et rat ion site of bran ch es th at su p ply th e in ferior m esen cep h -
In 25%of brain s, all m iddle perforators arise from th e BA. Middle alon . Th e p oster ior p er forated su bst an ce d ivid es in to an ter ior
perforators also com e from com m on t ru n ks w ith th e long pon - an d p oster ior h alves, w h ich are p er forated by t h e p aram ed ian
t in e ar teries (on e-fou r th to on e-th ird of cases), th e pon tom edu l- th alam ic an d th e su p erior p aram edian m esen cep h alic ar teries,
lar y ar ter y (on e-sixth of cases), an terolateral ar teries (on e-fou r th respect ively. Perforat ing ar teries origin ate from a t r un k exclu sive
of cases), t h e AICA (on e-sixt h of cases), t h e p osterolateral ar- to th e an terior h alf, posterior h alf, or both in 30%, 13%, an d 57%
ter y (on e-t w elft h of cases), or cau dal p er forators (on e-t w elft h of cases, respect ively. Param edian in ferior m esen ceph alic ar ter-
of cases). Per forators or igin ate at (on e-sixt h of cases) or below ies penet rat ing th e posterior on e-th ird of th e upp er par t of th e
(on e-fou r th of cases) th e level of th e AICA an d are n ever rost ral in terp ed u n cu lar fossa arise from th e P1 segm en t , t h e p roxim al
to th e posterolateral ar ter y. Th e sh or test distan ce bet w een th e 7 m m of th e superior cerebellar ar ter y, an d th e last 5 m m of th e
AICA origin an d th e n earest perforator ranges from 0.9 to 5.6 m m BA in 32%, 45%, an d 23% of cases, respect ively.
(m ean , 2.7 m m ).
Th ree t ypes of collateral bran ch es arise from th e m idd le p er-
forat ing ar teries. An terolateral bran ch es occur in all cases in Variations
w h ich the caudal branches supply (an d som etim es penetrate) the Fenestrations
abducen t n er ve. Long pon t in e ar teries occur in on e-four th of
cases. Th e pontom edullary artery occurs in on e-t w elfth of cases.39 Accord in g to large MR im agin g st u d ies, t h e p revalen ce of BA
A p erforat ing ar ter y, an terolateral vessel, an d bran ch to th e ab - fen est rat ion is as h igh as 2.1% an d is m ost com m on at th e proxi-
ducen t n er ve or a long p on t in e ar ter y form th e com p lex ar teries m al segm en t (94%of cases). Th e AICA arises from th e fen est rated
seen on th e righ t or left side in 41.6% or 58.3% of cases, respec- vessel in 39% of cases. Th e prevalen ce of fen est rat ion s at th e VBJ
t ively. In t w o-th irds of cases, on e or t w o an astom oses exist , m ost or V4 is 0.18% or 0.54%, resp ect ively. Th e PICA arises from th e
com m on ly bet w een t h e m iddle an d cau dal p erforat ing ar teries, fen est rated V4 in 56% of cases. Except ion ally, th e PICA an d th e
bet w een t w o adjacen t m iddle perforators, or (rarely) bet w een AICA m ay arise from th is fen est rated segm en t .43
rost ral an d m iddle p erforators or left an d righ t on es. Term in al
bran ch es of t h e m id d le p er forators p en et rate t h e edges of t h e
Carotido -Vertebrobasilar Anastomoses
basilar su lcu s an d d ivid e in to t h e long an d sh or t in t rap on t in e
bran ch es, w h ich t ravel n ear th e rap h e of th e p on s. Trigem inal, otic, an d hypoglossal em br yonic arteries underlie de-
Rost ral ar teries arise as in dividu al vessels or com m on stem s velopm en t of th e ver tebrobasilar system .44 Persisten ce of on e of
from t h e lateral an d d orsal su rfaces of t h e ter m in al BA (m ean , th ese em br yon ic vessels m ay lead to a carot ido-ver tebrobasilar

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60 I Developm ent, Anatomy, and Physiology of the Central Nervous System

an astom osis. Th ese variat ion s, w h ich t ypically are un ilateral (but n er ve com plex to form rost ral an d caudal t ru n ks. Th e rost ral
occasion ally bilateral) an d fou n d in cid en t ally, m ay be resp on - t ru n k cou rses along th e m iddle cerebellar pedu n cle to th e su p e-
sible for isch em ic even ts or an eu r ysm s.1 rior lip of th e cerebellop on t in e fissu re an d th e adjoin ing p et rosal
su rface. Th e cau dal t ru n k feeds th e in ferior pet rosal su rface, in -
clu ding p ar t of t h e floccu lu s an d ch oroid p lexu s. Th e AICA gives
Persistent Trigeminal Artery
rise to p erforat ing ar teries th at su pp ly th e brain stem , ch oroidal
Th e m ost frequ en t an astom osis is a persisten t t rigem in al ar ter y bran ch es t h at su p p ly t h e tela an d ch oroid p lexu s, an d several
(in ciden ce 0.1 to 0.2% on cerebral angiograp hy), in w h ich th e n er ve-related ar teries.11,46
p osterior in t racavern ou s ICA is lin ked to th e d ist al t h ird of th e
BA bet w een t h e or igin s of AICA an d t h e su p er ior cerebellar ar-
ter y.44,45 Lateral or p et rosal p ersisten t t r igem in al ar ter ies ar ise Segments
from th e p osterolateral C4 segm en t of th e cavern ou s ICA an d Th e AICA is d ivid ed in to t h e an ter ior p on t in e, lateral p on t in e,
cross undern eath th e abducen t n er ve.45 Th e n er ve m ay be dis- floccu lop ed u n cu lar, an d cor t ical segm en t s (Fig. 4.4). Dep en d -
placed superiorly by the artery, w hich pierces th e dura just m edial in g on th e level of th e ar terial bifurcat ion , each segm en t m ay be
to th e sen sor y root of th e t rigem in al n er ve. Medial or sph en oidal com posed of m ult ip le t r u n ks.11,46
p ersisten t t r igem in al ar ter ies ar ise from t h e p osterom ed ial C4
segm en t of th e caver n ou s ICA an d p ierce t h e d u ra of t h e d or- Anterior Pontine Segment (A1)
su m sellae. Th e BA proxim al to th is an astom osis an d th e VA are Th is segm en t is located bet w een th e clivu s an d th e belly of th e
hypoplast ic in 85% of cases. Th e size of th e ipsilateral posterior p on s. It exten d s from t h e or igin of AICA to t h e level of a lin e
com m u n icat ing ar ter y (PCoA) is inversely p rop or t ion al to th e exten ding u pw ard on th e pon s an d p assing th rough th e long axis
size of th e p ersisten t t rigem in al ar ter y.44 Th e p ersisten t t rigem i- of th e in ferior olive. Th e an terior pon t in e segm en t usu ally con -
n al ar ter y m ay com press th e abducen t n er ve, result ing in diplo- tacts th e abducen t n er ve rootlet s.11,46
p ia an d ir r it at ion of t h e t r igem in al n er ve associated w it h facial
n eu ralgia.45
Lateral Pontine Segment (A2)
Th is segm en t st art s at th e an terolateral m argin of t h e p on s. It
Otic Artery t ravels th rough th e cerebellopon t in e angle above, below, or be-
t w een t h e facial an d vest ibu lococh lear n er ves in p roxim it y to
Th e realit y of an ot ic ar ter y an astom osis is d ebated in t h e lit -
t h e in tern al au ditor y m eat u s, lateral recess, an d ch oroid plexu s
erat u re.44 It presum ably arises from th e ICA in th e in t rapet rous
prot r u ding from th e foram en of Lu sch ka. Th e AICA h as several
carot id can al, ru n s t h rough th e in tern al au ditor y can al, an d fu ses
n er ve-related bran ch es, in clu ding th e labyrin th in e ar ter y, w h ich
w ith th e cau dal BA.
su p plies th e facial an d vest ibu lococh lear n er ves as w ell as th e
vest ibulococh lear labyrin th ; th e recurren t perforat ing ar teries,
Hypoglossal Artery w h ich pass tow ard th e m eat us but t urn m edially to su pply th e
brain stem ; an d th e subarcuate ar ter y, w h ich en ters th e su barcu -
Th e in cid en ce of hyp oglossal ar ter y an astom osis is 0.02 to
ate fossa. Th e lateral p on t in e segm en t is divided in to p rem eatal,
0.09%.1,44 Bilateral an om alies, w h ich are obser ved in 1.4% of
m eatal, an d post m eatal port ion s, depen ding on its relat ion sh ip
cases, are sligh tly m ore frequ en t in w om en an d on th e left side.44
w ith th e poru s of th e in tern al acoust ic m eat us.11,46
Th e hypoglossal arter y st ar t s at th e posterior ICA u su ally at th e
C1–C2 level but n ever below C3–C4. Th e ar ter y ascen ds a sh ort
dist an ce p osteriorly an d sligh tly m edially u p to th e hypoglossal Flocculopeduncular Segment (A3)
can al, in w h ich it ru n s before en ding in th e BA. Th is segm en t p asses t h e floccu lu s rost rally or cau d ally, before
reach ing t h e m id d le cerebellar p ed u n cle an d cerebellop on t in e
fissu re. Tr u n ks t h at cou rse alon g t h e p ed u n cle m ay be h id d en
Branches ben eath th e flocculu s or th e lips of th e cerebellum .11,46
Major bran ch es of th e BA before th e vessel bifu rcates in to th e
PCAs are th e PICA (25% of cases), AICA, an d superior cerebellar Cortical Segment (A4)
ar ter y. Th e AICA ar ises from t h e p roxim al BA in m ore t h an 90% Th is segm en t is com posed of cor t ical bran ch es t h at su p p ly th e
of cases. Th e su p er ior cerebellar ar ter y exten d s from t h e ter m i- pet rosal surface of th e cerebellum .11,46
n al BA.39

Superior Cerebellar Artery


Anterior Inferior Cerebellar Artery
Th e su perior cerebellar ar ter y is th e m ost con st an t an d rost ral of
Th e AICA belongs to an d is closely related to several st r u ct u res of th e in fraten torial ar teries, belonging to th e u p per n eu rovascu lar
th e m iddle n eu rovascu lar com p lex, in clu ding th e p on s; m iddle com p lex w it h t h e m id brain ; cerebellom esen cep h alic fissu re;
cerebellar peduncle; cerebellopontine fissure; petrosal cerebellum su perior cerebellar pedun cle; ten torial surface of th e cerebel-
surface; and the abducent, facial, and vestibulocochlear nerves.11,46 lu m ; an d th e ocu lom otor, t roch lear, an d t rigem in al n er ves.11,33
Measu r in g 1 m m in d iam eter, t h e AICA t yp ically ar ises as a sin - Th e su p erior cerebellar ar ter y (m ean length , 1.38–1.5 m m ) u su -
gle t ru n k from th e p on t in e level of th e BA.11,12,46 It en circles th e ally arises from th e BA close to it s ap ex an d, in frequen tly, from
pon s, cou rses am ong th e abdu cen t , facial, an d vest ibu lococh lear th e p roxim al PCA.12,33,46 Each superior cerebellar ar ter y t ypically
nerves, and com m only bifurcates near the facial-vestibulocochlear origin ates as a single vessel from th e BA t run k, clearly separate

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4 Cranial Vascular Anatomy of the Posterior Circulation 61

from th e PCAs (35% of cases), or th e su p erior cerebellar ar teries su re. It form s a cau dal loop th at m ay exten d to th e m idp on t in e
or igin ate at t h e bifu rcat ion of t h e BA in to t h e PCAs (35% of level of th e root en t r y zon e of th e t rigem in al n er ve. Th e segm en t
cases).33 Less com m on ly, each su p erior cerebellar ar ter y m ay run s parallel an d below th e basal vein an d PCA. At it s m idpor-
origin ate from a PCA. On e superior cerebellar ar ter y m ay exit t ion , it crosses th e t roch lear n er ve in feriorly. Alth ough th e an te-
from th e PCA, w h ile th e con t ralateral su p erior cerebellar ar ter y rior par t of t h is segm en t is often obser ved above th e ten torial
arises from th e BA. On e superior cerebellar ar ter y m ay origin ate edge, its cau dal loop is usually located below th e ten torium .11,46
at th e BA bifu rcat ion in to th e ipsilateral PCA, w h ile th e oth er
origin ates directly from th e con t ralateral PCA. Duplicate supe- Cerebellomesencephalic Segment (S3)
rior cerebellar ar teries m ay arise from th e BA bilaterally, or t w o This segm ent courses w ithin the cerebellom esencephalic fissure.
su p erior cerebellar ar teries m ay arise from on e side of th e BA, Th e su p erior cerebellar ar ter y bran ch es en ter th e fissu re at it s
w h ile a single superior cerebellar arter y origin ates from the oth er sh allow est part above th e t rigem in al root en t r y zon e. Th e ar ter y
side.33 Th e superior cerebellar arter y usually arises as a single t ravels m edial to th e ten torial edge w ith it s bran ch es in ter t w in ed
t ru n k (90% of cases) th at bifu rcates at th e am bien t cistern in to w ith th e t roch lear n er ve. Th e superior cerebellar ar ter y un der-
rost ral an d caudal t ru n ks (or m edial an d lateral t run ks), m ost goes several sh arp loops deep in to th e fissure an d passes upw ard
com m on ly at a th ird of th e dist an ce arou n d th e u pp er p on s in to reach th e an terior ten torial surface, on th e low er m argin of th e
th e ven t rolateral region . How ever, th e su p erior cerebellar arter y ten torium .11,46
m ay arise as a dou ble or du plicate t r u n k.12,33,46 Th e rost ral t ru n k
supplies the verm ian and paraverm ian areas, and the caudal trun k Cortical Segment (S4)
su pplies th e h em isph ere on th e su boccip ital surface.46 Th is segm en t in clu des bran ch es dist al to t h e cerebellom edu llar y
Th e su perior cerebellar ar ter y gives off p erforat ing bran ch es fissure an d below th e ten torial edge. Cor t ical bran ch es term in ate
to th e brain stem an d cerebellar pedun cles.46 It h as th e m ost con - in to th e h em isph eric an d verm ian ar teries as w ell as in to a m ar-
st an t n u m ber of regu larly sp aced perforat ing bran ch es t h rough - gin al bran ch .46 Th e cort ical territor y of th e su perior cerebellar
out the cisternal course, w ith the least num ber of branches arising ar ter y is m ore con st an t th an th at of th e AICA an d PICA. It m ay
before th e bifurcat ion on th e m ain t r un k or im m ediately after var y from th e par t of th e ten torial surface th at lies an terior to th e
th e bifu rcat ion on th e proxim al h alf of th e ceph alad or cau dal ten torial fissu re by as m uch as a full h alf of th e ten torial surface,
bran ch .12 Because perforators arise on th e first 1 m m (on e-th ird overlapping onto th e opposite h alf of th e verm is, superior su b -
of cases) or 2 m m (h alf of cases) of t h e p roxim al su p er ior cere- occipital surface, and the upper t w o-thirds of the petrosal surface,
bellar ar ter y, th e p roxim al su p erior cerebellar ar ter y is n ot a in cluding both lips of th e pet rosal fissure.46
perforator-free segm en t .33
Perforators en ter th e brain stem in t w o m ain zon es. Th e in ter-
pedu n cu lar grou p , su perior an d in ferior por t ion s of th e m edial
pon t in e grou p , lateral p on t in e grou p , an d basal cerebellar grou p
en ter at th e basal p erforator zon e, an d t h e lem n iscal t rigon e
■ Posterior Circle of Willis Variations
grou p en ters at th e dorsal perforator zon e.33,47 Direct proxim al Th e m ain variat ion s of th e p osterior p or t ion of th e circle of Willis
su p erior cerebellar ar ter y p erforators belong to th e in terpedu n - are th e n orm al (adult t ype), fet al, an d t ran sit ion al/in term ediate
cular (85% in ciden ce) or superior m edial pon t ine group (15%).33 con figu rat ion s. Based on t h e associat ion bet w een brain d evel-
Sh or t circu m flex p er forators en ter at th e lateral p on t in e an d op m en t al st age an d t h e occu r ren ce of d ifferen t con figu rat ion s
par t of t h e su p er ior m ed ial pon t in e zon es. Th e least com m on of th e posterior circle of Willis, Van Overbeeke et al48 con clu ded
lon g circu m flex perforators belong to th e basal cerebellar grou p . th at variat ion s of th is st ru ct u re resu lt from develop m en t al m od -
Th e lem n isu p er ior sp in al ar ter y t r igon e grou p is located at th e ificat ion s. In d eed, th e frequ en cies of th e adu lt an d fetal con figu -
posterolateral su rface of th e brain stem an d is related to th e rat ion s gradu ally in crease at th e exp en se of t ran sit ion al con figu-
tegm en t u m . rations. A norm al posterior circle of Willis (incidence, 14 to 65.4%)
is defin ed by th e p resen ce of both P1 segm en t s w ith a diam eter
larger th an th at of th eir PCoAs.29,48–53 Variat ion s in clude PCoA
Segments
an d P1 hypoplasia (diam eter, < 1 m m )30 or absen ce, eith er un ilat-
Th e su p erior cerebellar ar ter y is divid ed in to an terior p on tom es- erally or (m ore rarely) bilaterally. A hypop last ic PCoA an d P1 give
encephalic, lateral pontom esencephalic, cerebellom esencephalic, rise to t h e sam e n u m ber an d size of p erforat ing ar teries, w h ich
an d cor t ical segm en t s (Fig. 4.4). term in ate sim ilar to n orm ally sized segm en ts. Th erefore, hypo-
plast ic segm en ts sh ou ld be h an dled w ith care an d divided to ex-
Anterior Pontomesencephalic Segment (S1) pose th e basilar bifurcat ion on ly after careful con siderat ion .29
This segm ent courses bet w een the dorsum sellae and upper brain- Fetal con figu rat ion of th e p osterior circle of Willis (4 to 28%
stem . It begin s at th e origin of su perior cerebellar ar ter y an d u n ilaterally in ciden ce, 2 to 12%bilaterally) 54,55 is broadly defin ed
p asses below t h e ocu lom otor n er ve (in t h e case of an or igin as th e case in w h ich P1 h as a sm aller diam eter th an PCoA.29,30,51
from th e PCA, it passes above th e n er ve). It exten ds to th e an - Van Raam t et al56 con sidered th is case as th e “p ar t ial” fet al con -
terolateral brain stem m argin . It s lateral par t courses m edial to figurat ion , defin ing th e “full” fet al con figurat ion by absen ce of P1
th e an terior h alf of th e free ten torial edge.11,46 on CT or MR angiography or by n o filling after VA con t rast injec-
t ion , w ith th e PCA arising from th e ICA. Th e fetal con figu rat ion ,
Lateral Pontomesencephalic Segment (S2) w h ich results in a larger area depen ding on th e ICA an d im plies
This segm ent extends from the anterolateral m argin of the brain - that leptom eningeal vessels cannot develop bet w een th e anterior
stem to th e an terior m argin of th e cerebellom esen cep h alic fis- an d posterior circulat ion s,56 is associated w ith an in creased risk

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62 I Developm ent, Anatomy, and Physiology of the Central Nervous System

of developing an ICA an eur ysm due to in creased flow in to th e P2 Segment


ICA.57 In th e t ran sit ion al con figu rat ion , th e diam eters of PCoA
Th e P2 segm en t (also called th e perim esen ceph alic or p ostcom -
an d P1 are th e sam e.49,56
m un icat ing segm en t) start s at th e level of th e jun ct ion bet w een
th e PCoA an d PCA. It ru n s in to th e cru ral an d am bien t cistern s
an d en ds at th e posterior edge of th e lateral m idbrain .30,31,58 Be-
cau se th e an terior an d p osterior p or t ion s of th e P2 segm en t re-
■ Posterior Cerebral Artery qu ire dist in ct su rgical ap p roach es an d to aid in id en t ifying th e
origin of th e m any bran ch es from th e P2 segm en t, th e P2 seg-
As th e m ost im por t an t ar terial st ru ct u re of th e p erim esen ce-
m en t is divided in to an an terior part (called th e P2A, cru ral, or
ph alic cistern , th e PCA arises at th e basilar bifu rcat ion . Alth ough
pedun cu lar segm en t) an d a posterior par t (called th e P2P, am bi-
it t ypically origin ates in th e in terpedu n cu lar cistern at th e level
en t , or lateral m esen cep h alic segm en t). Th e P2A cou rses arou n d
of th e pon tom esen ceph alic jun ct ion (t w o-th irds of cases), it m ay
t h e cerebral p ed u n cle in t h e cr u ral cister n , w h ereas t h e P2P
be located as far caudally as 1.3 to 2 m m below th e pon tom esen -
cou rses lateral to th e m idbrain in th e am bien t cistern .30
ceph alic jun ct ion an d as far rost rally as th e m am m illar y bodies
Various auth ors h ave defin ed th e t ran sit ion bet w een th e P2
an d adjacen t floor of th e th ird ven t ricle, w h ich m ay be elevated
an terior an d posterior par ts differen tly. Zeal an d Rh oton ,31 w h o
by a h igh bifu rcat ion . Th e PCA join s th e PCoA at th e lateral m ar-
coin ed th e term s P2A an d P2P, defin ed th e t ran sit ion area as th e
gin of th e in terpedu n cular cistern . It surrou n ds th e ipsilateral
posterior edge of th e cerebral peduncle, w h ich corresponds to the
peduncle, passes above the ipsilateral oculom otor nerve, and run s
lateral m esencephalic sulcus. Arguing that the transition can easily
th rough th e in terpedu n cu lar, cru ral, am bien t , an d qu adrigem i-
be iden t ified on angiography an d th at th eir defin it ion appropri-
n al cistern s, before being dist ributed to th e posterior h em isph ere
ately divides the range of the anterior and posterior approaches to
(Figs. 4.1, 4.2, 4.3).30,31,58 Th e PCA supplies th e basal surface of
th e PCA, Párraga et al58 con sidered th e t ran sit ion to be th e later-
th e tem poral an d occip it al lobes an d sen ds crit ical bran ch es to
alm ost prom inent aspect of the peduncle, inside the am bient cis-
th e th alam u s, m idbrain , an d oth er deep st ru ct u res, in clu ding th e
tern. Yaşargil47,66 did not subdivide the P2 segm ent, w hich he stated
ch oroid plexu s an d w alls of th e lateral an d th ird ven t ricles (Fig.
term in ated at th e origin of th e an terior tem p oral ar ter y, a t ran si-
4.6).30,31,58 Fig. 4.7 d isp lays t h e terr itor y su p p lied by t h e PCA
tion point that m ight be m ore variable and difficult to ident ify.58
ap p licable to CT an d MR im aging slices described by Tat u et al,59
Th e P2A t ravels bet w een t h e cerebral p edu n cle an d th e u n cu s
var iat ion s in t h e ar ter ial d ist r ibu t ion rep or ted by var iou s au -
w ith in th e cr ural cistern , an average of 4 to 6 m m 58 below th e
th ors,36,60–63 as w ell as m in im al an d m axim al exten sion s.
optic tract (closer from the distal than from the proxim al P2A seg-
m en t). Th e P2A t ravels below Rosen th al’s basal vein th at crosses
th e cister n roof.30,31,58 Th e average d ist an ce bet w een th e an te-
Segments rior ch oroidal ar ter y an d P2A is 5.3 m m (range, 1 to 10 m m ).58
Th e PCA is su bd ivid ed in to P1 to P4 or P5 segm en t s (Figs. 4.1 and Th rough th e cru ral cistern , it passes at th e level of th e u n cal
4.3), according to several classificat ion s.29,31,47,58,64 Th e m ain dif- n otch in 94.3%of th e cases, above it (by 3 m m ) in 2.9%, an d below
feren ces bet w een th e classificat ion system s of Zeal an d Rh oton 31 it (by 1 m m ) in 1.4%.58 Th e P2P segm en t courses w ith in th e am -
an d Párraga et al58 involve th e su bdivision of th e P2 segm en t in to bien t cistern along th e lateral m idbrain an d m edial to th e para-
P2A an d P2P an d t h e t ran sit ion bet w een t h e P3 an d P4 seg- h ippocam pal an d dent ate gyri. It th en t ravels below th e opt ic
m en t s. Angiograph ic classificat ion s proposed by Krayen b h l an d t ract , Rosen th al’s basal vein , an d th e lateral gen iculate body, in -
Yaşargil64 an d by Margolis et al65 in clu de t w o (circu lar/basilaris ferolateral to th e pulvin ar an d su perom edial to th e t roch lear
an d cor t ical) or th ree (pedu n cular, am bien t , an d quadrigem in al) n er ve an d th e free edge of th e ten torium .30,31,58 It en ds at th e
angiograph ic segm en ts, resp ect ively. For Margolis et al,65 th e p e- lim it boundary bet ween the am bient and quadrigem inal cisterns.
dun cu lar segm en t is bisected by th e PCoA. Zeal an d Rh oton 31 repor ted sim ilar length s for both P2 segm en t
par ts (~ 25 m m ). Párraga et al58 rep or ted average length s of 23.6
m m (range, 18 to 30 m m ) an d 16.4 m m (range, 9 to 25 m m ) for
P1 Segment P2A an d P2P, respect ively, w ith diam eters of 1.7 m m (range, 1 to
3 m m ) an d 1.4 m m (range, 0.8 to 2 m m ), respect ively.58
Th e P1 segm en t (also called th e p recom m u n icat ing, p roxim al
pedu n cu lar, m esen cep h alic, circu lar, or basilar segm en t) exten d s
from th e BA bifu rcat ion to th e ju n ct ion w ith th e PCoA. It h as an
P3 Segment
average lengt h of 7 m m (ran ge, 3 to 20 m m ), w h ich is ~ 2 m m
longer in th e case of th e fetal p at tern . Th e P1 segm en t borders Th e P3 segm en t (also called th e qu adrigem in al segm en t), w h ich
th e cerebral pedu n cle w h ile t raveling in a m ediolateral direct ion . cou rses p osteriorly from th e p osterior edge of th e lateral m id-
It begin s in an in ferior an d posterior posit ion , coursing from m e- brain , h as an average length of 19.8 m m an d an average diam eter
dial to su p erior to th e ocu lom otor n er ve.30,31,58 Bran ch es of th e of 1.1 m m .58 Both P3 segm en t s t ravel from th e am bien t cistern to
P1 segm en t in clu de th e th alam operforat ing ar ter y, w h ich en ters th e lateral quadrigem in al cistern . Th ey converge m edially to th e
th e brain th rough th e posterior perforated su bstan ce; t h e m edial collicu lar or qu adrigem in al poin t located p osterior to th e collic-
posterior choroidal arter y, w hich is directed to the ch oroid plexus u li, w h ere arteries of each side (PCA t run k or calcarin e ar ter y
in th e th ird an d lateral ven t ricles; th e bran ch to th e quadrigem i- in th e case of bifu rcat ion in to term in al bran ch es before reach ing
n al plate; an d ram i to th e cerebral pedu n cle an d m esen ceph alic th is poin t ) are closest on an an teroposterior angiograp h ic view,
tegm en t um . separated by an average of 8.9 to 15.7 m m .30,31,58

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4 Cranial Vascular Anatomy of the Posterior Circulation 63

Fig. 4.6a–f Basal, lateral, and m edial views of the brain illustrating the includes anterior, m iddle, and posterior temporal; calcarine; and parieto-
cortical distribution of the posterior cerebral artery. (a) Most com m on pat- occipital arteries. In this situation the anterior temporal artery supplies the
tern observed in 44% of hem ispheres. This pat tern includes hippocampal, region usually supplied by the hippocampal artery. (c) Third m ost com m on
anterior temporal, and posterior temporal arteries. The cortical distribution pat tern, in 16% of hem ispheres. There is a com m on temporal artery that
of the parieto-occipit al artery is larger than that of the calcarine artery. supplies the entire inferior surface of the temporal lobe. The calcarine and
(b) Second m ost com m on pat tern, in 20% of hem ispheres. This pat tern parieto-occipital arteries are also present. (continued on page 64)

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64 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 4.6a–f (continued ) (d) Fourth most com mon pat tern, in 10% temporal arteries com e from the PCA as in 6% of cerebral hem i-
of hemispheres. In this situation, anterior and posterior temporal, spheres. The parieto-occipital artery supplied the greater portion of
calcarine, and parieto-occipital arteries are present but no hippo- the medial surface. (f) Last pat tern illustrating som e notable variant s.
campal or middle temporal branches of the PCA are found. The area of Two hippocam pal arteries arise from the posterior cerebral artery
the calcarine artery is split into t wo sectors to illustrate the presence (PCA), as occurring in 12%of cerebral hemispheres. The anterior tem -
of t wo calcarine arteries arising from the PCA (10% of hemispheres). poral artery fed a sm aller area than usual with subsequently a larger
(e) Fifth most common pat tern, occurring in 10% of hemispheres. It supply by the m iddle cerebral artery. The calcarine artery supplies an
includes hippocampal, anterior, m iddle and posterior temporal, cal- unusually large area on the medial surface. (Redrawn from Zeal and
carine, and parieto-occipital arteries. The area fed by the posterior Rhoton.31 )
temporal artery is split into t wo parts to illustrate that t wo posterior

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4 Cranial Vascular Anatomy of the Posterior Circulation 65

Fig. 4.7 Arterial territory of the posterior cerebral artery according to well as m inim al (E) and m axim al (F) distribution of the posterior cerebral
Tatu et al.59 at different levels and variations at the sam e level according to artery according to Beevor.74 PChA, posterior choroidal artery.
A, Duret 61 ; B, Foix and Hillem and 36 ; C, Zülch 62 ; D, Stephens and Stilvell63 ; as

Yaşargil47,66 an d Párraga et al58 defin ed th e t ran sition bet w een Branches


P3 an d P4 at th e origin of th e parieto-occipit al su lcu s along th e
Th e PCA bran ch es are divided in to th ree m ajor t ypes.30,31,58 Cen -
calcarin e fissu re, w ith th e P3 segm en t lying along or in side th e
t ral p erforat ing bran ch es su pp ly th e dien cep h alon an d m idbrain .
proxim al calcarin e fissu re. Zeal an d Rh oton 31 p roposed a ver y
Ven t ricular bran ch es supply th e ch oroid plexus an d w alls of th e
sh or t P3 segm en t , w ith th e P4 segm en t star t ing at th e an terior
lateral an d th ird ven t ricles. Cerebral bran ch es su p ply th e cere-
lim it of th e calcarin e fissu re. Th e parieto-occipit al su lcu s m ay
bral cor tex an d splen ium of th e corpu s callosum .
or igin ate at t h e or igin of th e p ar ieto-occip it al an d calcar in e
ar ter ies,47,66 bu t th e P3 segm en t u su ally con sist s of m u lt ip le
vascular t r unks because th e PCA bifurcates in to its m ajor term i-
Central Branches
n al bran ch es (calcarin e an d parieto-occipital ar teries) before it
reach es th e calcarin e fissu re.30,58 Cen t ral bran ch es are divided in to t w o grou ps: direct perforat ing
ar teries th at pass directly from th e paren t t run k to th e brain -
stem , an d circu m flex ar teries th at en circle th e brain stem before
P4 Segment
en tering th e dien cep h alon an d m esen cep h alon . Direct p erforat -
Th e P4 segm en t corresp on ds to PCA bran ch es th at ru n along or ing bran ch es en com p ass th e t h alam operforat ing ar teries arising
in sid e t h e p ar ieto-occip it al su lcu s an d d ist al calcar in e fissu re. from P1 an d th e th alam ogen icu late an d pedu n cu lar perforat ing
Th e ar ter ies cor resp on d to t h e p ar ieto -occip it al an d calcar in e ar teries from P2. Circum flex bran ch es are divided in to long an d
ar teries, resp ect ively, an d in clude bran ch es th at d ist ribute to th e sh or t group s, depen ding on th e dist an ce th ey course aroun d th e
cor t ical su rface. brain stem .30

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66 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Thalamoperforating Arteries to six bran ch es),30,31,58 arise from th e su perior arter y (h alf of
cases) an d from t h e m ed ial su r face (34.3%of cases).58 Th ey p ass
Th alam operforat ing ar teries origin ate from th e P1 (p osterior
d irect ly from th e PCA in to th e cerebral pedun cle to irrigate th e
group ) an d PCoA (an terior grou p). Th e largest arter y in th e pos-
cor t icospin al an d cor t icobu lbar t ract s, su bst an t ia n igra, red n u -
terior th alam operforat ing group (called th e th alam operforat ing
cleus, m esencephalic tegm ent um , and nucleus of the oculom otor
ar ter y) is usually th e first P1 bran ch an d m ay h ave a diam eter of
n er ve.30,31,58
1.5 m m .29,30 An average of th ree an d as m any as 10 th alam oper-
forat ing bran ch es are seen .29,58 Occasion ally, P1 m ay n ot provide
any th alam operforat ing ar teries, an d th e territor y is su pplied by Circumflex Arteries
w ell-developed con t ralateral bran ch es.29 If th e first P1 bran ch is
Circum flex ar teries in clude sh ort an d long circu m flex vessels,
n ot a th alam operforat ing ar ter y, it correspon ds to a circu m flex
dep en ding on w h eth er th ey reach th e gen icu late bodies or col-
branch that ends in the peduncle or posterior m esencephalic area.
liculi. Circum flex arteries arise from P1 and P2 and course around
Th alam operforat ing bran ch es m ost often arise from th e m iddle
th e cerebral pedu n cle, in feriorly an d m edially to th e PCA, an d
third of P1, follow ed by the m edial or lateral third.30 Although they
sup eriorly to th e su perior cerebellar ar ter y.30,31,58
t ypically origin ate from th e p osterior P1 (t w o-thirds of cases),
Sh or t circu m flex ar teries t ravel on ly a sh or t dist an ce arou n d
th ey also m ay origin ate from th e su perior su rface (less th an on e-
the brain stem before en tering the brain.31 They originate from P1
th ird of cases) or, rarely, from th e an terior su rface.30,58
in 51.4% an d from P2A in 48.6% of h em isph eres, w ith an average
Th alam operforat ing ar teries t ravel posteriorly in to t h e u p p er
of 1.2 bran ch es.58 Párraga et al58 obser ved on e to t h ree bran ch es,
in ter p ed u n cu lar fossa, m ed ial to t h e cerebral p ed u n cle an d oc-
w h ereas Zeal an d Rh oton 31 n oted sh or t circu m flex ar teries in
u lom otor n er ve. Th ey cou rse beh in d t h e m am m illar y bod ies,
66% of h em isph eres. Th e arteries are located m edial to th e P2
p ass t h rough t h e p oster ior p er forated su bst an ce, an d en ter th e
segm ent , m edial posterior choroidal arteries, and long circum flex
brain .29,58 Th e PCoA bran ch es th at en ter th e sam e area are called
ar teries.30,31 Th ey p rovide bran ch es to th e posterolateral border
prem am m illar y arteries.30 Th ey supply th e an terior th alam us
of th e cerebral pedun cle an d m edial gen icu late body. Th ey m ay
an d par t of th e posterior thalam u s, hypoth alam us, subth alam us,
sen d ram i to th e in terp edu n cu lar fossa an d posterior perforated
an d m edial upper m idbrain, in cluding th e subst an t ia n igra, red
su bstan ce, w h ich are p redom in an tly su p plied by th e th alam o-
n ucleus, th ird an d four th cran ial n er ve n uclei, oculom otor n er ve,
perforat ing arteries.31 Sh or t circu m flex ar teries arising from P1
periaqu edu ct al ret icu lar form at ion , an terom edial su rface of th e
term in ate at th e posterolateral border of th e pedun cle in 76% of
fou r th ven t ricle, an d p osterior lim b of th e in tern al capsule.30,58
th e cases, at th e tegm en t al region in 11%, an d at t h e m ed ial ge-
n icu late body in 13%, w h ereas th ose arising from P2 su pply on ly
Thalamogeniculate Arteries th e gen iculate bodies an d m idbrain tegm en t um .30,31
Long circum flex ar teries (also called quadrigem in al ar teries)
An average of 2.4 to 3.6 th alam ogen iculate arteries (range, on e to are presen t in 96% of h em isph eres.31 Th ey origin ate from P1 in
17 vessels) origin ate directly from th e P2 segm en t ben eath th e ~ 80%, just distal to th e origin of th e sh or t circu m flex ar teries,
lateral t h alam u s.29,30,58,67 Accord ing to Pár raga et al,58 t h alam o - an d from P2A in 14.3 to 20%, an d from th e in ferior aspect of th e
gen icu late ar teries p rim arily origin ate from th e P2P segm en t ar ter y in 85.7% of cases.31,58 Usu ally on e or t w o bran ch es are
(90% of cases) im m ediately after th e t ran sit ion from P2A to P2P en cou n tered (m ean , 1.1 bran ch es).58 Th ey t ravel arou n d t h e
or from th e P2A segm en t (5.7%). Zeal an d Rh oton 31 n oted th at brain stem m edial to th e PCA th rough th e crural, am bien t, an d
th ese ar teries arise n ear th e ju n ct ion of P2A (cru ral) an d P2P qu adrigem in al cistern s to su p ply th e qu adrigem in al p late.30,58
(am bient) in nearly equal proportion. Branches originate from the Th ey give off five or m ore sm all ram i to th e cerebral p edu n cle
su p erior ar ter y (62.9% of cases), follow ed by th e m edial (21.4%) an d gen icu late bodies an d, occasion ally, to th e tegm en t um an d
an d in ferior ar teries (2.7%).58 pu lvin ar, an d en d at th e qu adrigem in al p late. Term in al bran ch es
Th alam ogen icu late ar teries cou rse su p eriorly tow ard th e roof of th e long circum flex arteries form a rich ar terial n et w ork over
of th e am bien t cistern form ed by th e lateral gen icu late body an d th e collicu li, w h ere th ey an astom ose w ith th e su p erior cerebel-
th e p u lvin ar of th e th alam u s. Th ey th en p erforate th e in ferior lar arter y bran ch es. Th e superior an d in ferior colliculi are su p -
su rface of th e gen icu late bodies to su pp ly th e p osterior h alf of plied by bran ch es from th e PCA an d su perior cerebellar ar ter y,
th e lateral th alam u s, p osterior lim b of th e in tern al capsu le, an d respect ively.30,31
optic t ract .30,31 Th ey en cou n ter th alam op erforat ing bran ch es of
P1 close to th e m iddle of th e th alam u s an d th e prem am m illar y
bran ch of th e PCoA an teriorly in th e lateral n u cleu s. Th is area is Ventricular and Choroid Plexus Arteries
also fed by branch es of th e long an d sh or t circu m flex an d m edial Th e PCA an d it s bran ch es give off vessels called p osterior ch oroi-
posterior ch oroidal ar teries as th ey en circle th e brain stem . How - dal ar teries, w h ich pen et rate th e lateral an d th ird ven t ricles an d
ever, th e term thalam ogeniculate arteries is reser ved for bran ch es su p ply th e ch oroid p lexu s an d ven t ricu lar w alls. Medial an d lat-
th at arise directly from th e PCA.30,31 eral p osterior ch oroidal ar teries h ave been described, according
to th eir origin an d su pp ly area.30
Th e m edial p osterior ch oroidal ar teries m ost frequ en tly arise
Peduncular Perforating Arteries
from th e p osterom ed ial asp ect of th e proxim al PCA or on e of it s
Most of th e p edu n cu lar p erforat ing arteries arise from th e P2A bran ch es.30 Dep en d ing on t h e classificat ion sch em e u sed, t h e
segm en t (58.6% an d 94% of cases, accord ing to Pár raga et al 58 m ed ial p oster ior ch oroidal ar ter ies or igin ate from t h e P1 in 12
an d Zeal an d Rh oton ,31 resp ect ively), follow ed by t h e P1 an d to 14.3% of th e h em isp h eres, from P2A in 50 to 70%, from P2P
circum flex arteries. On average, 2.8 to 3.3 bran ch es (range, zero in 5.7 to 21%, from P3 in 4 to 5.7%, an d from P4 in 1.4 to 13%.31,58

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4 Cranial Vascular Anatomy of the Posterior Circulation 67

In m ore th an 50% of h em isph eres, on e ar ter y is n oted,31,58 w ith p u lvin ar, dorsom edial th alam ic n uclei, an d body of th e caudate
t w o an d th ree ar teries being rep or ted in 32% an d 14% of th e n ucleus.30,31,68
h em isph eres, resp ect ively.31 Th e m edial p osterior ch oroidal ar-
teries course parallel an d m edially to th e m ain PCA t run k, en cir-
Cerebral Branches
cling th e m idbrain to reach th e qu adrigem in al cistern . Th ey t u rn
an teriorly along th e lateral pin eal glan d to en ter th e roof of th e Cerebral bran ch es of t h e PCA in clu d e t h e in fer ior tem p oral,
th ird ven t ricle w ith in th e velu m in terp osit u m cistern bet w een p ar ieto-occipit al, calcarin e, an d splen ial ar teries (Figs. 4.1b,c,
th e th alam i. Th ey t ravel along th e ch oroidal fissu re before reach - 4.3, 4.6, 4.7).
ing an d passing th rough th e foram en of Mon ro an d term in at ing
in th e ch oroid p lexu s of th e lateral ven t ricle.30,31,58
Inferior Temporal Artery
Med ial p osterior ch oroidal ar teries arising from th e p arieto-
occipital an d calcarin e ar teries an d th e distal PCA h ave a ret ro- In ferior tem poral ar teries, in cluding th e h ippocam pal, an terior,
grad e cou rse from t h eir or igin to en ter t h e roof of t h e t h ird m iddle, posterior, an d com m on tem poral arteries, origin ate at
ven t ricle.30 In 12% of h em isp h eres, a m edial p osterior ch oroidal th e PCA.30,58 Tem poral bran ch es arising from th e m iddle cerebral
ar ter y bran ch cou rses laterally w ith in th e qu adrigem in al cistern ar ter y are called su perior tem poral ar teries.30,31 According to
beh in d th e pulvin ar an d th rough th e ch oroid fissure in to an area Párraga et al,58 in ferior tem poral ar teries origin ate at th e t ran si-
th at is usu ally fed by a lateral p osterior ch oroidal ar ter y.31 In 17% t ion bet w een th e P2A an d P2P segm en ts in 45.7%of h em isp h eres
of h em isph eres, a bran ch from P2A (a circum flex bran ch of th e an d from th e P2A or P2P segm en t in 25.7%. An average of th ree
parieto-occipit al ar ter y) join s w ith th e m edial p osterior ch oroi- in ferior tem p oral arteries (range, t w o to five arteries) course lat-
dal ar ter y to form a single ar ter y th at en ters th e roof of th e th ird erally along t h e basal tem p oral lobe. Th ey reach th e lateral su r-
ven t ricle.31 Along th eir cou rse, th e m edial p osterior ch oroidal face of th e m iddle tem poral gyr us in 42% of th e h em isph eres,
ar teries send bran ch es to th e cerebral pedun cle, m esen ceph alic especially th e posterior tem poral ar ter y.30,31,58 Tem poral ar teries
tegm en t u m , m edial an d lateral gen iculate bodies, colliculi, pul- prod u ce bran ch es th at pass th rough th e ch oroidal fissu re in to
vin ar, pin eal glan d, an d m edial an d dorsal th alam us.30,31,58 th e tem p oral h orn of th e lateral ven t ricle to reach areas su p plied
Th e lateral posterior ch oroidal ar teries arise from th e PCA or by th e lateral posterior ch oroidal ar teries.30,31 Th ese ar teries su p -
it s bran ch es. Th ey r u n laterally t h rough t h e ch oroidal fissu re ply th e in ferom edial su rface of th e tem p oral lobe, in clu ding th e
an d u pw ard over th e pulvin ar to supply th e ch oroid plexu s of th e uncus, hippocam pus, parahippocam pal gyrus, and dentate gyri.58
lateral ven t ricle.30,31 An average of t w o to fou r lateral posterior Five group s of in ferior tem poral arteries h ave been prop osed
ch oroidal ar teries are n oted (range, on e to n in e vessels),68 w ith a on t h e basis of t h e bran ch es an d t h eir su p p ly area.29–31,58 In
single ar ter y being obser ved in 12% of cases.31 According to Zeal grou p 1 (10 to 36% in cid en ce), all of t h e in fer ior tem p oral
an d Rh oton ,31 lateral posterior ch oroidal ar teries arise m ost fre- bran ch es are presen t (h ippocam pal, an terior, m edial, an d poste-
qu en tly directly from th e P2P segm en t (35%), follow ed by th e rior arteries).30,31,58 In group 2 (16 to 23%incidence), a single large
P2A an d P3 segm en t s (16%an d 13%, resp ect ively). Th e PCA is th e t ru n k (th e com m on tem p oral ar ter y) arises from th e PCA an d
m ost com m on origin (25% overall in ciden ce), follow ed by PCA su p plies th e en t ire in ferior tem p oral lobe th rough it s bran ch es.
bran ch es such as th e h ippocam pal (8%), an terior tem poral (10%), Grou p 3 (8 to 20% in ciden ce) lacks th e h ippocam p al arter y but
posterior tem poral (9%), m iddle tem poral (2%), p arieto-occip ital con t ain s th e an terior, m edial, an d p osterior tem p oral ar teries.
(13%), m edial posterior ch oroidal ar ter y (4%), an d calcarin e ar- Grou p 4 (7 to 10% in cid en ce) lacks th e h ipp ocam pal an d m edial
teries (2%). The largest lateral posterior ch oroidal ar teries are tem poral arteries, but the anterior an d posterior tem poral arteries
th ose th at arise directly from P2P.31,69 Párraga et al58 n oted th e are presen t . In group 5 (26 to 44% in ciden ce), th e m edial tem po-
lateral posterior choroidal artery originated from the P2P in 87.1% ral arter y is absen t, bu t th e h ippocam pal, an terior, an d p osterior
of h em isp h eres, from P2A in 7.1%, from P2A an d P2P in 4.3%, tem poral ar teries are presen t .30,31,58
an d from P3 in 1.4%. Ar teries origin ated from th e lateral an d su-
p er ior su r faces of t h e PCA in 78.6% an d 20% of h em isp h eres,
Posterior Hippocampal Arteries
respect ively.
Zeal an d Rh oton 31 rep or ted t w o differen t cou rses depen ding Zeal an d Rh oton 31 n oted on e or t w o p osterior h ip pocam p al ar-
on th e origin of th e ar ter y. Lateral posterior ch oroidal ar teries teries in 52%an d 12%of h em isph eres, respect ively (range, zero to
origin at ing from th e P2A segm en t or its cor t ical bran ch es course four ar teries).72,73 Th e posterior h ipp ocam pal ar ter y is th e first
laterally th rough th e ch oroidal fissure to th e ch oroid plexu s of cor t ical PCA bran ch , arising in th e cru ral or am bien t cistern .30,31,58
t h e tem p oral h or n an d glom u s of t h e p lexu s in t h e at r iu m of According to Zeal an d Rh oton , th e posterior h ippocam pal arter y
t h e lateral ven t ricle an d an astom ose w ith th e an terior ch oroidal origin ates from th e PCA in 64% of th ese cases, from P2A in 54%,
ar ter y.31,70,71 Lateral p osterior ch oroidal ar ter ies arising from an d from P2P in 10%. According to Párraga et al,58 th ese ar teries
P2P, P3, or t h eir cor t ical bran ch es cou rse over t h e p u lvin ar an d arise from th e P2A, com m on an d an terior tem poral ar teries, an d
ben eat h colu m n s of t h e forn ix in to t h e at r iu m an d body of t h e P2P in 60%, 20%, 16%, an d 3% of cases, respect ively.
lateral ven t r icle.31 Th e largest lateral p oster ior ch oroidal ar ter- Th e p osterior h ip pocam p al ar ter y ru n s laterally, an d it gen er-
ies ar ising d irect ly from t h e P2P an astom ose on t h e ch oroid ally bifu rcates an d courses along th e fim briodentate sulcus. It
p lexu s of th e tem p oral h or n an d glom u s of t h e p lexu s in th e su p plies th e u n cu s, an terior p arah ip pocam p al gyru s, h ip pocam -
at r iu m w it h in bran ch es of t h e an ter ior ch oroidal ar ter y an d pu s, den tate gyru s, an d fim bria.30,31,58 Th e tem p oral p ole is u su -
m ed ial posterior ch oroidal ar ter y.30 Th e lateral posterior ch oroid ally supp lied by th e m iddle cerebral ar ter y, but a sm all cerebral
ar ter y irrigates th e cerebral pedun cle, posterior com m issure, PCA bran ch m ay exten d to t h e lateral tem p oral lobe an d an te-
part of th e cr u ra an d body of t h e for n ix, lateral gen icu late body, r iorly to th e tem p oral p ole.30,31 If th e first cor t ical bran ch feeds

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68 I Developm ent, Anatomy, and Physiology of the Central Nervous System

m u ch of th e in ferior tem p oral lobe an d th e h ip pocam p al gyru s, Th e p ar ieto -occip it al ar ter y r u n s in t h e p ar ieto -occip it al
th en t h e bran ch is con sidered to be an an terior tem p oral ar- su lcu s, su p p lying th e p oster ior p arasagit t al, cu n eu s, p recu n eu s,
ter y.30,31 A bran ch of th e h ippocam pal arter y exten ding to th e lateral occip it al gyr u s, an d , rarely, t h e p recen t ral an d su p er ior
tem p oral pole is n oted in 7 to 25% of cases.31,73 p ar iet al lobules.30,31,58 Ar teries w ith a proxim al origin ten d to be
larger and m ore vascularized than arteries from the m idbrain, thal-
Anterior Temporal Artery am us, pulvin ar, an d lateral gen iculate bodies. Th ey ru n th rough
Classically, th e an ter ior tem p oral ar ter y is th e secon d cor t ical th e am bien t cistern m edially to th e PCA58 an d w ith in th e h ippo-
bran ch of t h e PCA, bu t it m ay be t h e first bran ch in t h e absen ce cam p al fissu re as t h ey p ass p oster iorly.30,31 Ar ter ies w it h a
of a h ip p ocam p al ar ter y.30,31 Th is ar ter y, w h ich is n ot alw ays p roxim al origin sen d bran ch es th rough th e ch oroidal fissure in to
presen t , h as an in cid en ce of 84%according to Zeal an d Rh oton .31 the lateral ven tricle an d, occasionally, to the third ventricle in the
It ar ises in t h e p roxim al am bien t cistern from th e P2A from area supplied by th e m edial posterior ch oroidal ar ter y or to th e
64% an d t h e P2P in 20% of cases. It su p p lies t h e an teroin fer ior sp len iu m of th e corpu s callosu m .30,31
su r face of t h e tem p oral lobe, p ar t of t h e tem p oral pole in 6%,
an d reach es t h e m id d le tem p oral fissu re an d gyr u s in 52% of
Calcarine Artery
h em isp h eres.3,31
The calcarine artery is the second term inal branch of the PCA.30,31,58
Middle Temporal Artery It p resen t s as a single t ru n k in 90%30,31 an d as t w o t ru n ks in 10%
As th e sm allest an d least bran ch ed of t h e in ferior tem p oral ar ter- of cases.31 According to Párraga et al,58 th is ar ter y origin ates be-
ies, th e m iddle tem poral ar ter y is p resen t in on ly 38% of h em i- fore it en ters th e calcarin e fissure, specifically from P3 in 64.3%
sph eres. It arises in th e crural an d am bien t cistern s from th e P2A of cases, from th e PCA already in side th e calcarin e fissure in
in 16% an d from th e P2P segm en t in 22% of h em isp h eres an d 27.1%, an d un usu ally from th e parieto-occipital ar ter y. Th e cal-
sup plies th e in ferior tem poral lobe.30,31,54–57 carin e ar ter y origin ates from th e P3 (48% in ciden ce), P2P (42%
in ciden ce), or p arieto-occipit al arter y (10% in ciden ce).30,31 It
Posterior Temporal Artery cou rses th rough th e calcarin e fissu re to reach th e occipit al p ole
Except for th e com m on tem p oral ar ter y, th e p osterior tem poral an d h as bran ch es th at vascularize th e in ferior cun eus an d lingual
ar ter y (96% in cid en ce) is t h e largest t r u n k w it h t h e greatest gyrus.30,31,58
n u m ber of bran ch es. It ar ises from t h e in fer ior or lateral PCA,
specifically from th e P2P segm en t in th e am bien t cistern (86% Splenial Artery
in ciden ce), P2A segm en t in th e cru ral cistern (4% in ciden ce), or
P3 segm en t in th e qu adrigem in al cistern (3% in ciden ce). Tw o Th e PCA or it s bran ch es alw ays give rise to th e splen ial ar ter y
posterior tem p oral ar teries m ay be p resen t in 6 to 20% of h em i- (also called th e posterior pericallosal ar ter y).30,31,58,65 According
sp h eres. Th e p oster ior tem p oral ar ter y r u n s obliqu ely in a p os- to Párraga et al,58 th e origin of th e sp len ial ar ter y is th e p arieto-
terolateral d irect ion tow ard t h e occip it al p ole an d su p p lies th e occipit al ar ter y in 45.7%, P3 in 27.1%, m edial posterior ch oroidal
in ferior tem poral an d occipit al su rfaces, in cluding th e occipit al ar ter y in 14.3%, an d PCA in side th e calcarin e fissure in 2.9% of
pole an d lingu al gyru s.30,31,65 h em isph eres. According to Zeal an d Rh oton ,31 th e origin s are th e
parieto-occipit al arter y in 62%, calcarin e ar ter y in 12%, m edial
posterior ch oroidal ar ter y in 8%, posterior tem poral ar ter y in 6%,
Common Temporal Artery
P2P in 4%, P3 in 4%, an d lateral p osterior ch oroidal arter y in 4%of
Th e com m on tem p oral ar ter y w as n oted in 16% of h em isph eres
h em isph eres. Th e splen ial ar ter y courses upw ard arou n d th e
by Zeal an d Rh oton .31 Th is single PCA bran ch arises from t h e
splen ium an d an teriorly over th e corpus callosum sulcus un t il it
P2P segm en t (10% in ciden ce) or from th e P2A segm en t (6% in ci-
an astom oses w ith th e an terior pericallosal ar ter y (a bran ch of
den ce) an d su p p lies m ost of th e in ferior su rface of th e tem p oral
th e an terior cerebral ar ter y) a few cen t im eters an terior to th e
an d occip ital lobes.
posterior sp len iu m t ip .30,31,58 It su pp lies th e sp len iu m of th e cor-
pu s callosu m .
Parieto-Occipital Artery
As on e of th e t w o term in al bran ch es of th e PCA, th e parieto-
occipit al ar ter y is presen t in 96% of h em isph eres.30,31,58 Accord-
ing to Párraga et al,58 it origin ates from th e PCA before it en ters
■ Conclusion
t h e calcar in e fissu re, from P3 (71.4%) or P2P (1.4%), or from Th e cerebral p osterior circu lat ion arises from both ver tebral ar-
t h e PCA already in sid e th e calcar in e fissu re (27.1% of h em i- teries th at fu se togeth er to form th e basilar arter y, w h ich th en
sp h eres). According to Zeal an d Rh oton ,31 th e arter y origin ates en d s in th e p osterior cerebral ar teries. Along th eir cou rses, t h ese
from P3 in 46%, P2P in 40%, an d P2A in 10% of cases. On average, ar teries give several im por tan t bran ch es th at supply th e brain -
on e parieto- occipit al ar ter y exist s, alth ough t w o are occasion - stem an d cerebral h em isp h eres. In addit ion to th e classic an at-
ally obser ved.30,31,58 om y, m any relevan t an atom ic variat ion s exist .

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ar ter y: a brief over view of it s an atom ical variat ion an d in it ial cou rse. In : S29–S68
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Ar ter y. Paris: Springer; 2011 brain , diagn ost ic st udies, gen eral operat ive tech n iqu es an d path ological

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70 I Developm ent, Anatomy, and Physiology of the Central Nervous System

con siderat ion s of the in t racran ial an eur ysm s. In : Yasargil M, ed. Micro- 60. van der Zw an A, Hillen B. Review of th e variabilit y of th e territories of th e
n eu rosurger y. St ut tgar t , Germ any: Georg Th iem e Verlag; 1984:133–164 m ajor cerebral arteries. Stroke 1991;22:1078–1084
48. Van Overbeeke JJ, Hillen B, Tulleken CA. A com parat ive st udy of th e circle 61. Duret H. Rech erch es an atom iques sur la circu lat ion de l’en ceph ale. Arch
of W illis in fet al an d ad u lt life. Th e con figu rat ion of t h e p oster ior bifu r- Physiol Norm Path ol Deu xiem e Serie 1874:316–353
cat ion of th e posterior com m un icat ing ar ter y. J An at 1991;176:45–54 62. Z lch K. Die Pat h ogen ese von Massen blu t u ng u n d Er w eich u ng u n ter
49. Li Q, Li J, Lv F, Li K, Luo T, Xie P. A m ult idetector CT angiography st udy of beson derer Berucksich t igung klin isch er Gesich t spun kte. Act a Neuroch ir
variat ion s in th e circle of Willis in a Ch in ese p op u lat ion . J Clin Neu rosci Su ppl (Wien ) 1961;7:51–117
2011;18:379–383 63. Steph en s R, St ilvell D. Ar teries an d Vein s of th e Hu m an Brain. Springfield,
50. De Silva KR, Silva R, Am arat unga D, Gun asekera WS, Jayesekera RW. Types IL: Ch arles C. Th om as; 1969
of th e cerebral ar terial circle (circle of Willis) in a Sri Lan kan popu lat ion . 64. Krayen b hl H, Yaşargil M. Cerebral Angiography, 2n d ed. Philadelph ia:
BMC Neurol 2011;11:5 Lippin cot t; 1968
51. Eftekh ar B, Dadm eh r M, Ansari S, Gh odsi M, Nazpar var B, Ket abch i E. Are 65. Margolis M, New ton T, Hoyt W. Gross an d roen tgen ologic an atom y of
th e dist ribu t ion s of variat ion s of circle of Willis differen t in differen t pop - t h e posterior cerebral ar ter y. In : Radiology of Skull Base an d Brain , vol 2,
ulat ion s? Result s of an an atom ical st udy an d review of literat ure. BMC book 2. St . Lou is: Mosby; 1974
Neu rol 2006;6:22 66. Yaşargil M. Micron eurosurger y, vol 2. New York: George Thiem e Verlag;
52. Alp ers BJ, Berr y RG, Pad dison RM. An atom ical st u d ies of t h e circle of 1984
W illis in n orm al brain . AMA Arch Neu rol Psych iat r y 1959;81:409–418 67. Rh oton AL Jr, Saeki N, Perlm ut ter D, Zeal A. Microsurgical an atom y of
53. Riggs HE, Rupp C. Variat ion in form of circle of Willis. Th e relat ion of th e com m on an eur ysm sites. Clin Neurosurg 1979;26:248–306
variat ion s to collateral circulat ion : anatom ic analysis. Arch Neu rol 1963; 68. Fujii K, Lenkey C, Rhoton AL Jr. Microsurgical anatom y of the choroidal ar-
8:8–14 teries: lateral and third ventricles. J Neurosurg 1980;52:165–188
54. Kaplan H, Ford D. Th e Brain Vascular System . Am sterdam /New York: Else- 69. Gallow ay JR, Greit z T. Th e m edial an d lateral ch oroid ar teries. An an atom ic
vier; 1966 an d roen tgen ograph ic st udy. Act a Radiol 1960;53:353–366
55. Jongen JC, Fran ke CL, Ram os LM, Wilm in k JT, van Gijn J. Direct ion of flow 70. Car p en ter MB, Noback CR, Moss ML. Th e an ter ior ch oroidal ar ter y; it s
in posterior com m un icat ing arter y on m agn etic resonan ce angiography in or igin s cou rse, dist ribu t ion , an d variat ion s. AMA Arch Neu rol Psych iat r y
pat ien t s w ith occipit al lobe in farct s. St roke 2004;35:104–108 1954;71:714–722
56. van Raam t AF, Mali W P, van Laar PJ, van der Graaf Y. Th e fet al varian t of 71. Galat ius-Jen sen F, Ringberg V. An astom osis bet w een th e an terior ch oroi-
th e circle of Willis an d it s in flu en ce on th e cerebral collateral circu lat ion . dal ar ter y an d th e posterior cerebral ar ter y dem on st rated by ar teriogra-
Cerebrovasc Dis 2006;22:217–224 phy. Radiology 1963;81:942–944
57. Horikosh i T, Akiyam a I, Yam agat a Z, Sugit a M, Nu kui H. Magn et ic reso- 72. Waddington M. Atlas of Cerebral Angiography w ith An atom ic Correlat ion .
n an ce angiograph ic eviden ce of sex-lin ked variat ion s in th e circle of w illis Boston : Lit tle, Brow n ; 1974
and the occurrence of cerebral aneur ysm s. J Neurosurg 2002;96:697–703 73. Mu ller J, Sh aw L. Ar terial vascu lar izat ion of t h e h u m an h ip p ocam p u s.
58. Párraga RG, Ribas GC, An drade SE, de Oliveira E. Microsurgical an atom y of 1. ext racerebral relat ion sh ips. Arch Neurol 1965;13:45–47
th e p osterior cerebral ar ter y in th ree-d im en sion al im ages. World Neu ro- 74. Beevor C. On t h e d ist r ibu t ion of t h e differen t ar ter ies su p p lying t h e
surg 2011;75:233–257 h um an brain . Ph ilos Tran s R Soc Lon d [Biol]1909;200:1–55
59. Tat u L, Moulin T, Bogousslavsky J, Duvern oy H. Ar terial territories of
th e h u m an brain : cerebral h em isph eres. Neu rology 1998;50:1699–1708

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5 Cranial Venous Anatomy
Mauro A.T. Ferreira

Cerebral vein s, u n like brain ar teries th at ru n freely in th e su b term in ate in th e sph en oparietal sin us or an terior deep tem poral
arach n oid space, are at tach ed to th e pia m ater an d an astom ose vein s; (3) a posterior tem poral (pariet al) diploic vein in th e pari
freely. Th ey p ass th rough cistern s, fissu res, an d sulci. Th ey h ave et al bon es an d th at descen d s to th e p ariet al m astoid angle or
n o valves. Th ey are t h in w alled an d h ave a sm all n u m ber of m astoid foram en ; an d (4) an occipital diploic vein , th e largest ,
m u scle cells. Becau se of exten sive variat ion in an atom y, sacrifice con fin ed to th e occip it al bon es an d op en ing in to occip it al vein s
of any cerebral vein during surgical procedures sh ould be don e or t ran sverse sin us n ear th e con fluen ce of th e sin uses or in to an
cau t iou sly. Several rep or t s h ave d escr ibed n eu rologic dam age occip ital em issar y vein .1
related to a var iet y of ven ou s occlu sion s. In terest ingly, ven ou s
sacrifice or occlu sion m ay cau se dam age in on e p at ien t an d n o
sym ptom s in an oth er. Th ese fin dings p robably reflect th e great Emissary Veins
an atom ic variat ion an d differen t an astom ot ic pat tern s in differ Th ese ch an n els t raverse cran ial ap er t u res an d m ake con n ect ion s
en t in dividu als. bet w een ven ous sin uses an d ext racran ial vein s. Som e are con
Th is ch apter review s t h e su p er ficial an d d eep ven ou s sys st an t an d oth ers m ay be absen t . A m astoid em issar y vein in th e
tem s of th e brain . Th e superficial ven ous system s con n ect vein s m astoid foram en u n ites t h e sigm oid sin u s w it h t h e p oster ior
of th e differen t surfaces of th e brain to th e dural ven ous sin uses. au ricu lar or occipit al vein . W h en th e ret rosigm oid approach is
Th e deep ven ou s system com p rises m ain ly th e in tern al cerebral perform ed, th is vein is often sect ion ed an d bon e w a x is ap plied
vein s an d th e basal vein s (of Rosen th al) th at drain in to th e great to th e m astoid foram en . Care sh ould be t aken to avoid forcing
vein (of Galen ). Several con n ect ion s of th e scalp vein s or m uscu bon e w ax in to th e sigm oid sin us; doing so risks sin us occlusion .
lar ven ou s plexu ses sen d em issar y vein s th rough sku ll foram in a Mortazavi et al2 have recently described the anatom y and surgical
an d em issar y vein s th at t raverse cran ial aper t ures an d m ake im plicat ion s of th e cran ial em issar y vein s. Reis et al3 discu ssed
con n ect ion s bet w een ven ou s sin u ses an d ext racran ial vein s. th e an atom y an d su rgical asp ect s of th e m astoid em issar y vein .
Vein s m ay be obst acles to su rgical ap p roach es like t h e cor A pariet al em issar y vein t raverses th e p ariet al foram en to con
ridors along th e su p er ior sagit t al sin u s, th e pin eal region vein s n ect th e su perior sagit t al sin us w ith th e vein s of th e scalp. Th e
in th e qu adrigem in al cistern , an d th e vein of Labbé w h en th e venous plexus of the hypoglossal canal connects the sigm oid sinus
tem p oral lobe is elevated or ret racted . Again , u n like brain ar ter to th e in tern al jugu lar vein . A posterior con dylar em issar y vein
ies th at can be dissected free an d displaced, cerebral vein s are con n ects th e sigm oid sin u s w ith th e suboccipit al ven ous plexu s,
n ot am en able to aggressive su rgical m an ip u lat ion . For t h e m ost an d it m ay be t h e sou rce of p rofu se bleed ing d u r ing su rger y.
p ar t an d becau se th ey an astom ose freely, sacrifice of a sm all A p lexu s of em issar y vein s con n ect s th e cavern ou s sin u s to th e
n u m ber of su p er ficial vein s is u su ally w ell tolerated . How ever, pter ygoid plexu s via th e foram en ovale (th e so called laterocav
if a vein seem s to be larger th an exp ected in su rger y, care m u st ern ou s sin u s).4 Tw o or th ree sm all vein s t raverse th e foram en
be t aken to p reser ve it or, at least , to sacr ifice as few t r ibu t ar ies lacer u m con n ect in g t h e caver n ou s sin u s w it h t h e p h ar yn geal
as p ossible. vein s an d pter ygoid plexu s.4 A vein in th e em issar y sp h en oid
foram en con n ect s th e sam e vessels. Th e in tern al carot id ven ou s
plexu s p asses th rough th e carot id can al an d con n ects th e cav
ern ou s sin u s w ith th e in tern al jugu lar vein . Th e occipit al sin u s
■ Diploic Veins and Emissary Veins connects w ith variably developed veins around the foram en m ag
n u m (t h e m argin al sin u s) an d t h u s w it h t h e ver tebral ven ou s
Diploic Veins p lexu ses, an alter n at ive ven ou s d rain age w h en t h e jugu lar vein
Th ese vein s occu py ch an n els in th e dip loë of som e cran ial bon es. is blocked or ligated.1 Th e oph th alm ic vein s are poten t ially em is
They are large and have dilatations at irregular intervals. Their thin sar y, becau se t h ey con n ect in t racran ial to ext racran ial vein s.2
w alls are m erely en doth eliu m su pp or ted by elast ic t issu e.1 Th ey Th ese ven ou s con n ect ion s exp lain h ow in fect ion s sp read to th e
com m u n icate w ith m en ingeal vein s, du ral sin u ses, an d p ericra in t racran ial sp ace. Th ey also exp lain w hy inju r y or ligat ion of
n ial vein s. Th e four m ost t ypical cran ial ch an n el are as follow s: on e of th e in tern al jugular vein s m ay be asym ptom at ic: Ven ous
(1) a fron tal diploic vein th at em erges from th e bon e in the su blood is rerouted to alternative outflow channels. The venous con
praorbital foram en to join th e su p raorbit al vein ; (2) an an terior n ectors are also involved in th e process of air em bolism during
tem poral (parietal) diploic vein con fin ed m ain ly to th e fron tal su rger y, esp ecially w h en p at ien t s are p laced in t h e sit t ing or
bon e an d th at pierces th e greater w ing of th e sph en oid bon e to sem isit t ing posit ion .

71

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72 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Superior Sagittal Sinus


■ The Superficial Veins
Th e su p er ficial vein s d rain t h e cor t ical su r faces of t h e h em i Th e su p erior sagit t al sin u s begin s ju st beh in d th e fron t al sin u s
sph eres. Th is system drain s th e superficial on e fifth th ickn ess of an ter iorly an d r u n s p oster iorly, at m id lin e, tow ard t h e in n er oc
th e cerebr u m .5 Th is system collects in to four groups of bridging cip it al p rot u beran ce (Figs. 5.1a an d 5.2a). Th ere, it join s t h e
vein s 6 : a su p er ior sagit t al grou p t h at d rain s in to t h e su p er ior t ran sverse sin us; usually, th e righ t t ran sverse sin us receives th e
sagit t al sin u s, a sp h en oidal grou p t h at d rain s in to t h e sp h en o m ajorit y of th e blood from th e su perior sagit t al sin us (Fig. 5.2b).6
p arietal or in to th e cavern ous sin us, a ten torial group th at con In cross sect ion it is t riangu lar sh ap ed an d receives vein s arising
verges in to th e sin u ses in th e ten toriu m , an d a falcin e grou p th at from th e fron t al p oles, fron t al lobes, an d p ariet al lobes.1 It gradu-
em pt ies in to th e in ferior sagit t al or st raigh t sin u s or in to th eir ally en larges posteriorly.
t ribu taries. Th e su perior sagit tal, sph en oidal, or ten torial grou p At each side of th e sin us, en larged ven ous spaces are fou n d,
m ay drain th e m ajorit y of th e h em isph ere if it s t ribu t aries are th e so called lacu n ae (Fig. 5.1a,c). Th e arach n oid villi cells are
large. Ven ou s sin u ses are ch an n els, drain ing blood from th e brain fou n d predom in an tly in th ese lacun ae. Th e lacun ae are described
an d cran ial bon es an d lying bet w een t w o layers of dura m ater. as absen t in th e fet us an d large in th e elderly. Th ey seldom project
Th e sin u ses are lin ed by en doth eliu m an d h ave n o valves. Th eir in to th e su p er ior sagit t al sin u s.6 Th ese lacu n ae p redom in an tly
w all is devoid of m uscu lar t issu e.1 drain m en ingeal vein s th at accom p any m en ingeal ar teries.

Fig. 5.1a–c (a) Anatom ic preparation showing the left


cerebral hem isphere. The coronal, lam bdoid, and sagit tal
sutures were left in place. The superior sagit tal sinus re
ceives its tributaries, usually below the venous lacunae
(arrows). (b) Venous angiogram, lateral view. The superior
sagittal sinus receives frontal veins. There are usually spaces
bet ween the frontal veins where an anterior interhem i
spheric approach can be developed. (c) Anatom ic speci-
men showing a superior view of the superior sagit tal sinus
with the lacunae, in this case, m ore prom inent in the
middle third of the sinus. (Used with perm ission from Bar
row Neurological Institute.)

b c

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5 Cranial Venous Anatomy 73

Fig. 5.2a,b (a) Magnetic resonance angiogram showing


the venous sinuses. (b) Angiogram , posterior view, show
ing the superior sagit tal sinus draining preferentially into
the right transverse sinus. The straight sinus empties mainly
into the left transverse sinus. (Used with perm ission from
Barrow Neurological Institute.)

Vein s th at drain in to th e superior sagit tal sin u s sh ow differen t an in terh em isph eric approach . Th e literat ure repor t s th at liga
angu lat ion s as th ey join th e sin us. An terior vein s open at alm ost t ion of on e or m ore drain ing vein s in th e an terior th ird of th e
a r igh t angle to t h e su p er ior sagit t al sin u s, w h ereas p oster ior su p erior sagit t al sin u s is u su ally w ell tolerated . Fu r th erm ore, a
vein s are directed obliquely for w ard, again st th e curren t of th e few cen t im eters t ypically sep arate th e bridging vein s, w h ich en
sin u s.5,6 Th is orien t at ion m ay resist th e collap se of th in w alled ables th e app roach to be developed (Fig. 5.1b).
cerebral vein s th at m igh t result from a rise in in t racran ial pres How ever, Sh u car t 7 described t w o m ajor com plicat ion s, on e
su re, but an oth er factor is th e backw ard grow th of th e cerebral from pressu re p laced on a ret ractor over th e su perior sagit t al
h em ispheres an d th e con sequen t displacem en t of vessels during sinus. The other w as caused by inadverten t ligation of a large vein
developm en t .1 More often , th e su p erficial vein s p ass ben eath th e drain ing in to th e su perior sagit tal sin u s, leading to a bifron t al
lacu n ae before act u ally join ing th e sin u s 6 (Fig. 5.1a). Cor t ical ven ou s in farct ion an d in farct ion of th e righ t fron t al lobe, respec
vein s m ay pass directly to th e superior sagit tal sin us, or even join t ively. Yet , Hassan een et al8 reported an im m ediate com plicat ion
th e m en ingeal sin u ses, w h ich em pt y in to th e su p erior sagit t al rate of 50% in 38 pat ien t s un dergoing t u m or resect ion th rough
sin u s. Th ese m en ingeal sin u ses m ay exten d 0.5 to 3.0 cm lateral an an ter ior t ran scallosal ap p roach . Th eir dat a in d icated t h at
to th e sup erior sagit t al sin us. ligat ion of bridgin g vein s affect s ou tcom e. I recall t h e case of a
Th e p osit ion of th e vein s drain ing in to th e su p erior sagit t al bifron tal in farct ion leading to m ajor n eurologic deficit after su
sin u s is im p or tan t w h en p lan n ing su rgical app roach es th rough perior sagit tal sin us ligation (sinus laceration during craniotom y),

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74 I Developm ent, Anatomy, and Physiology of the Central Nervous System

an terior to th e coron al sut ure, to approach a pericallosal an eu callosu m an d en larges as it r u n s p osteriorly to join th e st raigh t
r ysm (unpublish ed data). Occipital in terh em isph eric approach es sin u s. It arises from th e u n ion of vein s from th e adjacen t par ts of
are usually safely developed becau se th ere are n o bridging vein s th e falx, corp u s callosu m , an d cingu late gyru s. Th e largest t ribu
5.0 to 9.0 cm proxim al to th e torcula.6 t aries of t h e in ferior sagit t al sin u s are t h e an terior p ericallosal
Obliterat ion of br idgin g vein s in t h e region arou n d t h e cen vein s. Care sh ould be taken in th e presen ce of an un usu ally large
t ral su lcu s m ay cau se con t ralateral h em ip aresis, m ost p rom i in fer ior sagit t al sin u s, w h ich m ay receive t h e m ajor it y of t h e
n en t in th e low er lim bs, an d it m ay be t ran sien t . Sp on t an eou s vein s d rain in g t h e m ed ial su r face of t h e h em isp h ere, u pw ard
occlu sion of t h ese vein s m ay cau se con t ralateral m otor d eficit , tow ard th e sup erior sagit tal sin u s.6
h eadach e, an d seizu res.6 In con t rast , t w o rep or t s 9,10 d escr ibe
good ou tcom es after sacrifice of on e or t w o bridging vein s at
t h e m id d le t h ird of t h e su p er ior sagit t al sin u s in a p ed iat r ic Tentorial Sinuses
p op u lat ion . St ill ot h er rep or t s claim t h at ligat ion of d rain ing Th ere are t w o con st an t , albeit asym m et rical, grou p s of blood
vein s to t h e m id d le t h ird of t h e su p er ior sagit t al sin u s m ay be ch an n els in t h e ten tor iu m : t h e m ed ial an d lateral ten tor ial si
h ar m fu l.6,11,12 n u ses. Th e m ed ial ten tor ial sin u ses are for m ed by th e conver
gen ce of vein s drain ing th e superior surface of th e cerebellum .
Th e lateral grou p is form ed by th e convergen ce of vein s from th e
Inferior Sagittal Sinus basal an d lateral su r faces of t h e tem p oral an d occip it al lobes
Th e in ferior sagit t al sin u s ru n s in th e in ferior aspect of th e falx (Fig. 5.3a). Kn ow ledge of th is an atom y is im p or t an t becau se th e
(Fig. 5.1b). It origin ates above th e an terior por t ion of th e corpus ten torium is split in surgical approach es such as th e occipital

Fig. 5.3a,b (a) Superior view of the cerebellum showing


the m edial and lateral tentorial sinuses. (b) Superior view
showing the basal vein empt ying into a tentorial sinus and
running toward the torcula. (Used with perm ission from
b Barrow Neurological Institute.)

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5 Cranial Venous Anatomy 75

transtentorial, supracerebellar infratentorial, and presigm oid trans its origin at th e torcu lar h eroph ili, th e t ran sverse sin uses ru n an
ten torial. Th e an teroposterior split t ing of th e ten torium sh ould teriorly an d laterally along th e con cavit y of th e occipit al bon e
be perform ed bet w een th e ten torial sin uses. W h en t ran sverse tow ard th e base of th e pet rous ridge, w h ere it m eets th e superior
sect ion s are p lan n ed , th e split sh ou ld be an terior to th e lateral pet rosal sin u s to becom e th e sigm oid sin u s (Figs. 5.2a an d 5.3a).
ten torial sin uses.13 I h ave fou n d an an atom ic variat ion in a ca It is ad h eren t to t h e occip it al bon e by at t ach m en t s from t h e
daveric specim en w h ere th e righ t basal vein ru n s in side th e ten ten toriu m . Th e righ t t ran sverse sin us is usu ally larger th an th e
torium em pt ying into th e st raigh t sin us (Fig. 5.3b). Th is fin ding left , an d it receives t h e m ajorit y of th e ven ou s blood from th e
is con sisten t w ith Rh oton’s 6 obser vat ion th at if th e posterior seg su p er ior sagit t al sin u s (Fig. 5.2b).6,14 Th e left t ran sverse sin u s
m en t of th e basal vein is absen t , th e m iddle segm en t drain s in to is sm aller an d u su ally receives th e ven ou s ou t flow from t h e
a sin u s in th e ten torial edge. st raigh t sin u s. Th u s, th e righ t t ran sverse, righ t sigm oid, an d righ t
in tern al jugu lar vein drain th e su perficial ven ou s blood of th e
brain , w h ereas th e left t ran sverse, left sigm oid, an d left in tern al
Cavernous Sinus jugular vein drain ven ous blood from th e deep brain st ruct ures
Th e cavern ou s sin u ses rest on both sides of th e sella an d con t ain (st raigh t sin us) (Fig. 5.2b). W h en a m astoidectom y is perform ed,
im por t an t n eurovascular st r u ct u res. Th e in tern al carot id arter y th e ju n ct ion of th e t ran sverse sigm oid to th e su perior pet rosal
(ICA) run s in side th e cavern ous sin us, origin at ing at its exit from sin us becom es eviden t .
t h e p et rou s bon e (at th e level of t h e p et rolin gu al ligam en t) to Th e cor t ical vein s from th e lateral p ar t of th e tem p oral lobe
t h e dist al du ral ring before it becom es in t radu ral. Th e ICA is th e m ay drain directly to th e t ran sverse sin u s or m ay loop u n der th e
m ost m edial st ruct ure in side th e cavern ous sin u s. Th e first divi tem poral lobe to drain to a ten torial sin us before drain ing in to
sion an d p ar t of th e secon d division of th e t rigem in al n er ve, th e t h e t ran sverse sin u s. Th e cor t ical vein s of t h e base of t h e tem
trochlear ner ve, and th e oculom otor n erves run in th e lateral w all p oral an d occipital lobes usually drain to a lateral ten torial sin u s.
of th e cavern ous sin us.14 Th e n eural sh eath exten ding from th ese Even t u ally, lateral tem poral sup erficial, tem porobasal, an d oc
n er ves for m s t h e t r u e lateral w all of t h e caver n ou s sin u s (Fig. cipitobasal vein s join to form th e com plex of Labbé th at usually
5.4a). Th e abd u cen t n er ve r u n s in sid e t h e sin u s w it h ou t being drain s in to th e t ran sverse sigm oid ju nct ion .
par t of its bou n daries.
Am ong these st ruct ures, various venous spaces are found (Fig.
5.4b). Th e ven ou s blood in th e cavern ou s sin u s is con n ected w ith
Superior Petrosal Sinus
its cou n terp ar t both an teriorly an d posteriorly t h rough th e an te Th e su perior p et rosal sin u s lies w ith in th e an terolateral at t ach
rior an d posterior in tercavern ou s sin u s, resp ect ively. An teriorly, m en t of t h e ten tor iu m . It con t in u es p oster iorly an d laterally
each caver n ou s sin u s com m u n icates w it h t h e sp h en op ar iet al from it s jun ct ion w ith th e posterior cavern ous sin us m edially,
sin u s an d op h th alm ic vein s. It s m id d le p or t ion com m u n icates tow ard th e t ran sverse sigm oid sin us laterally. It r u n s along th e
through a lateral exten sion on the inner surface of th e great sphe sup erior aspect of th e pet rou s ridge (Fig. 5.4c). It receives bridg
n oid w ing w ith th e pter ygoid plexus via sm all vein s th at pass ing vein s from th e cerebellu m or brain stem , but n ot from th e
th rough th e foram in a spin osu m an d ovale.1 Posteriorly, th e p os cerebr um .6
terior cavern ous sin us, posterior in tercavern ous sin us, superior
pet rosal sin u s, in ferior p et rosal sin u s, an d basilar ven ou s plexu s
m eet to form a con fluen ce of sin uses. It is alm ost im possible to Sphenoparietal, Sphenobasal, and
delin eate th e bou n daries of any of th ese sin u ses at th e p osterior Sphenopetrosal Sinuses
aspect of the sella (Fig. 5.4c). Various ven ous lakes inside the cav
ernous sin uses are located in different “com partm ents.” W h eth er Th e sp h en op ariet al sin u s is a large m en ingeal ch an n el th at fol
th e cavern ou s sin u ses’ ven ou s arch itect u re is form ed by a vein low s th e m en ingeal ar teries an d th at accom p an ies th e an terior
th at loop s arou n d it self, or w h eth er it is com p osed of m any vein s bran ch of th e m iddle m en ingeal ar ter y above th e level of th e
rem ain s a m at ter of debate. pterion . San Millán Ru íz et al15 p oin ted ou t th at th e sph en op ari
etal sin u s (of Bresch et) correspon ds, in realit y, to th e ar t ificial
com bin at ion of t w o ven ou s st ru ct u res: th e p ariet al por t ion of
Straight Sinus th e an terior bran ch of th e m iddle m en ingeal vein s an d a d u ral
ch an n el located u n der th e sp h en oid lesser w ing. It em pt ies in to
Th e st raigh t sin u s is form ed by th e u n ion of th e in ferior sagit t al th e an terior par t of th e cavern ou s sin u s. Th e sin u s th at cou rses
sin u s an d th e vein of Galen below th e sp len iu m of th e corpu s along th e sph en oid ridge m ay tu rn in feriorly to reach th e floor of
callosu m (Figs. 5.2a, 5.3a, 5.5). It also receives con t ribut ion from th e m idd le cran ial fossa rath er th an em pt ying in to t h e an terior
th e su p erior cerebellar an d basal vein s (Fig. 5.5). From its origin par t of th e cavern ou s sin u s. It m ay join th e pter ygoid plexu s via
an teriorly an d superiorly at th e jun ct ion of th e falx an d ten to em issar y sp h en oid vein s.
riu m , th e st raigh t sin us r u n s dow nw ard an d p osteriorly, drain ing Th e sp h en opariet al sin u s exten ds laterally to exit th e cran iu m
in to th e t ran sverse sin u s, u sually to th e left .6,14 to join th e pter ygoid plexus and sph en oid em issar y vein s, origi
n at ing th e sph en obasal sin us. Th e superficial sylvian vein s m ay
em pt y, m ore often th an n ot , in to th e sph en oparietal sin us. W h en
Transverse Sinus th e sin u s is n ot w ell developed or absen t , th e vein s m ay drain
Th e t ran sverse sin u ses, both left an d righ t , origin ate at th e level in to th e cavern ous sin us or in to th e sp h en obasal sin u s an d, less
of th e in tern al occipital prot uberan ce. A groove on th e in n er sur frequently, into the sphenopet rosal sinus.1 Lv et al4 have described
face of th e occipit al bon e in dicates it s an atom ic posit ion . From detailed an atom y of th e laterocavern ous sin us.

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76 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 5.4a–c The cavernous sinus, lateral view. (a) The


neural sheath extending through cranial nerves (CNs) III,
IV, and V1 and part of V2 form the actual lateral wall of the
cavernous sinus. ICA, internal carotid artery; SCA, superior
cerebellar artery. (b) The cavernous sinus and its contents.
The venous spaces are shown (arrowheads). (c) Posterior
view of the posterior cranial fossa. The venous sinuses
have been dissected on the left side. PICS, posterior in
tercavernous sinus; CS, cavernous sinus; PCS, posterior
cavernous sinus. (Used with permission from Barrow Neu
rological Institute.)

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5 Cranial Venous Anatomy 77
Fig. 5.5a,b (a) Posterolateral view of the quadrigem inal
cistern region showing the vein of Galen empt ying into
the straight sinus. (b) Posterior view of the quadrigem inal
cistern region showing the veins empt ying into the great
vein and then to the straight sinus. The straight sinus
has been displaced superiorly. 1, basal vein of Rosenthal;
2, internal cerebral veins; 3, great vein of Labbé; 4, choroid
vein over choroid plexus. (Used with perm ission from Bar
row Neurological Institute.)

Occipital Sinus su re (Fig. 5.6b). Th is m an euver is u su ally regarded as safe. Non e


th eless, w h en th e sylvian vein is form ed by on e or m ore large
Th is sm allest of th e sin u ses lies in th e at t ach ed m argin of th e falx
ch an n els, it p referen t ially drain s th e adjacen t fron t al, p ariet al,
cerebelli. It is occasion ally paired. It origin ates n ear th e foram en
an d tem poral lobes. Th e in discrim in ate sacrifice of vein s in th is
m agn um th rough several sm all ch an n els an d join s at th e en d of
sit u at ion m ay im p air ven ou s drain age an d cau se sw elling of th e
th e sigm oid sin u s. It con n ect s w ith th e in tern al ver tebral p lex
tem poral lobe.6
u ses an d en ds in th e con fluen ce of th e sin u ses.
W h en th e su p erficial sylvian vein is absen t , th e adjacen t vein s
from th e fron t al an d pariet al lobes ten d to ascen d to join th e
Superficial Sylvian Veins and Superior and vein s th at drain in to th e superior sagit tal sin us. Th e vein s of th e
adjacen t tem p oral lobe ten d to d rain p osteroin fer iorly to join
Inferior Anastomotic Veins t h e vein s en tering th e sin u ses below th e tem p oral lobe. Th e su
Th e su p erficial sylvian vein , or sylvian com p lex, ru n s along th e perior an astom ot ic vein (of Trolard) con n ect s th e su p erficial syl
lateral su lcu s of th e brain , u su ally at tach ed to th e su p erior tem vian vein to th e superior sagit t al sin us (Figs. 5.1a and 5.7). It is
poral gyr u s. It em pt ies in to th e ven ou s sin u ses along th e sp h e u su ally located at t h e level of t h e cen t ral an d p ostcen t ral su lci,
n oid ridge, m ore often th an n ot , in to th e sph en opariet al sin us.6,14 bu t its locat ion m ay var y. It run s superiorly an d receives t ribu
Th e vein m ay be a single vessel, it m ay form a com plex of sup er taries along its course on th e lateral su rface of th e fron topariet al
ficial sylvian vein s, or it m ay be absen t (Fig. 5.6). It receives lobes before drain ing, usu ally as a single vessel, in to th e sup erior
bran ch es from th e fron tal, parietal, an d tem poral lobes. sagit t al sin us. It m ay, h ow ever be duplicated (Fig. 5.7b).
Typically, th ere are bran ch es th at cross th e lateral sulcu s an d Th e in fer ior an astom ot ic vein (of Labbé) con n ect s t h e su
th ey m u st be sacrificed du ring su rger y to op en th e sylvian fis p erficial sylvian vein system to th e t ran sverse sin u s (Fig. 5.8a). It

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78 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 5.6a,b Anatom ic preparations showing the super


ficial veins. (a) The vein of Labbé may be quite prom inent.
(b) Com plex of sylvian veins m ay be present. In this prep
aration they are noted to be crossing over the lateral
sulcus. (Used with perm ission from Barrow Neurological
Institute.)

usually arises from th e m iddle por t ion of th e sylvian fissu re, but tem poral lobe is elevated or ret racted during a surgical proce
it m ay var y.6 It crosses th e su rface of th e tem p oral lobe an d con du re (Fig. 5.8c,d).
t in u es p osteriorly an d in feriorly to join th e t ran sverse sin u s (Fig.
5.8a– c). It u sually drain s in to th e ten torial sin us before reach ing
the tran sverse or tran sverse sigm oid sinus junction , usually in th e
preoccip ital n otch region (Fig. 5.8b). Th e in ferior an astom ot ic ■ Cortical Veins
vein is a single vessel, or it m ay be duplicated (Fig. 5.6b). The vein
of Labbé m ay receive t ributaries th at drain th e lateral par t of th e Th e cor t ical vein s com p rise th e differen t ven ou s system s th at
posterior tem p oral lobe an d th e in ferior su rface of th e tem p oral drain th e th ree surfaces—lateral, m edial, an d basal—of th e brain .
an d occip ital lobes to form th e so called com p lex of Labbé. Th e m ain ven ou s grou p s are d iscu ssed h ere, bu t like brain ar
Occlu sion of th e vein of Labbé m ay cause ven ous in farct ion of ter ies, t h ey can n ot be id en t ified in divid u ally d u r ing su rgical
th e tem p oral lobe, creat ing m ass effect on t h e brain , con t ralat ap p roach es. Alt h ough t h e vein s are m en t ion ed , t h e read er is
eral h em iparesis, aph asia, disorien t at ion , an d death .6 I recall a referred elsew h ere for a th orough review of th e an atom y.16
case of sp on t an eou s th rom bosis of th e vein of Labbé an d su bse
qu en t occlu sion of th e righ t t ran sverse sin u s, requ iring decom
pressive cran iotom y. Another case of tem poral lobe in farction w as
Frontal Lobe
likely related to occlu sion of th e vein of Labbé from p lacem en t of The veins of the frontal lobe are divided into groups that drain the
a self ret ain ing ret ractor un dern eath th e vein during presigm oid lateral, m edial, an d basal su rfaces of th e brain (Figs. 5.1b, 5.7a,
approach to a posterior cavern ou s sin us m en ingiom a (u npub 5.8a,c). Th e lateral fron t al vein s are divided in to ascen ding an d
lished data). Careful surgical planning is m andatory, and the m or descen ding grou p s. Th e ascen ding grou p drain s in to th e su p erior
ph ology an d locat ion of th e vein sh ou ld be est ablish ed w h en th e sagit t al sin u s. Th e descen ding grou p d rain s in to th e su perficial

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5 Cranial Venous Anatomy 79
Fig . 5.7a,b (a) Angiogram , lateral view, showing the
superior anastom otic vein (of Trolard). (b) Magnetic reso-
nance angiogram, lateral view, showing a doubled vein of
Trolard. (Used with perm ission from Barrow Neurological
Institute.)

sylvian vein . Th e ascen ding vein s are th e fron top olar; an terior, th e basal vein of Rosen th al. Th e ascen ding grou p is form ed by
m iddle, an d posterior fron tal; precen t ral; an d cen t ral vein s. Th e the anterom edial, cen trom edial, posterom edial frontal, and para
descen ding grou p is form ed by th e fron tosylvian vein s. Th e as cen t ral vein s. Th e d escen d ing vein s are t h e p er icallosal, p ara
cen ding group is u sually larger th an th e descen ding group. Th e ter m in al, an d an terior cerebral vein s. Th e in ferior fron tal vein s
less developed is the superficial sylvian vein; the ascending group (drain ing th e orbital surface of the frontal lobe) are divided into an
is m ore im por tan t . Ascen ding vein s m ay term in ate in th e supe an terior group th at drain s in to th e an terior par t of th e su perior
rior sagit t al sin u s or join an oth er ascen ding vein before drain ing sagit t al sin u s. Th e p osterior grou p, com p osed of th e olfactor y
in to th e su perior sagit t al sin u s. an d posterior orbitofron tal vein s, drain s in to th e first segm en t of
Th e m edial fron t al lobe h as an in n er grou p of cor t ical ven ou s th e basal vein .5,6
ch an n els an d an ou ter zon e separated by th e cingu late su lcu s.
Th e m edial fron t al vein s are divided in to an ascen d ing grou p
Parietal Lobe
th at drain s in to th e su p erior sagit t al sin u s an d a descen ding
group th at drain s in to th e in ferior sagit t al sin u s or in to th e vein s Th e su perficial vein s of th e p ariet al lobe are divided in to a grou p
aroun d th e corpus callosu m th at drain in to th e an terior en d of th at drain s th e lateral su rface an d an oth er grou p th at drain s th e

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80 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 5.8a–d (a) Anatom ic preparation showing the infe


rior anastom otic vein (of Labbé) arising from the superfi
cial sylvian vein and running toward the transverse sinus.
(b) The lateral skull base has been dissected, and the tem
poral lobe has been elevated to show the tributaries of the
complex of Labbé empt ying into a tentorial sinus before
joining the transverse sigm oid junction. (c) Angiogram
showing a prom inent vein of Labbé.

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5 Cranial Venous Anatomy 81
Fig. 5.8a–d (continued ) (d) The temporal lobe has been
elevated as in a presigm oid transtentorial approach, and
the tributaries to the vein of Labbé are shown draining
into a lateral tentorial sinus. A self retaining retractor in
place, after inspection for the absence of important veins.
CN, cranial nerve; ICA, internal carotid artery. (Used with
perm ission from Barrow Neurological Institute.)

m edial surface. Th e lateral grou p is fu rth er divided in to ascen d sph eric approach is a safe surgical route becau se n o bridging
ing vein s th at drain in to th e su p erior sagit t al sin u s an d descen d vein s are presen t 4 to 9 cm proxim al to th e torcula along th e
ing vein s t h at drain in to th e sup erficial sylvian vein (Figs. 5.1b, m idlin e.6 Th e m ed ial su rface of t h e occipit al lobe is drain ed by
5.7a, 5.8a,c). Th e ascen ding vein s are th e cen t ral an d postcen t ral th e an terior (also called th e m edial occipit al vein ) an d p osterior
vein s an d th e an terior an d posterior parietal vein s. Th e descen d calcarine veins. Occlusion of the anterior calcarine vein m ay cause
ing group is form ed by th e parietosylvian vein s. Th e m edial pari h om onym ous h em ian opsia. Th e posterior par t of th e calcarin e
et al vein s are also divided in to ascen ding an d descen ding groups. fissure (prim ar y visual cortex) is drain ed by th e posterior calca
Th e ascen ding vein s are th e p aracen t ral, an terom edial, an d an rin e vein . Th e in ferior su rface of th e occip it al lobe is drain ed by
teroposterior veins that drain into the superior sagit tal sinus. The t h e occip itobasal vein . It or igin ates from t r ibu t ar ies t h at d rain
descen ding vein s are th e p osterior p ericallosal vein s th at cou rse t h e in ferolateral p ar t of t h e lin gu al gyr u s an d th e adjacen t p ar t
aroun d th e splen ium of th e corpus callosum to em pt y in to th e of th e occip itotem poral an d in ferior tem p oral gyri. It cou rses in
vein of Galen or its t ribu taries. ferolaterally tow ard th e preoccipital n otch an d frequen tly join s
th e p osterior tem p orobasal vein before em pt ying in to th e lateral
ten torial sin us.
Temporal Lobe
Th e cor t ical vein s of th e tem p oral lobe are also divided in to a
lateral grou p th at drain s th e lateral su rface of th e h em isp h ere
an d an in ferior group th at drain s th e base of th e tem poral lobe ■ Deep Cerebral Veins
(Figs. 5.1b, 5.7a, 5.8a,c). Th e lateral grou p is fu r th er divided in to Th e d eep cerebral ven ou s system drain s th e deep w h ite m at ter
an ascen ding group (th e tem porosylvian group) th at em pt ies an d gray m at ter surroun ding th e lateral an d th ird ven t ricles as
in to t h e su p er ficial sylvian vein an d in to a d escen d ing grou p w ell as th e basal cistern s. It is cen tered aroun d th e vein of Galen
(an terior, m iddle, an d posterior sylvian vein s) th at drain in to th e an d h as t w o m ajor t ributaries: th e paired in tern al cerebral vein s
ven ou s sin uses below th e tem poral lobe. Th e in ferior tem poral an d t h e basal vein of Rosen t h al.6,14 Th e d eep ven ou s system is
vein s are divided in to a lateral grou p, w h ich drain s in to th e si respon sible for th e ou tflow of th e in n er fou r fifth s of th e cere
n uses in th e an terolateral par t of th e ten toriu m (th e an terior, bral h em isph ere.5
m iddle, an d posterior tem porobasal vein s), an d a m edial group Th e deep ven ou s system is divided in to ven t ricu lar vein s an d
th at em pt ies in to th e basal vein as it cou rses arou n d th e u p per cistern al vein s.6 Th e th alam us is drain ed by both ven t ricular an d
brain stem , below th e opt ic t racts, an d n ear th e st ru ct ures of th e cistern al vein s. Th e ven t ricular vein s drain th e basal ganglia,
m edial tem poral lobe (th e un cal, an terior h ippocam pal, an d m e thalam us, internal capsule, corpus callosum , sept um pellucidum ,
dial tem poral vein s). Th e base of th e tem p oral pole is drain ed by forn ix, an d deep gray m at ter. Th e cistern al vein s drain st ruct ures
th e tem porosylvian vein s. adjacen t to th e th ree an atom ic region s related to th e an terior,
m iddle, an d posterior cistern al region s an d th e so called an te
rior, m iddle, an d posterior in cisu ral sp aces.
Occipital Lobe
Th ree grou p s of cor t ical vein s drain th e lateral, basal, an d m edial
Cisternal Group
su r faces of t h e occip it al lobe. Th e vein s d rain ing t h e p oster ior
p ar t of t h e tem p oral an d p ar iet al lobes m ay d rain t h e an ter ior Th e cistern al grou p of deep vein s drain s th e area begin n ing an te
p ar t of t h e occip it al lobe in th e lateral su r face. Becau se t h ese riorly, in fron t of th e th ird ven t ricle, an d exten ding laterally in to
drain ing vein s are directed an teriorly an d n ot posteriorly tow ard t h e sylvian fissu re an d p oster iorly to in clu d e t h e w alls of t h e
th e su perior sagit t al sin u s, th e occipit al (or p osterior) in terh em i ch iasm at ic, in terp edu n cu lar, cr u ral, am bien t , an d qu adrigem in al

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82 I Developm ent, Anatomy, and Physiology of the Central Nervous System

cistern s. Th e vein s drain ing an teriorly to th e qu adrigem in al cis it join s th e oth er in sular vein s (Fig. 5.9b). It ru n s p osteriorly to
tern em pt y in to th e basal vein , an d th ose of th e region of th e term in ate w h ere th e pedun cular vein join s th e basal vein at th e
qu adrigem in al cistern drain in to th e basal, in tern al cerebral, or an terolateral p ar t of t h e cerebral p ed u n cle. Th e vein p roceeds
great vein . p oster iorly in th e m id d le in cisu ral sp ace bet w een t h e lateral
Th e basal vein is form ed in th e an terior in cisu ral space by th e brain stem an d m edial tem poral lobe. Its m ain t ributar y is th e
un ion of th e deep m iddle cerebral an d an terior cerebral vein s, in ferior ven t ricu lar vein , w h ich drain s th e tem poral h orn of th e
in ferior st riate vein s (exit ing th e an terior p erforated su bst an ce), ven t ricle, an d vein s drain ing th e m edial surface of th e tem poral
fron to orbit al, an d olfactor y vein s (Fig. 5.9a). Th e deep m iddle lobe (u n cu s, h ip pocam p u s). At th e am bien t cistern th e lateral
cerebral vein begin s as a vein in th e cen t ral sulcus of th e in sula m esen ceph alic vein is th e m ajor t ribut ar y to th e basal vein , an
and runs anteriorly and inferiorly tow ard the lim en insulae, w here im port an t surgical lan dm ark th at in dicates th e p osterior por t ion

Fig. 5.9a,b (a) Lateral view of a cadaveric specimen


showing the insular veins joining to form the deep m iddle
temporal vein. The frontotemporal opercula have been
rem oved. (b) Inferior surface of the brain showing the
position and tributaries to the basal vein. 1, deep m iddle
tem poral vein; 2, posterior frontobasal vein; 3, anterior
cerebral vein; 4, anterior perforated veins; 5, olfactory
vein; 6, basal vein, anterior segm ent; 7, anterior peduncu
lar vein; 8, second segm ent, basal vein; 9, lateral m esen
cephalic vein; 10, third segm ent, basal vein; 11, anterior
calcarine vein; 12, superior vermian vein; 13, proxim al
great vein; 14, superior ventricular vein. (Used with per
m ission from Barrow Neurological Institute.)

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5 Cranial Venous Anatomy 83

of the cerebral peduncles. The posterior incisural space is situated lateral ven t ricles. Th ese cavit ies are posit ion ed aroun d t h e th ala
posterior to th e m idbrain an d corresp on ds to th e p in eal region . m us in a C sh aped fash ion (Fig. 5.10). Th ese cavit ies h ave a roof,
Th e p osterior segm en t of th e basal vein begin s at th e posterior floor, an d lateral an d m edial w alls. Th e fron t al h orn an d at rium
m argin of th e am bien t cistern , w h ere th e vein run s tow ard th e also h ave an an terior w all. Th e ch oroid plexu s r un s parallel to
posterior m argin of th e m idbrain to reach th e qu adrigem in al cis th e forn ix an d exten ds in ferolaterally from th e in ferior ch oroid
tern , an d it en ds in th e in tern al cerebral or great vein . poin t to th e foram en of Mon ro. Th e ch oroid p lexu s rests over a
cleft bet w een th e forn ix an d th alam u s, th e so called ch oroidal
fissu re (Fig. 5.10b).
Ventricular Group Ventricular veins are disposed into a lateral and a m edial group
Th e su praten torial ven t ricu lar system h as five differen t cavit ies: w h eth er th ey drain th e th alam ic side or th e forn ical side of th e
t h e fron t al, body, at r iu m , occip it al, an d tem p oral h or n s of t h e ch oroid fissu re (Fig. 5.11a). Both grou ps ru n along th e w alls of

Fig. 5.10a,b Ventricular system as seen from


above. (a,b) Divisions of the ventricular system
and the ventricular veins. (Used with perm is
b sion from Barrow Neurological Institute.)

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84 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 5.11a–d (a) Ventricular system , superior view (ver


tebral artery, venous angle). (b) Form ation on the internal
cerebral vein, superior view. The columns of the fornix
have been cut and displaced posteriorly. (c) Lateral view of
the velum interpositum and anatom ic display of the inter
nal cerebral vein empt ying into the vein of Galen.

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5 Cranial Venous Anatomy 85

Fig. 5.11a–d (continued ) (d) Transchoroidal dissection.


The fornix has been displaced m edially without sacrificing
any tributaries to the internal cerebral veins. CN, cranial
nerve. (Used with perm ission from Barrow Neurological
Institute.)

th e ven t ricle in a su bep en dym al locat ion tow ard th e ch oroidal form ed on th e th alam ic side, sacrifice of th e vein s in th e lateral
fissure. The lateral group drains the lateral w alls and passes along w all of th e fron t al h orn an d body of th e ven t ricle as w ell as th e
th e in n er th alam ic side of th e ven t ricle. Th ey p ass th rough th e t h alam ost r iate an d t h alam ocau date vein s is in evit able w it h
th alam ic sid e of t h e ch oroidal fissu re in a su bepen dym al loca p ossible clin ical con sequen ces. Th e m icrosurgical an atom y of
t ion to em pt y in to th e in tern al cerebral, basal, an d great vein s. th e t ran sch oroidal app roach is elegan tly p resen ted by Wen at
Th e m edial grou p drain s th e m edial w all an d roof of th e fron al.18 Inju r y to th e in tern al cerebral vein s is described as cau sing
tal h orn , body, at riu m , occip ital h orn , an d floor of th e tem poral sym ptom s su ch as dien ceph alic ed em a, m en tal sym ptom s, com a,
h orn . After reach ing th e m edial par t of th e ven t ricle n ear th e hyperpyrexia, tachycardia, tachypnea, m iosis, rigidit y of the lim bs,
ch oroid fissu re, th e vein s in th e m edial grou p exit th e ven t ricle an d exaggerat ion of deep ten don reflexes.6
by piercing th e forn ix to join th e in tern al, basal, or great vein . In terest ingly, th e term thalam ost riate vein im p lies a relat ion
Th e su perior an d in ferior ch oroidal vein s are th e m ost con sisten t sh ip bet w een t h is vein an d t h e t h alam u s. Alt h ough t h e vein s
vein s in th e ch oroid p lexu s. cou rse alon g t h e lateral m argin of t h e t h alam u s, it is join ed by
n on e of th e th alam ic vein s.
Th e deep th alam ic vein s are categorized as an terior, su perior,
Internal Cerebral Veins in ferior, an d posterior. Th e an terior th alam ic vein drain s th e an
Th e paired in tern al cerebral vein s origin ate ju st beh in d th e fora terior por t ion of th e th alam us an d em pt ies in th e region of th e
m en of Mon ro an d r u n p oster iorly en d in g ju st su p erolaterally foram en of Mon ro. Th e su p er ior t h alam ic vein is t h e largest of
to th e pin eal body to em pt y in to th e great vein (Fig. 5.11a). Th e t h e t h alam ic vein s. It ar ises in t h e cen t ral su p er ior p ar t of th e
in tern al cerebral vein s ru n in side th e velu m in terp osit um in th e t h alam u s, r u n s p oster iorly an d u n d er n eat h th e velu m in ter
roof of th e th ird ven t ricle (Fig. 5.11b). In side th e velu m in ter p osit um , an d em pt ies in to th e in tern al cerebral or great vein .
p osit u m , t h e vein s lie bet w een t h e for n ix su p er iorly an d t h e Th e in ferior th alam ic vein s arise from th e an teroin ferior p ar t of
ch oroid plexus of th e th ird ven t ricle in feriorly (Fig. 5.11c). Th eir th e th alam u s an d t raverse th e p osterior perforated su bst an ce to
an terior par t is form ed by th e con fluen ce of th e an terior septal drain in to th e p osterior com m u n icat ing or p edu n cu lar vein . Th e
vein w ith th e th alam ost riate vein (Fig. 5.11a). Th ey receive sev p oster ior t h alam ic vein s d rain t h e p oster ior in ferolateral p or
eral t r ibu t ar ies of adjacen t st r u ct u res. Th e vein s from t h e fron t ion of th e th alam u s an d em pt y in to th e posterior par t of th e
t al h orn , body, an d par t of th e at riu m of th e lateral ven t ricle en d basal or in to th e vein s follow ing th e posterolateral su rface of th e
in t h e in ter n al cerebral vein s as t h ey r u n t h rough t h e velu m m idbrain .
in terp osit um .
Sect ion ing th e th alam ost riate vein to en h an ce th e posterior
exp osu re of t h e t h ird ven t r icle t h rough t h e foram en of Mon ro
Vein of Galen
m ay cau se n eu rologic com p licat ion s su ch as d row sin ess, m u t Th e vein of Galen is located in th e p osterior in cisu ral sp ace (th e
ism , h em ip legia, an d ven ou s in farct ion of t h e basal ganglia.17 qu adrigem in al cistern ) an d relates to th e p in eal body. It is a sh or t
Dissect ion of th e ch oroidal fissu re m ay be useful to reach deep an d large ven ous ch an n el located at th e in ferior an d posterior
seated lesion s in th e th ird ven t ricle; p in eal region ; an d cru ral, aspect of th e splen ium of th e corpus callosum , from w h ere it
am bien t , an d quadrigem in al cistern s. Th e dissect ion sh ould al rises to em pt y in to th e st raigh t sin u s at th e ten torial apex. It is
w ays p roceed by op en ing th e forn ical side of th e fissu re, w ith ou t form ed by th e jun ct ion of th e in tern al cerebral vein s, basal vein s,
th e n eed to sacrifice any vein s (Fig. 5.11d). If dissect ion is per m edial occipital (an terior calcarin e) vein s, an d superior verm ian

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86 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 5.12 Pineal region veins, inferior view. 1, basal veins;


2, internal cerebral veins; 3, great vein; 4, anterior calca
rine vein; 5, superior verm ian vein displaced posteriorly;
6, straight sinus; 7, inferior thalamic vein; 8, internal cerebral
veins. (Used with perm ission from Barrow Neurological
Institute.)

vein s. It receives several sm all t r ibu t ar ies from th e adjacen t poten t ials or t rigem in al evoked p oten t ials in 8.6% of p at ien t s
st r u ct u res in th e pin eal body region (Fig. 5.12). Th ese vein s h ave w h en th e vein w as tem porarily occluded. The m ost com m on com
im por t an t clin ical sign ifican ce because ap p roach es directed to plicat ion is congest ion of th e cerebellu m an d brain stem . Usually,
th e p in eal region m ay requ ire sacrifice of on e or m ore vein s in on e or m ore t ributaries of th e vein m ay be ligated w ith ou t th e
th is region . It is believed th at occlu sion of th e great vein is n ot n eed to sacrifice it s m ain t ru n k.
w ell tolerated.6 Variou s repor t s h ave described th e m an agem en t Th e ten tor ial (or p oster ior) grou p d rain s in to t h e ten tor ial
of deep seated lesion s in th is area 19–21 as w ell as it s det ailed m i sin uses n ear th e torcula an d in cludes th e in ferior verm ian vein
crosu rgical an atom y.22 How ever, on e case rep or t described liga an d its superior an d in ferior ret roton sillar t ribu taries an d th e
t ion of th e great vein w ith ou t clin ical con sequ en ces.23 su p erior an d in ferior h em isp h eric vein s (Fig. 5.13c). Th e su p e-
rior (or galen ic) grou p drain s in to th e great vein an d in clu des th e
m esen ceph alic t ribut aries (th e m edian an terior pon tom esen ce
p h alic vein , lateral p on tom esen cep h alic vein , lateral m esen ce
■ Posterior Fossa Veins ph alic, p edu n cu lar, p osterior m esen cep h alic, an d tect al vein s),
an d th e cerebellar t ributaries (th e precen t ral cerebellar vein an d
Th e p oster ior fossa ven ou s system can be d ivid ed in to t h ree
its varian ts an d th e su perior verm ian vein ).
grou p s. Th e an terior (or pet rosal) grou p d rain s in to th e su perior
Th e p et rosal grou p m ay be categorized as follow s: (1) vein s
an d in ferior pet rosal sin u ses. Th e superior (or galen ic) group
related to t h e an ter ior asp ect of t h e brain stem ; (2) vein s in t h e
drain s in to th e vein of Galen . Th e p osterior (or ten torial) grou p
w ing of t h e p recen t ral cerebellar fissu re; (3) vein s in th e su p e
drain s in to th e sin u ses n ear th e torcu la. Th e vein s ten d to d rain
r ior an d in ferior su rfaces of th e cerebellar h em isp h eres (su perior
in to th e n earest drain ing system . Th e p osterior fossa vein s sh ow
an d in ferior h em isph eric vein s, in cluding th e vein s of th e great
n um erous an astom oses. Th e vein s of th e pet rosal su rface of th e
h orizon t al fissure); (4) vein s on th e cerebellar side (th e m edial
cerebellum and the anterior surface of the brainstem tend to drain
ton sillar vein) an d m edullary side (th e retro olivary vein an d vein
in to th e pet rosal sin u ses via th e su p erior p et rosal vein , except for
of th e in ferior cerebellar p edu n cle of th e cerebellom edullar y fis
th e vein s r u n n ing on th e su rface of t h e m idbrain th at drain in to
su re; an d (5) vein of t h e lateral recess of t h e fou r t h ven t r icle.
th e galen ic system . Th e su p erior pet rosal vein is form ed by th e
Mat su sh im a et al27 p rovided det ailed m icrosu rgical an atom y of
jun ct ion of th e t ran sverse pon t in e an d pon tot rigem in al vein s
th e p osterior fossa vein s.
an d th e vein of th e cerebellopon t in e fissure (Fig. 5.13b). Th e su-
perior pet rosal vein is frequ en tly exp osed in lateral su boccip ital
approach es, par t icularly in procedures directed to th e upper cer
ebellopon t in e angle an d p et rou s apex.
Su rgical occlu sion of th is vein is u su ally regarded as h arm less.
■ Conclusion
Th e rerou t ing of th e ven ou s ou t flow cou ld be est ablish ed ac Th orough kn ow ledge of th e cerebral vein s is n ecessar y to avoid
cording to an an atom ic st u dy.24 How ever, Koerbel et al25 fou n d surgical com plicat ion s. Unexpected neurologic deficits after a suc
com p licat ion s related to sect ion ing th e pet rosal vein in n in e of cessfu l op erat ion m ay be related to ven ou s d rain age p roblem s.
30 pat ien t s operated on for m en ingiom as of th e pet rous apex. Th e ven ou s system var ies m ore often t h an ar ter ies d o, so w h en
Zh ong et al26 also fou n d abn orm al brain stem auditor y evoked ever ven ou s m an ip u lat ion is an t icip ated , p reviou s kn ow ledge

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5 Cranial Venous Anatomy 87
Fig . 5.13a–c Posterior fossa veins. (a) Suboccipit al
view. (b) Anterior view of the veins of the brainstem and
cerebellum showing the num erous venous anastom oses.
(c) Formation of the superior petrosal vein. (Used with per
mission from Barrow Neurological Institute.)

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88 I Developm ent, Anatomy, and Physiology of the Central Nervous System

of th e p at ien t ’s p ar t icu lar ven ou s system p at ter n is m an dator y. rificed, w h ile others rem ain asym ptom at ic postoperatively. Thus,
If a vein is dam aged du ring su rger y, its repair is far m ore difficu lt ever y effor t to keep as m any vein s as p ossible w h en p er for m
to perform w h en com p ared w ith ar teries. In terest ingly, som e in g a su rgical ap p roach or rem oving a su rgical lesion is h igh ly
pat ien ts develop n eu rosu rgical deficits if a p ar t icu lar vein is sac advised.

References
1. William s PL, Ban n ister LH, Berr y MM. Cran ial an d int racran ial vein s. In : 14. Casecki AP, Barn et t HJM. Ven ous an atom y. In: Car ter LP, Spet zler RF, eds.
Gray’s An atom y, 38th ed. New York: Ch urch ill Livingston e; 1996:1580– Neurovascular Surger y, 1st ed. New York: McGraw Hill; 1995:35–64
1589 15. San Millán Ruíz D, Fasel JH, Rü fen ach t DA, Gailloud P. Th e sph en opariet al
2. Mor t azavi MM, Tu bbs RS, Riech S, et al. An atom y and path ology of th e sin us of bresch et: does it exist? An an atom ic st u dy. AJNR Am J Neurora
cran ial em issar y vein s: a review w ith surgical im plicat ions. Neurosurger y diol 2004;25:112–120
2012;70:1312–1318, discussion 1318–1319 16. Oka K, Rh oton AL Jr, Barr y M, Rodriguez R. Microsurgical an atom y of th e
3. Reis CV, Desh m u kh V, Zabram ski JM, et al. An atom y of th e m astoid em is superficial veins of the cerebrum . Neurosurger y 1985;17:711–748
sar y vein an d ven ous system of the posterior neck region : n eurosurgical 17. Hirsch JF, Zou aou i A, Ren ier D, Pier re Kah n A. A n ew su rgical ap p roach
im p licat ion s. Neu rosu rger y 2007;61(5, Su p p l 2):193–200, d iscu ssion to th e th ird ven t ricle w ith in terr upt ion of th e st rioth alam ic vein . Act a
200–201 Neuroch ir (Wien ) 1979;47:135–147
4. Lv X, Jiang C, Li Y, Liu L, Liu J, Wu Z. The laterocavern ous sin us system : 18. Wen HT, Rh oton AL Jr, de Oliveira E. Transch oroidal approach to the
ven ou s in flow s, ven ous ou tflow s, an d clinical sign ifican ce. World Neuro th ird ven t ricle: an an atom ic st udy of th e ch oroidal fissure an d it s clin ical
surg 2011;75:90–93, discussion 34–35 ap p licat ion . Neu rosu rger y 1998;42:1205–1217, discu ssion 1217–1219
5. Wen HT, Mussi ACM. Surgical an atom y of the brain . In : Win n HR, You 19. Ku n icki A. Operat ive exp erien ces in 8 cases of pin eal t u m or. J Neu rosu rg
m an s JR, eds. Youm an s Neurological Surger y, 5th ed. Ph iladelph ia: Saun 1960;17:815–823
ders; 2004:5–44 20. Stern W E, Bat zdorf U, Rich JR. Ch allenges of surgical excision of t um ors in
6. Rhoton AL Jr. The supratentorial arteries. Neurosurger y 2002;51(4, Suppl): th e p in eal region . Bu ll Los Angeles Neu rol Soc 1971;36:105–118
S53–S120 21. Suzuki J, Iw abuchi T. Su rgical rem oval of pin eal t um ors (pin ealom as an d
7. Sh ucar t W. Th e an terior t ran scallosal an d t ran scor t ical approaches. In : teratom as). Experien ce in a series of 19 cases. J Neurosurg 1965;23:565–
Apuzzo M, ed. Surger y of th e Th ird Ven t ricle, 2n d ed. Balt im ore: William s 571
& Wilkin s; 1998:369–389 22. Ch ayn es P. Microsurgical an atom y of th e great cerebral vein of Galen an d
8. Hassan een W, Suki D, Salaskar AL, et al. Im m ediate m orbidit y an d m or t al it s t ribut aries. J Neu rosurg 2003;99:1028–1038
it y associated w ith t ranscallosal resect ion of t um ors of th e th ird ven t ricle. 23. Youssef AS, Dow n es AE, Agazzi S, Van Loveren HR. Life w ith out the vein of
J Clin Neu rosci 2010;17:830–836 Galen : Clin ical an d radiograph ic sequelae. Clin An at 2011;24:776–785
9. McNat t SA, Sosa IJ, Krieger MD, McCom b JG. In ciden ce of ven ou s infarc 24. Ebn er FH, Roser F, Sh iozaw a T, et al. Pet rosal vein occlusion in cerebello
t ion after sacrificin g m id d le t h ird su p erior sagit t al sin u s cor t ical br idg pont in e angle t um our surger y: an an atom ical st u dy of altern at ive drain
ing vein s in a pediat ric populat ion . J Neu rosurg Pediat r 2011;7:224–228 ing path w ays. Eur J Surg On col 2009;35:552–556
10. Ar yan HE, Ozgu r BM, Jan dial R, Levy ML. Com plicat ion s of in terhem i 25. Koerbel A, Gh arabagh i A, Safavi Abbasi S, et al. Ven ous com plicat ion s fol
sp h eric t ran scallosal ap p roach in ch ildren : review of 15 years experien ce. low ing pet rosal vein sect ion ing in surger y of pet rous apex m en ingiom as.
Clin Neu rol Neurosurg 2006;108:790–793 Eu r J Surg On col 2009;35:773–779
11. Kalberg RM. Cerebral ven ous th rom bosis. In : Kapp JD, ed. Th e Cerebral 26. Zhong J, Li ST, Xu SQ, Wan L, Wang X. Man agem en t of pet rosal vein s dur
Ven ous System an d It s Disorders. Orlan do: Gru ne & St rat ton ; 1984:505– in g m icrovascu lar d ecom p ression for t r igem in al n eu ralgia. Neu rol Res
536 2008;30:697–700
12. Krayen bü h l HA. Cerebral ven ou s an d sin us th rom bosis. Clin Neurosu rg 27. Mat sush im a T, Rh oton AL Jr, de Oliveira E, Peace D. Microsurgical an atom y
1966;14:1–24 of the vein s of th e posterior fossa. J Neurosurg 1983;59:63–105
13. Lust ig LR, Jackler RK. Th e vuln erabilit y of th e vein of Labbé during com
bin ed cran iotom ies of th e m iddle an d p osterior fossae. Skull Base Su rg
1998;8:1–9

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6 Spinal Vascular Anatomy
Peter Kim Nelson and Mak sim Shapiro

Th is ch apter su m m arizes th e con tem p orar y an atom ic an d p hysi- ■ Developmental Aspects: The Grid-Like
ological u n derst an ding of th e ver tebrosp in al vascu lar an atom y. Pattern of the Vertebrospinal
We em ph asize t h e p ract ical clin ical im p licat ion s of both n at ive
an d path ophysiological disposit ion s of th e spin al vascular an at- Arterial Arrangement
om y, becau se u n d erst an d in g t h ese issu es w ill facilit ate t h e
Th e adu lt ap pearan ce of th e spin al ar terial supply, w ith all its
p lan n ing an d perform an ce of opt im al diagn ost ic an d th erapeu t ic
an atom ic variat ion s, is determ in ed in th e first several w eeks of
procedu res. A special em p h asis also is placed on th e ven ous sys-
develop m en t as on e facet of th e body’s overall som atotop ic orga-
tem an d its role in th e p ath op hysiology of ar terioven ous sh un ts.
n izat ion , w h ich con cept u ally can be view ed as recapit ulat ing a
phylogen et ic blu eprin t of m u lt icellu lar organ ogen esis, from th e
w orm to th e h u m an . Th e h u m an em br yo is su bd ivided in to 31
som ites, each corresponding to a developing m etam eric segm ent,
■ Historical Perspective t h at u lt im ately gives r ise to all en d o -, ecto -, an d m esod er m al
Our kn ow ledge of spin al vascular an atom y is based on a rela- d erivat ives. Each som ite is supplied by paired segm en t al ar teries
t ively com p act body of w ork; alth ough it is n ot p ossible to list all origin at ing from th e dorsal aor tae. Th us, from th e stan dpoin t of
sem in al con t ribu t ion s, th e follow ing m ileston es are p rovided as cran iocaudal n om en clat ure, th e early vascular n et w ork con sists
bot h t ribu te an d referen ce. Gross an atom ic invest igat ion s by of m u lt ip le t ran sversely or ien ted vessels (segm en t al ar ter ies)
Alber t Adam kiew icz 1,2 in th e 1870s led to th e descript ion of th e join ed by a longit udin al vascular con n ector (aor ta). Progressive
ar ter y th at n ow bears h is n am e. In 1889, Hein rich Kadyi3 pub - grow th of th e em br yo is accom p an ied by develop m en t of longi-
lish ed a su p erbly accu rate an d in sigh tfu l m an u script on th e ar te- t u d in al an astom ot ic ch an n els t h at cross-br idge t h e t ran sverse
rial an d ven ou s ver tebrosp in al an atom y; m ost of h is cen t u r y-old segm en t al n et w ork. Persisten ce of t h is r u d im en t ar y gr id -like
con clu sion s h ave stood th e test of evolving tech n iqu e. Follow ing array is recogn ized in th e adult vascular arrangem en t of th e en -
th e developm en t of pract ical in vivo sp in al angiograp hy, im por- t ire ver tebrosp in al a xis (Fig. 6.1). Th is organ izat ion is perh aps
tan t con t ribut ion s w ere m ade in 1960s an d 1970s by Doppm an , m ost easily iden t ified in th e low er th oracic an d upper lum bar
Djin djian , an d Lazorth es,4–9 am ong oth ers, providing part icular levels, w h ere each segm en tal ar ter y p ar t icip ates in su pp ly of its
in sigh t in to spin al vein s and th eir role in th e path ogen esis of corresponding osseous, m uscular, and neural/radicular elem ents,
w h at is n ow kn ow n as th e spin al dural ar terioven ou s (AV) fis- fu r th er giving rise, in th e th oracic spin e, to th e in tercostal ar ter y
t u la. Ar m in Th ron et al’s 10 p u blicat ion of Vascular Anatom y of th at m ost app aren tly retain s its segm en t al organ izat ion . Succes-
the Spinal Cord in 1988 su m m arized a lifet im e of obser vat ion s sive transversely orien ted segm ental arteries anastom ose th rough
in to th e an atom y an d path ophysiology of th e sp in al vascu lat ure. several p araspin al vessels longit u din ally arranged along th e axis
Sh or tly before, th e lan dm ark first edit ion of th e Surgical Neu- of th e spin e. Th ese longit udin al ch an n els in clude th e prever te-
roangiography series by Lasjau n ias an d Beren stein ,11 w ith m any bral ar ter y sit uated adjacen t to th e an terolateral aspect of th e
referen ces to Th ron’s w ork, cr ystallized ou r p resen t-day u n der- ver tebral body, t h e p ret ran sverse an astom oses an ter ior to t h e
st an ding of spin al vascu lar an atom y (volu m e 3) an d th e role of t ran sverse p rocess, as w ell as th e p ost t ran sverse sp in al an asto-
en dovascu lar t reat m en t (volu m e 5) in th e m an agem en t of sp in al m ot ic arcade th at exten ds cran iocaudally along both sides of th e
vascu lar lesion s. A secon d edit ion of Surgical Neuroangiography, spin al processes. In th e low er lum bosacral spin e, a h om ologous
volum e 1, w as publish ed in 2001.12 Th e last t w o decades h ave arrangem en t is recogn izable—w ith th e m edian sacral ar ter y rep -
been ch aracterized by advan ces in diagn ost ic m icroangiograph ic resen t ing th e con t in u at ion of th e aor t a, an d in tern al iliac ar ter-
an d em bolizat ion tech n iqu es. ies con sidered th e h om ologu es of th e paravertebral longit udin al

89

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90 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 6.1 Som atotopic organization of the vertebrospinal arterial vasculature, highlighting segm ental vessels and homologous longitudinal anastom oses.
(Courtesy of Maksim Shapiro, www.neuroangio.org.)

arcades, respect ively—supplying th e correspon ding low er lu m - cer vical spine. Developm ent of craniocaudal intersegm ental anas-
bar an d sacral m etam eres (Fig. 6.1). Select ive inject ion of th e tom oses su p por t ing vascu larizat ion of th e h ead, cou pled w ith
m edian sacral ar ter y t yp ically en ables visu alizat ion of m ost or th e overall redu ct ion in n eck t issu e volu m e, produ ce an arrange-
all of the low er lum bar (L5) an d sacral segm en tal ar teries, w h ich m en t apparen tly dom in ated by longit udin al ch an n els, each of
an astom ose laterally w ith correspon ding bran ch es of longit udi- w h ich correspon ds to a h om ologous vessel at th e th oracic level.
n ally orien ted lateral sacral ar teries, h om ologues of prever tebral From an terior to p osterior, th e an terior (ascen d ing) cer vical ar-
ar teries at th e th oracic level (Fig. 6.2). Th us, a com plete spin al ter y correspon ds to th e prever tebral ar ter y, th e ver tebral ar ter y
angiogram m ust in clu de inject ion s of both in tern al iliac ar teries, (cou rsing in t h e cer vical osseou s h om ologu e of t h e t ran sverse
to op acify t h e lateral sacral ar ter ies bilaterally, as w ell as t h e p rocess) is h om ologou s w it h t h e p araver tebral ar ter y, an d t h e
m edian sacral ar ter y. deep cer vical arter y is hom ologous w ith the post tran sverse anas-
Th e sam e segm en t al ar ran gem en t , w it h con sid erable m od i- tom osis (Fig. 6.1). Th e rem n an t t ran sverse segm en tal ar teries of
ficat ion , can be recogn ized t h rough ou t t h e u p p er t h oracic an d th e cer vical sp in e con n ect th ese sep arate longit u din al ch an n els

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6 Spinal Vascular Anatomy 91

a b c

d e f

Fig. 6.2a–f Inferior lum bar and sacral anatomy. (a) Stereo pair. (b) Native B, native image. (d,e) Stereo pair and native angiographic images of left in-
im age. (c) Selective catheterization of a com m on L5 segm ental trunk ternal iliac artery injection, demonstrating an S2 level dural arteriovenous
(white arrow), also giving rise to the m edian sacral artery (normally arising fistula bet ween S1 and S2 level radicular arteries (Ka) and S2 radicular vein (j).
from the region of aortoiliac bifurcation). The injection opacifies bilateral (f) Another patient with a dural arteriovenous fistula supplied from internal
L5 and sacral segm ental arteries (B), and the prevertebral anastom otic net- iliac radicular arteries. (Courtesy of Maksim Shapiro, www.neuroangio.org.)
work (G), which is hom ologous with lateral sacral arteries. A, stereo pair;

and ser ve as potential collateral channels w ithin the cer vical ver- u llar y bran ch (ar ter y of Lazor th es, Fig. 6.3) origin ates from t h e
tebrobasilar system , becom ing m ore n ot iceable in th e set t ing of low er ver tebral ar ter y. Th e u pper th oracic spin e ser ves as a t ran -
occlusive ver tebral disease. As a con sequen ce of th is em br yologi- sit ion al zon e in w h ich segm en t al ar teries are su pp lied by th e
cally d erived vascu lar arrangem en t , cer vical con t ribu t ion s to th e suprem e in tercostal arter y, w hich corresponds to prom inen t con -
an terior spin al axis can arise from any of th e above longit udin al tin u at ion of th e pret ran sverse an astom osis above th e aor t ic arch
vessels, alt h ough m ost com m on ly, t h e d om in an t rad icu lom ed - an d below th e m etam eric subclavian ar ter y.

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92 I Developm ent, Anatomy, and Physiology of the Central Nervous System

a b c

d e f

Fig . 6.3a–f (a,b) Front al and (c) lateral stereo pair projection digit al segm ental artery (short white arrow). P, radiculom edullary artery. (f) Stereo
subtraction and native angiographic views of right vertebral artery injec- pair, right suprem e intercostal segm ental artery origin of the anterior spi-
tion, visualizing a dom inant cervical radiculom edullary artery (P, artery nal artery (sam e legends as above) opacified via right T4 segm ental artery
of Lazorthes) and the anterior spinal artery (Q), anastom osing with its basi- injection. Note the transient contrast reflux into a cervical radiculom edul-
lar hom ologue (long white arrow). Very faint posterior spinal artery (T) is lary branch (P); prom inent post transverse anastom osis is present (I), as
best seen in stereo, as well as the lateral spinal artery (short white arrow). well as another longitudinal anastom osis (white arrow) bet ween adjacent
(d,e) Anterior spinal artery (Q) origin from deep cervical artery. Note the suprem e intercostal, T4, and T5 segm ental arteries. (Courtesy of Maksim
collateral opacification of the vertebral artery (long white arrow) via the C2 Shapiro, www.neuroangio.org.)

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6 Spinal Vascular Anatomy 93

Segmental Arterial Anatomy After its origin from th e aor ta, th e proxim al segm en t al ar ter y
(label B in Fig. 6.4) follow s p osterolaterally t h e con tou r of t h e
Th e follow ing discu ssion is visu ally recap it u lated in Fig. 6.4. Th e ver tebral body, giving off sh or t bran ch es (label D) pen et rat ing
protot ypical th oracic or lu m bar spin al segm en tal ar ter y (label B th e cortex an d p oten t ially p ar t icip at ing in su pp ly of m arrow -
in Fig. 6.4) origin ates from th e aort a (label A). Th e occasion ally replacing vascular lesion s. At th e lateral aspect of th e ver tebral
observed developm ental hypoplasia of a segm ental artery is usu- body, th e segm en tal ar ter y gives rise to its dorsal sp in al t r un k
ally com pensated by hypertrophy of prevertebral or paravertebral (label E, a.k.a. d orsal spin al ar ter y or dorsosp in al ar ter y), w h ich
an astom oses w ith th e adjacen t ipsilateral segm en ts (Fig. 6.5) ap - itself quickly bifurcates in to dorsal (K) an d ven t ral division s (H).
pearing angiograph ically as a “conjoined” segm ental artery. In the (In som e cases th e ven t ral division com es off separately, as dia-
lu m bar sp in e, fu lly or n early conjoin ed con t ralateral segm en t al gram ed in Th ron et al10 [p age 9] an d in Fig. 6.4 [w h ere both ar-
ar teries are seen w ith in creasing frequ en cy (Fig. 6.2). Th e L4 an d rangem en t s are diagram ed] an d n am ed th e sp in al bran ch .) Th e
L5 segm ental arteries m ay originate from the m edian sacral artery segm en t al ar ter y con t in u es as eith er an in tercostal (label F, th o-
or vice versa, depen ding on th e level of th e aor t ic bifurcat ion . racic levels) or m u scu lar ar ter y (F, lum bar levels).

Fig. 6.4 Schem atic of vertebrospinal arterial circulation. A, aorta; B, seg- P, radiculom edullary artery; Q, anterior spinal artery; R, m esh-like pial ar-
m ental artery; Ba, intersegm ental arterial anastom osis; C, prevertebral terial net work; S, T, posterior spinal artery; U, V, pial arterial net work anas-
anastom otic net work; D, direct vertebral body feeding arteries; E, dorsal tom oses bet ween anterior and posterior spinal arterial system s; W, sulco-
spinal artery; F, intercostal/m uscular artery; G, pretransverse anastom otic commissural artery; X, central (centrifugal) system of sulcal arteries; Y, rami
net work; H, dorsal division of the dorsal spinal artery; I, post transverse perforantes of the peripheral (centripetal) system, originating from pial net-
anastom otic net work; J, m uscular branches of the post transverse anasto- work of the cord; altogether, the pial net work and ram i perforantes (R + Y)
m otic net work; K, ventral division of the dorsal spinal artery; Ka, radicular are called the vasocorona or corona vasorum ; Z, rami cruciantes (a.k.a. crux
artery; La, ventral epidural arcade; Lb, dorsal epidural arcade; M, nerve root vasculosa or ram i anastom otici arcuati). (In all figures pertaining to the ar-
sleeve dural branch of the ventral division dorsal spinal artery; N, dural terial system , these same labels apply.) (Courtesy of Maksim Shapiro, www
branch of the ventral division dorsal spinal artery; O, radiculopial artery; .neuroangio.org.)

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94 I Developm ent, Anatomy, and Physiology of the Central Nervous System

With respect to th e dorsal spin al arter y (label E in Fig. 6.4), it s becom e th e radicular ar ter y (Ka), supplying an terior an d poste-
ven t ral d ivision (K) t raverses t h e n eu ral foram en an d su p p lies rior n er ve roots, an d at discrete levels con t ribut ing to th e vascu -
all n eural, du ral, an d osseous st ruct ures w ith in an d adjacen t to larizat ion of th e spin al cord as radicu lom edu llar y (P) or radicu -
th e spin al can al. An teriorly, prior to con t in u at ion th rough th e lopial ar teries (O, see below ).
n er ve root sleeve, th e ven t ral division gives off an terior epidu ral Th e dorsal division of th e dorsal spin al ar ter y (label H in Fig.
bran ch es th at form a ch aracterist ic, h exagon al-sh aped ret rocor- 6.4) p asses p osteriorly ben eath th e ip silateral t ran sverse process
poreal arcade vascu larizing th e ven t ral epid u ral sp ace (label La), an d along th e outer surface of th e lam in a, form ing a post t ran s-
an d ser ving as a poten t ial collateral con duit to th e con t ralateral verse longit u d in al ar ter ial p lexu s (I) close to t h e sp in ou s p ro-
segm en t al ar ter y. Bran ch es to t h e p oster ior (d orsal) ep id u ral cesses, and supplying the paraspinal tissues via m ultiple branches
space (Lb) form a less consistently visualized epidural arcade, an d (J). Collateral an astom oses bet w een adjacen t segm en tal arteries
su p p ly som e of p osterior osseou s elem en t s. Th e con t in u at ion of occur th rough m ult iple in t ra- an d ext raspin al levels. As m en -
th e ven t ral bran ch becom es associated w ith th e corresp on ding t ion ed above, th e m ost effect ive t ran sverse an astom osis bet w een
n er ve root sleeve, w h ere it p rovid es rad icu lod u ral bran ch es to left- an d righ t-sided vessels is rep resen ted by th e ret rocorporeal
su p p ly region al du ra (M), an d u lt im ately pen et rates th e sleeve to arcade (La) w ithin the anterior epidural space (Fig. 6.5). The sam e

a b c

Fig. 6.5a–c (a-c) T12 segm ental artery injection of a young, norm oten- (single white arrow, one level above the catheter), with a corresponding
sive slender patient, providing exquisite visualization of the various trans- sm all intercostal artery caudal to it s norm al position (double white arrow).
segmental anastomoses, demonstrating a hexagon-shaped (white hexagons) Both radiculom edullary (P) and radiculopial (O) arteries are present, the
m ultilevel anterior epidural arcade (La), and prevertebral anastom oses former demonstrating its characteristic midline course. (Courtesy of Maksim
(G). Note the developm ental hypoplasia of the right T11 segm ental artery Shapiro, www.neuroangio.org.)

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6 Spinal Vascular Anatomy 95
arcade is capable of suppor t ing adjacen t cran iocau dal levels, al- Supply of the Spinal Dura
though extraspinal prevertebral (label C in Fig. 6.4), pretran sverse
(label G in Figs. 6.5 an d 6.6), an d occasion ally post t ran sverse Th e su pp ly of th e sp in al du ra follow s a bilateral segm en t al d ist ri-
(Fig. 6.7) longit u din al an astom oses bet w een segm en t al ar teries but ion , arising from th e ven t ral (in t raspin al) division of each
are m ore effect ive in th is role. Occasion ally, th e post t ran sverse dorsal spin al arter y (label K in Fig. 6.4). Th ese m en ingeal vessels
arcade is m istaken for the posterior or anterior spinal arter y, de- (M) su p p ly t h e n er ve root sleeves an d give r ise to bran ch es ven -
spite its m ore m eandering course and different orientation of the t rally an d d orsally w it h in t h e sp in al can al, h avin g lim ited p o -
dorsal trunk as com pared w ith th e radiculom edullar y arter y. Ste- ten t ial for collateral suppor t of its n eigh bors. At th e level of th e
reoscopic or oblique view s are useful in resolving these issues (Fig. foram en m agn um , th e ven t ral dural bran ch es an astom ose w ith
6.6). At cer vical spin al levels, th e ascen ding cer vical, ver tebral, du ral bran ch es of th e ascen ding p h ar yngeal ar ter y. Th e dorsal
an d deep cer vical ar teries represen t h om ologu es of th e prever- m en ingeal arteries likew ise an astom ose w ith dural bran ch es of
tebral (label C in Fig. 6.4), pret ran sverse (G), an d post t ran sverse th e ver tebral, occip ital, an d un u su ally, th e posterior in ferior cer-
(I) longit u din al arcad es, resp ect ively (see also Fig. 6.1). ebellar ar teries.

a b c

Fig. 6.6a–c (a) Stereo pair, and (b) legend, demonstrating multiple trans- proxim al segm ental arteries (Ba) is present, along the anterior circum fer-
verse and longitudinal anastom otic connections. The prevertebral anasto- ence of the vertebral body. A prom inent posterior spinal artery (T) and its
m osis, hallm arked by its proxim al location relative to segm ental artery os- radiculopial feeder (O) can be seen, in an off-m idline position. (c) A radicu-
tium , is labeled C. Also present are pretransverse (G) and post transverse (I) lomedullopial artery (white arrow) supplying both anterior (Q) and posterior
anastom oses. A not so com m only encountered anastom osis bet ween t wo (T) spinal arteries. (Courtesy of Maksim Shapiro, www.neuroangio.org.)

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96 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 6.7 Lum bar segm ental artery injection, dem onstrating a well-devel- visualization of the adjacent cranial segm ental artery (B). F, m uscular ar-
oped post transverse anastom otic net work (I) visualized through the ven- tery, hom ologue of the intercostal artery. (Courtesy of Maksim Shapiro,
tral division (H) of the segm ental artery (B), with its m uscular branches (J), www.neuroangio.org.)
as well as the pretransverse anastomosis (G), both contributing to collateral

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6 Spinal Vascular Anatomy 97
Arterial Supply of the Spinal Cord slen der over th e m idth oracic area (0.1–04 m m ) (Th ron et al,10
p. 7) (Fig. 6.9). Duplicat ion s an d fen est rat ion s are com m on , par-
Th e ar teries su p plying n eu ral st ru ct u res w ith in t h e du ral sh eath
ticularly adjacent to confluence points w ith th e dom inant radicu -
can be divided in to th ree grou p s. Sm all radicu lar ar teries (label
lom edu llar y arteries (Fig. 6.8).
Ka in Fig. 6.4), bran ch es of th e dorsal spin al ar ter y (see above),
are presen t at n early ever y level, an d supply th e n er ve root . Th ey
do not participate in the supply of the cord, and are usually below
angiograph ic resolut ion . At som e levels, th e territor y of th ese ar- Radiculomedullary Arteries
teries is n ot lim ited to th e n er ve root , in w h ich case th e vessel is Th e radicu lom edu llar y con t ribu t ion to th e cer vical an terior sp i-
term ed (1) radiculom edullar y (P), w h en su pplying th e an terior n al ar ter y (in dom in an t form kn ow n as th e ar ter y of th e cer vical
spin al axis (Figs. 6.3, 6.6, 6.8), (2) radiculopial (O) w h en supply- en largem en t) m ost com m on ly arises from th e p roxim al cer vical
ing posterior or posterolateral spinal arterial arcades (Fig. 6.6a,b), ver tebral ar ter y (som et im es n am ed th e ar ter y of Lazor th es) (Fig.
or occasion ally (3) radicu lom edullopial w h en con t ribut ing to 6.3a– d), th ough n ot in frequen tly it origin ates in stead from an te-
th e an terior an d p osterior spin al axes sim u lt an eou sly (Fig. 6.6c). rior cer vical, deep cer vical (Fig. 6.3d,e), su p rem e in tercost al, or
u pper th oracic segm en t al arteries (Fig. 6.3f), reflect ing con se-
qu en ces of variat ion in th e in d ividu al developm en t of segm en t al
Anterior Spinal Artery som atotop ic organ izat ion . At th oracic an d lum bar levels, radicu -
From a developm ental stan dpoin t, the anterior spinal artery (label lom ed u llar y vessels ar ise from t h e ven t ral d ivision of t h e seg-
Q in Fig. 6.4) form s as an oth er longit udin al an astom osis bet w een m en t al ar ter y. Typ ically six to 10 rad icu lom ed u llar y ar ter ies
m ultiple t ran sverse radicular arteries, follow ed by regression p ersist in to adulth ood, in cluding th e h igh ly ch aracterist ic ar ter-
(d esegm en t at ion as p er Lasjau n ias et al,12 p p . 77–81) of m ost ies of th e cer vical (Lazorth es ar ter y) an d lum bar (a.k.a. ar ter y of
radicu lar con t ribu tors, w ith th e except ion of th ose p ersist ing Adam kiew icz or ar ter ia rad icu lar is m agn a) en largem en t s. Th e
as rad icu lom edu llar y (P) ar ter ies. In t h e adu lt for m , t h e an te- ar ter y of Adam kiew icz (Figs. 6.6 an d 6.8) ar ises var iably from
r ior sp in al ar ter y is a longit u d in al ch an n el located in th e an terior th e low er th oracic or u p p er lu m bar segm en t s. It origin ates from
m edian sulcus. Th e caliber of an terior spin al arter y varies w ith th e left side bet w een T9 an d T12 segm en t s th ree-fou r th s of th e
region al h em odyn am ic requ irem en t s, being larger in th e cer vi- t im e, likely driven by h em odyn am ic con dit ion s of th e develop ing
cal (0.2–0.5 m m ) an d lu m bar region s (0.5–0.8 m m ), an d qu ite fet us, an d provides th e prin cipal radiculom edullar y con t ribu t ion

a b c d

Fig. 6.8a–d (a) Early arterial, (b) late arterial, (c) native, and (d) venous (La). Note the subtle caliber change where the radiculopial artery pierces
phase im ages. The artery of Adam kiewicz (Ka), originating at the left L1 the dura (short black arrow). (d) Venous phase im age dem onstrating ex-
level, opacifies the anterior spinal artery (Q). The force of contrast injection pected visualization of surface cord vein (e, either anterior or posterior),
transiently reverses flow in a sm aller radiculom edullary contributor (Ka) and the great radicular vein (j), the venous hom ologue of the Adam kiewicz.
cephalad of the Adam kiewicz. A faint radiculopial artery (O) from the con- (Courtesy of Maksim Shapiro, www.neuroangio.org.)
tralateral right L1 level is visualized through the anterior epidural arcade

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98 I Developm ent, Anatomy, and Physiology of the Central Nervous System

Fig. 6.9 Double-catheter investigation of anterior spinal artery integrit y thoracic anterior spinal artery (Q). (Courtesy of Maksim Shapiro, www
in a patient with sudden onset of lower extrem it y paraplegia. Sim ultaneous .neuroangio.org.)
left T9 and L1 segm ental artery injections opacify a slender section of lower

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6 Spinal Vascular Anatomy 99

to th e an terior spin al axis w ith in th e low er spin al cord. Radicu- Th e su rface of th e cord is covered w ith a m esh w ork of th in
lom ed u llar y ar ter ies t race a ch aracter ist ic ascen d in g cou rse ar ter ial ch an n els, w h ich for m t h e p ial ar ter ial n et w ork. Bot h
follow ing th eir pen et rat ion of th e dura. Th e con fluen ce of th e an ter ior an d p oster ior sp in al ar ter ies m ay be con sid ered as en -
radicu lom edu llar y ar ter y an d an terior sp in al arter y t ypically larged longit udin al ch an n els of th is n et w ork (Th ron et al10 ). Oc-
displays a h airpin t urn, w here a larger inferior an d sm aller caliber casion ally, a dom in an t pial t r un k (label V in Fig. 6.4) from th e
su p erior segm en ts of th e an terior sp in al arter y are visu alized, an terior spin al ar ter y m ay circum feren t ially con t ribute to th e
w ith a ch aracterist ic discon t in uit y of th e an terior spin al arter y posterior sp in al arcade, an d even vice versa.
proper (Fig. 6.8). Except ion s to t h e d iscon t in u ou s n at u re of t h e p oster ior sp i-
In con t rast to th e an terior spin al system , th e posterior spin al n al system are n ot ably p resen t at bot h en d s of t h e sp in al cord .
ar ter ies (labels S an d T in Fig. 6.4) d o n ot exist as p aired con - Ar ter ial su p p ly of con u s m ed u llar is con sist s of a ch aracter is-
t igu ou s ch an n els (th ough are st u bborn ly m isrep resen ted as su ch t ic “basket-like” arrangem en t , reflect ing th e con flu en ce of th e
in cou n tless text s an d diagram s). In realit y, th e p osterior spin al term in al an terior spin al ar ter y w ith paired posterior (or pos-
ar ter ial arcad e is rat h er d iscon t in u ou s beyon d several adjacen t terolateral) spin al ar teries, via relat ively prom in en t an astom ot ic
levels. It is principally supported by m ultiple radiculopial arteries ch an n els called ram i cr u cian tes (label Z in Fig. 6.4, a.k.a. cru x
(label O), th e larger of w h ich can be visu alized angiograp h ically vascu losa or ram i an astom ot ici arcu at i) (Fig. 6.10). Visu alizat ion
as h airp in -like vessels, sim ilar to th e radicu lom edu llar y ar ter y, of th is vascu lar basket , con sist ing of th e term in al an terior (label
but alw ays located off-m idlin e on a w ell-align ed an teroposterior Q) an d p aired p osterior sp in al (T) ar teries an d t h eir vasocoron al
exp osu re an d w ith ou t direct con n ect ion to th e an terior sp in al con n ect ion s (Y), is h igh ly desirable as p ar t of a com plete sp in al
ar ter y (Fig. 6.6). Th e n u m ber of visu alized radicu lopial ar teries is angiogram and angiographically identifies the spinal cord conus.
related to angiographic technique and qualit y of X-ray equipm ent. At th e rost ral en d of th e spin al cord, th e an terior spin al arter y

Fig. 6.10 Anterior spinal artery, conus basket views, in a petite patient. crux vasculosa, and ram i anastom otici arcuati. Faintly seen are several coro-
Early arterial phase im age shows the very rarely dem onstrated (in vivo) sul- nary pial arteries (R) on the surface of the cord. Venous phase im age shows
cocom m issural arteries (W), seen end-on as m ultiple dots outlining the the anterior spinal (or posterior spinal) surface vein (e), the filum term inal
m edian fissure. Late arterial-phase im ages dem onstrate the ideal appear- vein (i), and m ultiple cauda equina radicular veins (o). Several interverte-
ance of the conus m edullaris basket, with anterior spinal (Q) to posterior bral veins (n) are seen in the background, empt ying into the ascending
spinal (T) anastom oses (Z), which are variously termed as ram i cruciantes, lum bar vein (r). (Courtesy of Maksim Shapiro, www.neuroangio.org.)

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100 I Development, Anatomy, and Physiology of the Central Nervous System

usually an astom oses w ith th e basilar ar ter y (w h ich m ay be con - ral ven ou s p lexu s. Alth ough th e in t rin sic an d ext radu ral system s
sidered a h om ologu e of th e an terior spin al ar ter y at brain stem are h igh ly redun dan t , th e ext rin sic system an d specifically ra-
levels) (Fig. 6.3). Th e p oster ior/lateral su r face of t h e cer vico- dicu lar vein s represen t th e relat ively w eak segm en t in states of
m edu llar y ju n ct ion an d u p p er cer vical spin e is su pp lied by th e ven ou s congest ion .
lateral spin al ar ter y. Its relat ion sh ip w ith distal ver tebral or p os- Alth ough th e above n om en clat u re w as u sefu l at th e t im e of
terior in ferior cerebellar ar teries (from w h ich it t ypically arises) gross an atom ic dissect ion s, it is both con fu sing an d in conven ien t
w as u sed by Lasjau n ias et al13 th eoret ically to exp lain m u lt ip le w h en prim ar y an atom ic em ph asis is placed on th e angioarch i-
variat ion s in th e arrangem en ts of th e posterior in ferior cerebel- tect u re of th e spin al cord an d ver tebral colum n . Th e n am es as-
lar ar ter y an d ver tebral arteries.14 Alth ough oth er auth ors do n ot sign ed to various plexuses do n ot int uitively reflect their locations
su p p or t t h is con cept u al fram ew ork, all agree on p resen ce of a or fu n ct ion al roles. Oth er term in ologies, alth ough less an atom i-
relat ively con stan t p osterolateral vessel th at su pplies th e up per cally defin ed, act u ally carr y m ore fu n ct ion al im p licat ion s, su ch
cer vical spin al cord. as th e role of various com pon en ts of Bat son’s 15 ven ous plexus, in
From th e st an dp oin t of in t rin sic cord su pp ly, sin ce th e inves- it s p rim ar y role as a collateral to th e caval system . With th is in
t igat ion s of Kadyi3 an d Adam kiew icz,1,2 th e m icroar terial system m in d, w e w ill refer to ven ou s com p on en t s of th e ver tebrosp in al
of th e spin al cord w as subdivided in to cen t rifugal (cen t ral) an d system based m ore specifically on th eir locat ion and drain age ter-
cen t ripetal (periph eral) com pon en ts. Th e an terior spin al (an d ritor y, w ith correlation to the old nom enclature in parentheses.
dom in an t radicu lom edu llar y) ar ter y gives rise to m u lt ip le su lco- Th e intram edullar y veins, corresponding precisely to the older
com m issu ral vessels (label W in Fig. 6.4), w h ich p en et rate d eep term in ology of th e in t rin sic ven ous system (black color in Fig.
w ith in th e an terior m edian sulcu s to vascularize th e cen t ral gray 6.11) are respon sible for drain ing th e subst an ce of th e cord. Al-
m at ter. Th ese vessels are m ost n u m erous in region s of th e cer vi- low ing for extensive variation (m uch m ore than would be the case
cal an d lu m bar en largem en t s an d are usu ally below digit al su b - for an ar terial coun terpar t), th e in t ram edu llar y n et w ork con sists
t ract ion angiography resolu t ion , alth ough occasion ally m ay be of t w o prin cipal com pon en ts: cen t ral (sulcal) and periph eral (ra-
visualized in slender or young patients (Fig. 6.10). The sulcocom - dial) vein s. Th e cen t ral com p on en t (label a in Fig. 6.11) predom i-
m issural arteries give rise to a n et w ork of sm all vessels (label Y in n an tly drain s th e territor y of gray m at ter in a cen t ripetal fash ion
Fig. 6.4), w h ich radiate cen t rifugally from cen t ral cord to n ou rish (opposite to th e cen t rifugal ar terial system of th e sulcocom m is-
both gray an d w h ite m at ter. Th e sulcocom m issural dist ribut ion su ral ar teries), con du ct ing its ou tflow in to su lcocom m issu ral
is classically described as sp an n ing th e an terior t w o-th irds of t h e vein s (label b), w h ich in t urn em pt y in to th e (surface) spin al cord
cross-sect ion al area of th e spin al cord. Its distal-m ost , cen t rifu - vein s. Th ere is n o an terior versu s posterior dist ribu t ion in ve-
gally orien ted t ributaries, an astom ose w ith pen et rat ing bran ch es n ous drain age, an d th e en t ire system fun ct ion s in a kin d of circle.
of fine, centripetally directed ram i perforantes (label X), originat- Th e p erip h eral in t ram ed u llar y vein s com p rise sh or t radial vein s
ing from th e exten sive pial vascular m esh w ork covering th e su r- circum feren t ially arrayed aroun d th e spin al cord (c, also called
face of the spinal cord (a.k.a. vasocorona or corona vasorum ). This m argin al bran ch es by Th ron et al 10 ), w h ich d rain p er ip h eral/
arrangem en t creates a w atersh ed zon e w ith in th e cord paren - su bp ial w h ite m at ter an d em pt y directly in to su rface spin al cord
chym a bet w een cen t rip et al an d cen t rifugal system s, exqu isitely (p er im ed u llar y) vein s. Th e overall ar rangem en t is st rongly
dem on st rated in ex vivo sect ion s by Th ron et al10 (pp. 29, 30). t ran sverse (segm en tal), w ith a p au cit y of longit u din ally arrayed
veins w ithin the cord parenchym a. An extensive net w ork of trans-
versely arranged ven ou s collaterals, h ow ever, does exist w ith
Spinal Venous Anatomy spin al cord segm en t s bet w een th e cen t ral an d periph eral in t ra-
Historically, th e bu lk of vascular an atom ic w ork in th e ver tebro- m edu llar y vein s (d) (in con t rast w ith th e collateral disposit ion of
spin al axis w as focused on th e ar terial n et w ork. Relat ively recen t spin al ar teries), w ith even larger t ran sm edullar y an astom oses
in terest in th e ven ou s system h as been , to a large exten t , m ot i- presen t bet w een su rface cord vessels (g, h , vid e in fra), both of
vated by gradual recogn it ion of its crit ical role in th e path ophysi- w h ich ap p aren t ly fu n ct ion to effect ively equ alize ven ou s p res-
ology of spin al vascular disorders, m ost n ot ably represen ted by sures across region al segm en ts of th e cord.
th e sp in al d u ral fist u la. Ou r u n derst an ding of both an atom ic an d Ext rinsic system is a par t icularly m isleading term , as it con -
physiological asp ects related to th e sp in al ven ou s system con t in - sist s of t w o an atom ically an d fu n ct ion ally d ist in ct elem en t s. It
u es to evolve. Lasjau n ias an d Beren stein ,11,12 an d Th ron et al 10 is m ade u p of w h at sh ou ld p rop erly be called cord su rface vein s
can be st u d ied for in d epth d iscu ssion s of both an atom y an d (e, f) an d radicular vein s (k), w h ich con n ect cord surface vein s
path op hysiology. th rough th e n er ve root sleeve w ith th e in ter ver tebral vein s (n ).
Histor ically, t h e ver tebrosp in al ven ou s system h as been t ra- Th e on ly p rop er t y th ese t w o system s h ave in com m on is th at
d it ion ally su bdivided in to th ree com pon en t s, illust rated in Fig. th ey are both in t radu ral an d ext ram edullar y, w h ich is sufficien t
6.11; in t radural vein s con sist of (1) an in t rin sic ven ous n et w ork for a gross descript ion , but does n ot take in to accoun t th eir fun -
su bser ving th e sp in al cord p aren chym a an d (2) an ext rin sic sys- dam en tal differen ces, as discu ssed below.
tem in cluding surface vein s of th e spin al cord an d n er ve root s Th e vein s p resen t on t h e su r face of t h e cord w ill be refer red
(th e radicu lar vein s) lin king th e in t radural ven ous system w ith to as cord surface vein s or sim ply spinal vein s, as th ey are usu ally
(3) th e ext radural ven ous plexus, w h ich con sists of both vein s called in th e cross-sectional im aging literat ure, particularly w hen
su rroun ding an d w ith in th e ver tebral body, an d dorsally in th e d escr ibing t h eir p rom in en ce in t h e set t ing of ar ter ioven ou s
parasp in al m u scu lat u re an d adjacen t to th e p osterior elem en ts. sh u n t s. Desp ite great var iabilit y, m ost sp ecim en s d em on st rate
Th e in t rin sic ven ou s system ser ves th e su bst an ce of th e spin al t h e p resen ce of w ell-d evelop ed an ter ior m ed ian sp in al vein s
cord . Th e ext rin sic system , also in t radu ral, con sist s of su rface (e, run n ing w ith in th e an terior [ven tral] m edian sulcus, closely
cord vein s an d radicu lar vein s, lin king th e cord w ith th e ext radu - adjacen t to th e an terior spin al ar ter y) an d posterior m edian spi-

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6 Spinal Vascular Anatomy 101

Fig. 6.11 Vertebrospinal venous system . a, centripetal net work of veins, dura of the nerve root sleeve; n, intervertebral vein; o, radicular veins of the
predominantly draining the gray m at ter into (b) the central (sulcal) veins of cauda equina; p, anterior epidural (a.k.a. ventral intrinsic) venous plexus;
the intrinsic system; c, peripheral (radial, a.k.a. m arginal) centrifugal veins q, posterior epidural (a.k.a. dorsal intrinsic) venous plexus; r, ascending
of the intrinsic system ; d, venous anastomosis bet ween the centripetal and spinal (lum bar) vein; s, basivertebral vein, draining the intravertebral
centrifugal system s; e, anterior (ventral) m edian vein (surface cord vein); body venous plexus (t); u, anterior extrinsic venous plexus surrounding the
f, posterior (dorsal) m edian vein (surface cord vein); g, transm edullary surface of the vertebral body; v, posterior extrinsic venous plexus on the
anastom osis bet ween dorsal and ventral surface cord veins; h, extrinsic sur- surface of the lam ina/posterior elem ents, also participating in drainage of
face anastomosis bet ween dorsal and ventral surface cord veins; i, vein of the paraspinal muscles. (In all figures pertaining to the venous system, these
filum term inale; j, dom inant radicular vein of the cauda equina; k, radicular sam e labels apply.) (Courtesy of Maksim Shapiro, www.neuroangio.org.)
vein; l, nerve root sleeve; m, shallow angle of radicular vein piercing the

n al vein s (f) along th e dorsal m edian fissure. Un like th e ar teries, secon dar y to an ar terioven ou s fist u la (Fig. 6.12). In th e cer vical
eith er set of th ese cord su rface vein s m ay be larger or sm aller, spin e, it is n ot un com m on for surface cord vein s to be angio-
reach ing u p to 1.5 m m in size. In th e th oracic segm en t , th e pos- graph ically visu alized as w ell, as th ey are less at ten uated by th e
terior vein s ten d to be larger, an d often split in to t w o or m ore; caliber of th e n eck w h en com pared w ith th e th ickn ess of t ypical
th is posterior dom in an ce is m ain t ain ed in path ological st ates, h um an t r un ks. At th e cran iocer vical jun ct ion , th e spin al vein s
w h en dilated posterior cord surface vein s ser ve as a h allm ark of com m u n icate w ith th e m argin al sin u s (w h en p resen t ), circu m -
a spin al dural AV fist ula. Th e an terior an d posterior m edian vein s scr ibing th e foram en m agn u m , or w it h t h e in fer ior p et rosal/
are con n ected by m u lt ip le t ran sverse “coron al” vein s (h ) fol- occip it al sin u ses, as w as elegan t ly d em on st rated by Bat son .15
low ing th e cur vat ure of th e cord, as w ell as t ran sm edullar y Th ese cer vicocran ial ven ou s con n ect ion s can be occasion ally
ch an n els (g) ru n n ing th rough th e cord su bst an ce. Th ese con n ec- dem on st rated w ith delayed im aging of th e n eck du ring angio-
t ion s are greatest in th e cer vical an d u pp er th oracic sp in es, an d graphic exploration of a particularly advanced spinal dural AV fis-
are th ough t to represen t an effect ive m ech an ism for pressure t ula, at test ing to severe cord congest ion an d segm en t al occlusion
equ alizat ion th rough ou t th e su rface sp in al ch an n els, esp ecially of sequen t ially affected radicular vein s (Fig. 6.12). At th e cauda
in ligh t of poten t ially lim ited in t ram edu llar y p ressu re equilibra- equin a, th e an terior an d posterior spin al vein s often con t in ue as
t ion m ech an ism s. Th e sp in al vein s are relat ively large, an d angio- th e vein of filu m term in ale (label i in Fig. 6.10) or along on e of
grap h ic opacificat ion of a dom in an t radicu lom edu llar y arter y th e n er ve root s as a prom in en t term in al vein (label j in Fig. 6.11),
(Adam kiew icz) t ypically is follow ed by th eir appearan ce in ve- w h ich can also be con sidered as a radicular vein , em pt ying in to
n ou s p h ase im ages, w h ich occu rs tem p orally som ew h at later in th e ext radu ral in ter ver tebral vein s (label n in Fig. 6.11).
th e angiograph ic sequen ce com pared w ith th e AV t ran sit n or- Th e radicu lar vein s (label k in Fig. 6.11), w h ich ru n along dor-
m ally obser ved in the brain (6–8 seconds). Failure to obser ve such sal and/or ventral ner ve roots, exten d from the surface of the cord,
cord surface vein or vein s follow ing a spin al p aren chym agram is across th e subarach n oid space, an d en ter th e dural n er ve root
eviden ce of un derlying spin al ven ous congest ion , occasion ally sleeve (l). Th ese vein s p ierces th e n er ve root sleeve at a sh allow

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a b c d e f g h

Fig. 6.12a–h Investigation of spinal veins in a patient with high-flow dural cal spine and skull base, with rem aining radicular vein (draining the fistula
fistula. (a) Left T8 segm ental artery injection giving rise to the artery of at cervical spine level; m ore cranial drainage is also present, as the surface
Adamkiewicz, late arterial phase, dem onstrating the anterior spinal artery cord vein is seen to the level of skull base). (g ) Following N-but yl cyanoac-
(Q). (b) Delayed view of the same injection, with no visible surface cord rylate em bolization, injection of the anterior spinal artery, now visualizing
veins and contrast persisting as parenchym al blush—strong evidence of the conus basket in late arterial phase, and (h) venous phase im ages now
underlying venous congestion. (c,d) Left L4 segm ental artery injection, un- dem onstrating spinal cord drainage into a cord surface vein (e, anterior or
covering the underlying dural fistula with m arked congestion of thoracic posterior), at testing to postem bolization resolution of spinal venous con-
and lum bar surface cord veins; no radicular veins are visualized along the gestion. (Courtesy of Maksim Shapiro, www.neuroangio.org.)
entire thoracic spine. (e,f) Delayed views of fistula injection over the cervi-

angle (m ), su ch th at a por t ion of th e vein s r un w ith in th e dura— as exem plified by con dit ion s accom panying sym ptom at ic spin al
an arrangem en t n ow th ough t by th e m ajorit y of an atom ists to du ral AV fist u las (Fig. 6.12). Th e p rotot yp ical fist u la is est ab -
act as a fun ct ion al valve, preven t ing ven ous reflu x in to th e cord lish ed bet w een a radicular ar ter y an d adjacen t radicular vein , in
du ring th e Valsalva m an euver an d oth er states of in creased cen - th e region of th e n er ve root sleeve. Th is leads to radicu lar vein
t ral ven ou s p ressu re (m ech an ical valves h ave n ot been con sis- congest ion , w ith reversal of blood flow in to th e su rface p erim ed-
ten tly docum en ted w ith in radicular vein s, an d alm ost cer t ain ly u llar y sp in al cord vein s. It follow s from th is descript ion th at th e
d o n ot exist in t h e h u m an ). On t h e ou t sid e of t h e n er ve root m ost depen den t aspects of th e cord are alw ays m ost congested,
sleeve, th e radicu lar vein s join w h at are classically term ed th e regardless of th e act ual locat ion of th e AV fist u la. Th is st ate m ay
in ter ver tebral vein s (n ), w h ich also drain th e an terior (ven t ral, p) be tolerated for som e t im e th rough redist ribut ion of th e path o-
an d posterior (dorsal, q) in tern al epidural ven ous plexu ses, dis- logical in flow across effect ive sp in al su rface ven ou s an astom o-
cussed below. A great radicular vein can be dem on st rated angio- ses (described above), u lt im ately ch an n eling th e excess sh u n ted
grap h ically often in th e region of th e th oracolu m bar ju n ct ion , blood volum e in to adjacen t n orm al radicular vein s. Over t im e,
but alm ost n ever exit ing at th e sam e level as th e ar ter y of Adam - how ever, th ese draining radicular veins appear to close (occlude),
kiew icz (Fig. 6.8). At th e cau dal en d, n orm al fin e radicu lar vein s in creasing congest ion as progressively m ore dist an t cran ial ra-
can be occasion ally visu alized (in th e p et ite pat ien t) follow ing dicu lar vein s are recru ited to accom m odate th e excess drain age
th e cou rse of cauda equ in a n er ve root s (o); frequ en tly, a single of cord surface vein s. In som e cases, on ly direct drain age of lon -
large radicu lar vein w ith su ch off-cen ter orien tat ion (j) drain s git udin al spin al vein s in to skull base sin uses can be angiograph i-
th e spin al cord basket . Bet w een 30 an d 50 radicu lar vein s are cally visu alized by t h e t im e of d ed icated evalu at ion . W it h t h is
docu m en ted by p ost m or tem inject ion s in Th ron et al’s 10 sp eci- in m in d, it is rem arkable th at n eu rologic im p rovem en t or recov-
m en s; far few er are visu alized angiograph ically, in large par t du e er y can be ach ieved by closing t h e fist u la, even w h en t h e exist -
to sp at ial resolu t ion lim itat ion s of in vivo angiography, an d th e in g radicu lar drain age system is so badly dam aged. As suggested
in abilit y to sim u ltan eously opacify th e en t ire spin al axis. Never- above, an im por tan t in dicator of spin al ven ous congest ion is th e
th eless, th e sam e Adam kiew icz inject ion as w ou ld visu alize th e lack of t im ely visu alizat ion of su rface spin al vein s follow ing an -
an ter ior or p oster ior sp in al vein (s) sh ou ld also op acify at least giograph ic invest igat ion of a dom in an t radiculom edullar y arter y
on e (u su ally t w o or t h ree) rad icu lar vein s, eit h er in t h e sam e (usually accom pan ied by a prolonged paren chym al ph ase spin al
region or along th e cau da equ in a (vide sup ra). cord blu sh ), at test ing to im p airm en t of n orm al drain age. Con se-
Th e radicu lar vein s, for w h atever reason , seem to be p ar t icu - qu en tly, successful t reat m en t of th e fist ula, via en dovascular or
larly p ron e to failu re in th e states of ch ron ic ven ou s congest ion , su rgical app roach , is often con firm ed, n ot on ly by obliterat ion of

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6 Spinal Vascular Anatomy 103

a b c d e

Fig. 6.13a–f Internal epidural venous plexus. (a,b) Stereo pair. (c) Native N-but yl cyanoacrylate em bolization of the hem angiomas. (e) A different
im age. (d) Legends. Injection of internal iliac artery in a patient with m ul- patient with m ultiple compression fractures, status post–percutaneous ce-
tiple paraspinal hem angiom as, one of which was located in the L5/S1 ven- m ent injection; dem onstrating basivertebral vein ostia (white arrows) and
tral epidural space (long white arrow) opacifies congested ascending lum bar m ethylm ethacrylate fill (black arrows). (Inset f) Two venous channels, part
veins (r), the superior and inferior foram inal (intervertebral) veins (n), and of the anterior external venous plexus (u) have been perm anently opacified
the ventral internal venous plexus (p). The patient suffered from back pain following injection of another level. (Courtesy of Maksim Shapiro, www
and radiculopathy secondary to venous congestion, which was relieved by .neuroangio.org.)

the sh unt, but also by angiograph ic visualization of surface spinal n orm al-caliber foram in al vein t raverses th e foram en surroun ded
cord veins in the appropriate spinal cord venous phase 16 (Fig. 6.12). by fat an d m ay be w ell seen , along w ith correspon ding arter y
Th e h istorical term ext rinsic venous system in clu des th e an te- and nerve, on high-qualit y MRI (particularly of the lum bar spine).
rior in tern al ver tebral p lexu s (label p in Fig. 6.11, a.k.a. ven t ral Outside th e foram en , it join s various cer vical an d paraver tebral
ep idu ral ver tebral p lexu s, an d variou s perm u t at ion s of t h ese vein s, often em pt ying in to a region al vein , in th e lum bar spin e
n am es), posterior in tern al ver tebral plexus (q, a.k.a. dorsal epi- term ed th e ascen ding (lum bar) vein (r), an d su bsequen tly in to
du ral ver tebral), an d th e in ter ver tebral vein (n ), w h ich sh ou ld azygou s/h em iazygou s vein s, th e in ferior ven a cava, an d p elvic
properly be called th e n eu ral foram in al ven ou s plexu s. An atom i- vein s, dep en ding on locat ion .
cally, th e term s vent ral epidural venous plexus an d dorsal epi- Ven ou s drain age of th e osseous ver tebral colum n is w ell de-
dural venous plexus seem to be m ost ap p rop riate. Both ep idu ral scribed. A rich ven ou s n et w ork w ith in th e ver tebral body em p -
plexu ses are h igh ly redu n dan t , th e ven t ral on e being som ew h at t ies in to th e ven t ral epidu ral ven ou s p lexu s by w ay of a com m on
larger overall. Both are equ ally poorly d em on st rated on arterial ven ou s collector at th e posterior m edian cor t ical surface, called
angiography; th eir direct ven ous inject ion s are largely of h istori- t h e basiver tebral vein (s). It s osseou s ch an n el is often seen as
cal in terest for diagn osis of disk h ern iat ion s an d oth er con dit ion s a ch aracter ist ic cleft on m id sagit t al recon st r u ct ion com p u ted
n ow h an dled by t ran saxial im aging (Fig. 6.13). Venous ph ase tom ography (CT) im ages. Mult iple addit ion al t ran sosseous vein s
con t rast com pu ted tom ograp hy angiograp hy (CTA) an d con t rast (t , som et im es best seen w ith m ethylm eth acr ylate, Fig. 6.13e)
m agn et ic reson an ce im aging (MRI) sh ow th e plexu ses w ell. Th eir also exist an d, in th e ver tebral body, op en in to w h at h as been
angiograp h ic ap p earan ces, h ow ever, sh ou ld be fam iliar, so as to h istorically term ed th e an terior extern al ver tebral ven ous plexus
recogn ize p oten t ial ven ou s congest ion ; t h e cer vical p lexu s is (u); prevertebral venous plexus seem s like a m ore precise n am e.
perh ap s m ost often involved w ith ver tebral an d p eriver tebral AV Th e p osterior elem en t s drain in to w h at is loosely defin ed as th e
fist ulas. From a fu n ct ion al st an dpoin t , it is m ost usefu l to th in k posterior external vertebral venous plexus (v), w hich w e feel m ay
of both plexuses as longit udin al colum n s of redun dan t ven ous be bet ter term ed paraspinal venous plexus. It is sit uated on th e
lakes, exten d ing along th e en t ire vertebral axis, w ith poten t ial outside of th e lam in a, along th e in terspin ou s ligam en t s, w ith in
con n ect ion s in t racran ially to th e m argin al an d p et rosal sin u ses, th e p arasp in al m u scu lat u re of erector sp in ae m u scles an d con -
as dem on st rated by Bat son .15 n ect ive t issues.
Th e ep id u ral p lexu ses d rain in to t h e in ter ver tebral vein s
(label n in Fig. 6.11), w h ich also receive th e radicu lar vein s (k).
Rath er th an u sing th e vagu e term intervertebral veins, w e prefer
th e m ore descript ive altern at ive of foram inal veins. Th ese vein s,
■ Conclusion
w hich m ay in fact be plexiform , h ave great capacit y for en large- Th e vascu lar an atom y of th e sp in al cord is less con sisten t th an
m en t to accom m odate sh un ts, as m ay be seen w ith h igh -flow AV th at of th e in t racran ial circulat ion . Despite variabilit y, com m on
fist u las of th e cer vical vertebral ar ter y, w h ere th e en t ire n eural pat tern s, based on developm en tal p rogram s from em br yon ic de-
foram en is filled w ith a large ven ou s st r uct ure. Th ey also provide velopm en t , are com m on ly seen . A detailed un derst an ding of spi-
t h e p r in cip al com m u n icat ion bet w een Bat son’s p lexu s an d th e n al vascular an atom y is essen t ial for diagn ost ic an d th erapeut ic
azygou s/h em iazygou s system s in st ates of caval occlu sion . Th e procedu res.

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References
1. Adam kiew icz AW. Die Blutgefäß e des Men csh lich en Rü cken m arks. I. Die 9. Djindjian R. Treatm ent of spinal angiom as by em bolization. In: Pia HW,
GefaBe der Ru cken m arks Subst an z. Berlin : Sit z. Ber. Akad. Wiss. Wien , Djindjian R eds. Spinal Angiom as: Advances in Diagnosis and Therapy. Ber-
Math . n at . Kl.; 1881:469–502 lin: Springer; 1978:189–200
2. Adam kiew icz AW. Die Blutgefäß e des Mencsh lich en Rü cken m arks. II. Die 10. Th ron AK, Rossberg C, Miron ov A. Vascular An atom y of th e Spin al Cord:
Gefäß e der Rü cken m arks- Oberflash e. Berlin : Sit z. Ber. Akad. Wiss. Wien , Neuroradiological Invest igat ion s an d Clinical Syndrom es. Vien n a; New
Math . n at . Kl.; 1882:101–130 York: Springer-Verlag; 1988
3. Kadyi H. Uber die Blutgefäß e des Men sch lich en Rü cken m arkes. Lem berg: 11. Lasjau nias PL, Berenstein A, Raybaud C. Surgical Neu roangiography. Ber-
Gubr yn ow icz u Sch m idt; 1889 lin ; New York: Springer-Verlag; 1987
4. Djin djian R. Angiography of th e spin al cord. In : Hu rth M, ed. Angiography 12. Lasjau n ias PL, Beren stein A, Ter Br ugge K. Su rgical Neu roangiograp hy,
of th e Spin al Cord. Balt im ore: Universit y Park Press; 1970:482 2n d ed. Berlin ; New York: Springer; 2001
5. Lazor th es G, Gou aze A, Djin djian R. Vascularizaion et path ologie vascu - 13. Lasjaun ias P, Vallee B, Person H, Ter Brugge K, Ch iu M. Th e lateral spin al
laire de la m oelle épin ière. Masson , Paris; 1973 ar ter y of th e upper cer vical spin al cord. An atom y, n orm al variat ion s, and
6. Dop p m an JL, Di Ch iro G, Om m aya AK. Percu t an eou s em bolizat ion of angiograph ic aspect s. J Neu rosurg 1985;63:235–241
sp in al cord ar terioven ou s m alform at ion s. J Neu rosu rg 1971;34:48–55 14. Siclari F, Burger IM, Fasel JH, Gailloud P. Developm en t al an atom y of th e
7. Djin djian R, Merlan d JJ, Djin djian M, Houdar t R. [Em bolizat ion in th e dist al ver tebral ar ter y in relat ion sh ip to varian t s of th e posterior an d lat-
t reat m en t of m edullar y ar terioven ous m alform at ions in 38 cases (au- eral spin al ar terial system s. AJNR Am J Neuroradiol 2007;28:1185–1190
th or’s t ran sl)]. Neu roradiology 1978;16:428–429 15. Bat son OV. The ver tebral system of vein s as a m ean s for can cer dissem in a-
8. Djindjian R. Angiography in angiom as of the spinal cord. In: Pia HW, Djind- t ion . Prog Clin Can cer 1967;3:1–18
jian R eds. Spin al Angiom as: Advan ces in Diagn osis an d Th erapy. Berlin : 16. Sh ap iro M. [Cerebrosp in al n eu rovascu lar in form at ion sou rce]. 2012.
Springer; 1978:98–136 w w w.n euroangio.org

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7 Cerebrovascular Physiology
Jens Bjerregaard and Richard A. Jaffe

Th is ch apter p resen t s a con cise yet com p reh en sive review of First developed in th e early 1980s, t ran scran ial Doppler ult ra-
cerebrovascular physiology an d clin ically useful assessm en t tech - son ography is clin ically accessible, con t in u ou s, an d n on invasive.
niques. The chapter covers basic prin ciples that govern the brain’s How ever, t h e u se of t ran scran ial Dop p ler u lt rason ograp hy is
vascu lar respon se to ch anging physiological con dit ion s in both con fin ed to large ar teries (e.g., m idd le cerebral ar ter y) an d lim -
h ealt hy an d inju red t issu e. Th e effect s of an est h et ic an d ot h er ited by relying on th e assu m pt ion th at th e velocit y of red blood
p h ar m acological agen t s t h at n eu rosu rgical p at ien t s are often cells an d th e volum e of blood flow are directly correlated. Th us,
exposed to are discu ssed . it m ay be difficu lt to differen t iate cerebral vasocon st rict ion or
vasospasm from act ual ch anges in CBF. If vessel diam eter an d
blood viscosit y are con stan t , th en m ore th an a 60% decrease in
velocit y in an esth et ized pat ien ts m ay be associated w ith a CBF
■ Cerebral Metabolism and Blood Flow < 20 m L/100 g/m in .4 Tran scran ial Dopp ler ult rason ography also
can be u sed to est im ate th e u p per an d low er lim it s of au toregu -
Normal Values and Measurement of Cerebral
lat ion an d to est ablish th e m ean ar terial pressure below w h ich
Blood Flow CBF ceases.5
Th e brain delicately balan ces it s en ergy su p p ly an d dem an d. At Am ong th e first approach es to quan t ifying CBF are m olecule-
~ 2% of body w eigh t , th e brain h as n o sign ifican t en ergy stores, t racin g tech n iqu es. Th ese tech n iqu es involve follow in g eit h er
but it h as a ver y h igh relat ive en ergy requ irem en t . Th e brain con - t h e d ist r ibu t ion of t racer m olecu les (e.g., injected or in h aled
su m es 20% of th e en t ire body’s basal oxygen requ irem en t an d xen on ) or t h e w ash -in /w ash -ou t cu r ves of th ose t racer m ole-
25% of tot al glu cose con su m pt ion at rest . To m eet its en ergy de- cules (Fig. 7.1). For est im at ing global but n ot region al CBF, th ese
m an ds, th e brain receives on ly 15% of th e rest ing cardiac out put , tech n iques rely on th e Ket y-Sch m idt m eth od. Th e ext racran ial
or ~ 750 m L/m in . Th e brain requires en ergy for both basal an d blood su pplying an d ret urn ing from th e brain is sam pled to m ea-
fu n ct ion al pu rp oses. Basal en ergy m ain tain s cellu lar in tegrit y— su re t h e flow -related ch ange in ar ter ioven ou s con cen t rat ion s
ion ic gradien t s an d oth er basic cellu lar fu n ct ion s. Fu n ct ion al of an in er t t racer. Th is m eth od requires periph eral ar ter y an d
en ergy con su m pt ion (60 to 70% of th e brain’s tot al en ergy re- cen t ral ven ou s access. Con sequen tly, it is cum bersom e, m aking
quirem en t) is u sed for h igh er level n eu ron al act ivit ies, in clu ding it difficult to assess dyn am ic ch anges in blood flow adequ ately
gen erat ion an d propagat ion of act ion poten t ials an d n eurot ran s- w ith in a clin ically useful t im efram e. PET an d fMRI are n on inva-
m it ter syn th esis, release, an d reupt ake. sive im aging tech n iqu es th at requ ire costly, com plex equ ipm en t .
In n or m al aw ake h u m an s, global cerebral blood flow (CBF), Th eir exp en se lim it s t h eir clin ical ap p licat ion s. How ever, t h ese
com posed of both gray an d w h ite m at ter blood flow s, is 50 m L/ m et h od s allow clin ician s to easily cor relate p hysiological dat a
100 g/m in , an d th e m etabolic rate of oxygen (CMRO2 ) is ~ 3.5 m L w ith an atom ic st r uct ural in form at ion . For n ow, th ese tech n iques
O2 /100 g/m in .1 Gray m at ter flow is ~ 70 to 80 m L/100 g/m in u te, can n ot be u sed in t raoperat ively, but im proving tech n ology m ay
w h ereas w h ite m at ter flow is on ly 15 to 20 m L/100 g/m in u te.2 ch ange th at in th e fu t u re.
W h ile CBF regu lat ion p rim arily occu rs in t h e m icrocircu lat ion at Magn et ic reson an ce im aging (MRI), PET, an d older m olecu lar
th e level of th e p ial an d p en et rat ing ar terioles, th ere is eviden ce t racer tech n iqu es are equ ally accu rate.6 Th e range of CBF valu es
to suggest th at th e larger cerebral ar teries con t ribu te as w ell.3 obtain ed w h en invest igators com pared a variet y of MRI an d PET
tech n iques on th e sam e h ealthy volu n teers h igh ligh t s th e vari-
abilit y to be expected am ong in dividuals an d m easurem en t tech -
Measuring Cerebral Blood Flow n iques.7 Alt h ough all m eth odologies est im ate th e average CBF
No clin ically relevan t gold st an dard for m easu ring CBF exist s. close to th e often -cited 50 m L/100 g/m in , th e values can deviate
Com paring tech n iqu es an d devices is d ifficu lt becau se th eir in - by as m uch as 50%.
vasiven ess varies as do th e t im e an d equipm en t required. Th at Bot h p er ip h eral an d CBF can be visu alized w it h ICG vid eo
said , clin ician s can est im ate CBF w it h t ran scran ial Dop p ler u l- angiography. Th e ICG m olecu le, w h ich em it s n ear-in frared fluo-
t rason ograp hy, m olecu le t racing, posit ron em ission tom ography rescence in the presence of near-infrared light, is used intraopera-
(PET), fun ct ion al m agn et ic reson an ce im aging (fMRI), in docya- tively to qualitat ively assess blood flow during cerebral vascular
n in e green (ICG) video angiograp hy, th erm al diffusion , an d oth er p roced u res, in clu d ing ext racran ial-to-in t racran ial byp ass for
indirect m easurem ent techniques (Table 7.1). Many invasive tech - p at ien t s w ith m oyam oya disease 8 (Fig. 7.2). Invest igators h ave
n iques, in cluding th e radioact ive m icrosph ere tech n ique or th e validated this technique by com paring it to digital subtraction an -
hydrogen clearan ce m eth od, are rest ricted to an im al laborator y giography an d com puted tom ography (CT) angiography in th ese
exp erim en t s. p roced u res.9 ICG vid eo an giograp hy p rovid es qu alit at ive focal

105

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106 I Development, Anatomy, and Physiology of the Central Nervous System

Table 7.1 Comparison of Methodologies for Measuring Cerebral Blood Flow

Repeat
Relative Measurement
Methodology Cost Resolution Time Scale possible Invasiveness Tracer Radiation

Ket y-Schmidt + Hemispheric Intermediate Yes Jugular puncture N2 No


133 Xe
Yes
83 Kr Yes
AVDO2 + Hemispheric Short Yes Jugular puncture N/A No
IV 133 Xenon + 3–4 cm Interm ediate Yes IV 133 Xe Yes
cortical
PET +++++ < 1 cm, 3D Long Limited IV Positron emit ters Yes
fMRI +++ < 1 cm, 3D Long Limited IV contrast Magnetic
Transcranial Doppler + Hemispheric Short Yes No N/A Ultrasound
ultrasonography
ICG videography + <1 cm Short Yes No Indocyanine green Fluorescence
Abbreviations: AVDO2 , arteriovenous oxygen content difference; fMRI, functional m agnetic resonance imaging; ICG, indocyanine green; IV, intravenous; PET, positron
em ission tom ography; 3D, three-dim ensional.
Source: Adapted from Cot trell JE, Young WL. Cot trell and Young’s Neuroanesthesia, 5th ed. Philadelphia: Mosby/ Elsevier; 2010.

a b

c d

Fig. 7.1a–d Post-acetazolam ide xenon–computed tom ography (Xe-CT) The perfusion index scale is shown. Note that lower perfusion index num -
perfusion scans from one m oyam oya patient at t wo levels. (a,b) Severely bers (shades of blue) correspond to higher levels of perfusion. (Courtesy of
reduced perfusion in watershed areas preoperatively. (c,d) Im ages ac- G. K. Steinberg, MD, PhD.)
quired 1 year following bilateral extracranial to intracranial (EC to IC) bypass
surgeries, and dem onstrate a m arked improvem ent in cerebral blood flow.

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7 Cerebrovascular Physiology 107
Fig. 7.2a–c (a) Photographs of intraoperative cortical
microvasculature (top) and corresponding indocyanine
green (ICG) video angiogram s (bot tom ) for norm al con-
trol patient, a patient with atherosclerotic vascular dis-
ease (ACVD), and a patient with m oyam oya disease
(MMD). (b) ICG video angiogram and (c) corresponding
intraoperative photograph after EC to IC bypass surgery.
(a: Reprinted from Czabanka M, Peña-Tapia P, Schubert
GA, Woit zik J, Vajkoczy P, Schm iedek P. Characterization
of cortical m icrovascularization in adult m oyam oya dis-
ease. Stroke 2008;39(6):1703–1709. b,c: Courtesy of G. K.
Steinberg.)

in form at ion about CBF, bu t th e tech n iqu e h as yet to be adapted ret rograde can n u lat ion of th e in tern al jugu lar vein . Based on it s
for assessing region al or global perfu sion . oxim et r y dat a, clin ician s can m ake global in feren ces abou t th e
Cerebral blood flow can be est im ated u sing jugu lar bu lb ox- balan ce bet w een CBF su p p ly an d d em an d . To obt ain region al
im et r y, cerebral oxim et r y, th erm al diffusion , an d n ear-in frared in form at ion , a cerebral oxim et r y probe (e.g., Licox ®, In tegra Life-
spect roscopy, all of w h ich p rovide som e in form at ion abou t th e Scien ces, Rat ingen , Germ any) can be in ser ted directly in to brain
adequacy of CBF. Jugular bulb oxim et r y is invasive; it requires t issue to m easu re t issu e oxygen p ar t ial pressure at th e in ser t ion

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108 I Development, Anatomy, and Physiology of the Central Nervous System

Fig. 7.3 Illustration of a near-infrared spectroscopy system (INVOS Sys- By m easuring absorption ratios at m ultiple wavelengths and by at tem pt-
tem , Som anetics, Troy, MI). The basic near-infrared spectroscopy setup ing to subtract the shallow tissue contribution, oxygenation can be esti-
consist s of a light em it ter and t wo or m ore detectors. In theory, the light m ated. Although, the usefulness of this estim ate is lim ited by the inabilit y
reaches the detectors after passing prim arily through shallow tissues (short to fully compensate for the variable signal contam ination caused by over-
path length) or through both shallow and deep tissues (long path length). lying tissues. (Courtesy of Barrow Neurological Institute.)

site. How ever, th is probe is an invasive an d relat ively im pract ical Chemical Mediators of Cerebral Vascular Tone
altern at ive in m ost cen ters.
Nit ric oxide (NO), en doth elin , an d oth er ch em icals m ediate cere-
A differen t , yet equally invasivean d t raum at ic, device is th e
bral vascular ton e th rough com plex processes an d path w ays th at
Hem edex ® cerebral perfu sion probe (Hem edex, In c., Cam bridge,
w e h ave on ly just recen tly st arted to un derstan d (Fig. 7.4). NO,
MA), w h ich relies on th erm al diffusion tech n ology to m easure
a w ell-described m ediator of cerebral vascu lar ton e, operates by
local CBF. As w ith t issu e oxim et r y, it m ay h elp clin ician s to opt i-
com p lex m ech an ism s, involving in teract ion s w ith m any oth er
m ize perfusion m an agem en t in pat ien t s w ith a t raum at ic brain
m ediators. W h en NO h as been syn th esized by en doth elial cells,
inju r y by iden t ifying th e adequ acy of CBF an d au toregulator y
a cyclic gu an osin e m on oph osph ate–m ediated m ech an ism causes
m ech an ism s.10 Near-in frared spect roscopy (NIRS), a developing
NO to in teract w ith th e vascu lar sm oot h m u scle, cau sing relax-
tech n ology, p rovides a m ore region al an d n on invasive view of
at ion . W hether NO plays a role in the vasodilator y effects of CO2 is
tissue oxygenation in the frontal cortex (Fig. 7.3) or oth er tissues.
uncertain. How ever, investigators found that NO synthase (NOS)
Un for t u n ately, NIRS readings can be con t am in ated by th e overly-
m ay be suppressed during subarachnoid hem orrhage (SAH), con-
ing t issues (e.g., scalp , sku ll, cerebrosp in al flu id [CSF]), m aking
tribut ing to th e occu rren ce of vasospasm .12
dat a in terpret at ion difficu lt . How ever, lim ited, em erging, clin ical
Th e exact m ech an ism is u n cert ain ; h ow ever, suppressed NOS
eviden ce su ppor ts using NIRS in both th e cardiovascu lar an d
appears to sh ift th e balan ce of vascular ton e tow ard vasocon -
n eu rosu rgical pat ien t p opu lat ion s.11
st rict ion th rough th e effect s of m ediators su ch as en doth elin an d
cer t ain p rost aglan d in s. Han sen -Sch w ar t z 13 obser ved u p regu la-
t ion of en d ot h elin receptors in cerebral ar ter ies after SAH, p ro -
vid in g ad d it ion al evid en ce for a sh ift in g balan ce. Nicard ip in e
■ Cerebral Functional Activation ap pears able to block th e en doth elin com pon en t of vasospasm
du ring SAH th rough its calciu m -ch an n el blockade, th u s p reven t-
Variations in Regional Blood Flow in g t h e calciu m in flu x cr it ical to en d ot h elin’s m ech an ism of
Alth ough global values for blood flow an d m etabolism can be act ion .14
st able, region al CBF can var y greatly as a resu lt of ch anges in p ar- Vasoact ive pept ides, su ch as subst an ce P an d n eu rokin in A,
t ial p ressu res of ar terial oxygen (PaO2 ) an d ar terial carbon diox- can also be vasodilators in th e cerebral vasculat u re. A vasoact ive
ide (PaCO2 ) in an d local p erfu sion pressu re. Becau se th e brain peptide im plicated in the pathophysiology of m igraines, calcitonin
lacks sign ifican t en ergy stores, th ese ch anges in region al dem an d gene-related peptide, has also been show n in rats to be an im por-
depend on autoregulat ion, a rapid com pen sator y supply–dem and tant m ediator of au toregulation during periods of hypotension.15
m atching m echanism . Autoregulatory processes help regulate CBF Other cellular m essengers—carbon m onoxide (CO) and hydro-
to m atch dem an d over a range of perfusion pressures, th ereby gen su lfide (H2 S)—h ave been im plicated in m ediat ing vasodila-
preven t ing isch em ia. Th ey also h elp avoid th e risks of overp erfu - t ion . CO is a p rodu ct of h em e d egradat ion by h em e oxygen ase
sion , in cluding h em orrh age an d edem a. (HO), w h ose isoform , HO-2, is presen t at baselin e in brain t is-

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7 Cerebrovascular Physiology 109

Fig. 7.4 Cerebral blood flow (CBF) is partially regulated by the effect of noic acid (20-HETE) and the vasodilating epoxyeicosatrienoic acids (EETs).
glutam ate on astrocytes and neurons. The direct effect of glutam ate is in- Endothelial NOS (eNOS) can be activated by flow-induced shear stress or
creased levels of Ca 2+, which result in the form ation of nitric oxide (NO) and by acet ylcholine (Ach). It produces vasodilating NO, which also has an in-
various arachidonic acid–derived m essengers. NO contributes to vascular hibitory effect on 20-HETE in arteriole smooth muscle. AA, arachidonic acid;
tone both directly and by interacting with the arachidonic acid–derived cGMP, cyclic guanosine m onophosphate; PLA2 , phospholipase A2 , PGE2 ,
m essengers. NO produced by nitric oxide synthase (NOS) inhibits (dashed prostaglandin E2 . (Courtesy of Barrow Neurological Institute.)
lines) the production of both the vasoconstricting 20-hydroxyeicosatetrae-

su e.16 W h en isch em ia, acute hypoxia, or epilept ic seizu res occur, out n u m ber n euron s in th e cortex an d h elp to m ain tain an d con -
HO-2–m ediated CO rap idly in creases, con t ribu t ing to in creased t rol cerebral h om eost asis. Ast rocyte effect s on n eu ron al cells,
CBF. Alt h ough t h e effect is rap id , d ilat ion is p rogressively lost th e blood–brain barrier (BBB), an d sign al t ran sm ission are w ell
d u e to a CO-m ediated in h ibitor y effect on NOS, resu lt ing in a described . Koeh ler et al19 ch aracterized th e role of ast rocytes in
t ran sien t , sh or t-term p rotect ive effect . Th e prod u ct ion of H2 S m ain tain ing cerebral vascular ton e. A key m ediator of cerebral
appears to be lin ked to th e presen ce of NO. Its site of act ion is the vascu lar ton e app ears to be in t racellular levels of Ca 2+ in th e ter-
ad en osin e t r ip h osp h ate (ATP)-sen sit ive K+ ch an n els. In creased m in al p rocesses of ast rocytes (i.e., th e en d feet) t h at cover th e
K+ ou tflow hyp erp olarizes t h e cellu lar m em bran e, relaxing th e m ajorit y of the cerebral m icrocirculation. Furtherm ore, data sug-
vascu lar sm ooth m uscle.17 H2 S also m ay p lay a role in th e prolif- gest th at ast rocytes can be st im ulated to release CO in respon se
erat ion an d apoptosis of vascular sm ooth m u scle cells.18 to in creased aden osin e diph osph ate (ADP) an d glutam ate levels,
an effect th at requires th e con curren t presen ce of NO.16 CO m ay
Astrocytes as Mediators of Cerebral be par t icularly im por tan t for cerebrovascu lar regu lat ion in n ew -
born s. Becau se experim en ts h ave m ostly been con du cted in pig-
Vascular Tone let brain s, th e role of CO in adult h um an brain s is less cer t ain .19
Glial cells, in clu ding ast rocytes, are kn ow n to in fluen ce cerebral To tolerate isch em ic con dit ion s, ast rocytes appear to h ave
vascu lar ton e. Ast rocytes, th e brain’s m ost com m on glial cells, protect ive adapt at ion s: a low er den sit y of ion ic ch an n els th an

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110 I Development, Anatomy, and Physiology of the Central Nervous System

regular n euron s result ing in low er en ergy requ irem en t s to m ain - t ive effect on CMR. Th ir t y percen t of rest ing CMRO2 rep resen t s
tain cellular integrit y and relatively high glycogen stores that m ay basal m etabolism , the absolute m inim um level obtainable by phar-
be protect ive in n ear-isch em ic con dit ion s.20 How ever, during m acological in h ibit ion of cerebral fu n ct ion at n orm oth erm ia.21
com plete isch em ia, th e ben efit of glycogen stores m ay be m oot Th is poin t rep resen t s th e m in im u m level of en ergy requ ired to
du e to th e dam aging effect s of lactate p rodu ced du ring an aerobic m ain tain basic cellular fun ct ion s, in cluding ion t ran sport pu m ps
glycolysis. Th is process is sim ilar to th at respon sible for cellu lar u sed to m ain t ain vit al t ran sm em bran e ion gradien t s. Th e m et a-
injur y in st roke p at ien t s during hyperglycem ia. bolic effect described above also applies to oth er con dit ion s (e.g.,
St udies suggest th at th e sym p ath et ic n er vou s system directly hypoth erm ia) an d an esth et ic agen ts (e.g., propofol) th at can in -
in flu en ces CBF. It ap p ears to p rovide a p rotect ive m ech an ism h ibit an d sup press EEG act ivit y (Fig. 7.5).
by w h ich in creases in p er fu sion p ressu re are at ten u ated . Th is At t yp ical d oses, th e effect of op ioid s on CBF an d CMR is lim -
m ech an ism is m ediated by large arteries an d arterioles in re- ited an d ap p ears largely related to t h e effect s of ot h er con cu r-
spon se to sym path et ic st im ulat ion .3 Th e sign ifican ce of n euro- ren t ly u sed an est h et ics.22 In sp on t an eou sly breat h ing p at ien t s,
gen ic vasom otor m odulat ion is n ot yet clear, bu t it ap pears to be t h e resp irator y d ep ressan t effect s of op ioid s m ay in d irect ly in -
on e com pon en t of a com plex system design ed to m ain tain ade- crease CBF d u e to hyp ercap n ia. Th e ben efit of op ioid s in bal-
qu ate cerebral perfu sion . an ced an esth esia is th eir blun t ing of th e sym path et ic respon se to
su rgical st im u lat ion an d th eir h elp in stabilizing h em odyn am ic
con dit ion s.
At con cen t rat ion s approach ing on e m in im um alveolar con -
cen t rat ion or above, in h alat ion al agen ts like isoflu ran e, sevoflu-
■ Pharmacologic Effects on rane, an d desfluran e produce a decoupling effect in w h ich further
Cerebrovascular Physiology m etabolic inhibition paradoxically increases CBF, an effect not ob-
ser ved w ith int ravenous an esthet ics. PET dem on st rates that this
Anesthetics vasodilator y effect varies region ally in h ealthy in dividu als, rep -
In th e fin ely balan ced an d sen sit ive m ilieu of th e cerebral vascu - resenting a potential hazard to patients w ith com prom ised intra-
lat u re, th e effects of p h arm acological agen t s on CBF, in t racran ial cran ial com plian ce.23 By using in h alat ion al agen ts like isofluran e
pressu re (ICP), an d cerebral m etabolic rate (CMR) can be p ro- at h igh con cen t rat ion s (e.g., 2 m in im u m alveolar con cen t rat ion ),
fou n d. Pat ien ts rarely receive on ly on e an esth et ic-related dr ug. on e can ach ieve a CMR plateau effect after reach ing a flat ten ed
Con sequ en t ly, clin ician s m u st con sid er an d u n d erst an d th e col- EEG sim ilar to th at associated w ith in t raven ous an esth et ics.24
lect ive in flu en ce of all an est h et ic in ter ven t ion s—in t raven ou s Using n it rous oxide (N2 O) in n eurosurger y is con t roversial. In
an est h et ics, op ioid s, in h alat ion al agen t s, an d m u scle rela xan t s som e set t ings it ap p ears to in crease CBF, CMR, an d ICP, alth ough
(Table 7.2). th e exten t dep en ds on w h at oth er agen t s h ave been coadm in is-
In creasing n euron al in h ibit ion w ith escalat ing doses of barbi- tered (e.g., isofluran e, sevofluran e, or propofol).25,26 Mild hyper-
t u rates is w ell ch aracterized. For exam ple, in creased th iop en tal ven t ilat ion (hyp ocap n ia), h ow ever, ap p ears to at ten u ate t h ese
doses cau se a CBF-cou p led decrease in m etabolism , un t il, fin ally, in creases, even in p at ien t s w it h a n eu rologic inju r y.27,28 In t h e
th e elect roen ceph alograph ic (EEG) w aveform is supp ressed, an d even t of a ven ou s air em bolism , con t in u ed ad m in ist rat ion of
bu rst su p p ression is ach ieved . At th is p oin t , t h e m easu red m e- N2 O w orsen s th e physiological effects by cau sing th e t rapped air
t abolism level is ~ 30% of th at fou n d in an aw ake p erson . Any to expan d. It w as th ough t th at a sim ilar process m igh t w orsen
fu r th er in crease in th iop en t al level h as n o m easu rable, p rotec- pn eu m oceph alu s du ring cran iotom y if N2 O w as n ot discon t in -

Table 7.2 Effect of Anesthetic Agents on Cerebral Physiology

CO2 CSF
Anesthetic Agent CBF ICP CMRO2 Autoregulation Reactivity Production/Absorption

Thiopental _ _ _ No change No change No change


Etomidate _ _ _ No change No change No change
Propofol _ _ _ No change No change No change
Ketamine a + + + No change No change Decrease absorption
Benzodiazepines _ _ _ No change No change No change
Opioids (IPPV) No change No change No change No change No change Increase absorption
Opioids (SV) + + No change No change No change Increase absorption
Inhalational agents
Isoflurane b + + _ Impaired No change Decrease production and
increase absorption
Sevoflurane b + + _ Impaired No change Decrease production
Desflurane + + _ Impaired No change No change
Nitrous oxide + + _ No change No change No change
Abbreviations: CBF, cerebral blood flow; CMR, cerebral m etabolic rate; CSF, cerebrospinal fluid; ICP, intracranial pressure.
Source: Adapted from Garner A, Hirsch N. Pharmacological and pathological modulation of cerebral physiology. Anaesth Intensive Care Med 2007;8:413–417.
a When administered as sole agent to spontaneously breathing person.

b At lower concentrations, CBF is decreased.

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7 Cerebrovascular Physiology 111

cal eviden ce is lacking, m any basic scien ce an d an im al st u dies


sh ow th at ket am in e decreases n eu rologic inju r y in hyp oxia, isch -
em ia, an d m ech an ical injur y m odels.
Non depolarizing neurom uscular blockers do not have a m arked
direct effect on CBF or CMR (Table 7.3). Th e com m on ly used
n on depolarizing n eurom uscular blockers agen ts—rocuron ium ,
vecuron ium , pan curon ium , an d cis-at racurium —produ ce n o sig-
n ifican t h ist am in e release an d th us avoid th e in creased CBF seen
w ith older agen ts (e.g., d-t u bocurarin e).
Th e on ly dep olarizing n eu rom u scu lar blocking agen t in u se
today, succinylch olin e, in creases both CBF an d ICP w h en u sed in
procedu res for elect ive n eu rosu rgical excision of brain t u m ors.36
Th is fin ding is con sisten t w ith th ose in an im al st u dies, in w h ich
t h is effect is blu n ted w h en su ccinylch olin e ad m in ist rat ion is
p reced ed by a sm all (d efascicu lat ing) d ose of n on d ep olar izin g
n eu rom u scu lar blockers.37,38 How ever, in brain inju r y p at ien t s
w it h in creased ICP, su ccinylch olin e d oes n ot ap p ear to fu r t h er
in crease ICP.39

■ Other Drugs
Osm ot ic agen t s, catech olam in es, an d in dom eth acin also h ave
im por t an t effects on cerebrovascu lar physiology.
Man n itol an d hyp er ton ic salin e are com m on osm ot ic agen t s
u sed to redu ce elevated ICP an d to im prove surgical exposure
Fig. 7.5 The effect that different levels of consciousness have on the ce- con d it ion s. Man n itol decreases brain w ater con ten t rath er th an
rebral m etabolic requirem ent. At norm otherm ia, 30%of baseline metabolic
cerebral blood volum e.40 In fact, a rapid infusion of m ann itol could
rate m arks the lowest level of m etabolism that can be reached with a bar-
biturate com a. Hypotherm ia is required to decrease the cell’s energy utili- t ran sien tly h ave d et rim en tal effect s on ICP by in creasing cere-
zation further. (Modified from Astrup J, Sørensen PM, Sørensen HR. Oxygen bral blood volum e w h ile decreasing cerebral perfu sion pressure.
and glucose consumption related to Na-K transport in canine brain. Stroke If appropriately adm in istered, m an n itol can im prove cerebral
1981;12:726; and Astrup J, Sørensen PM, Sørensen HR. Inhibition of cere- perfu sion . In p at ien ts w ith a TBI, m an n itol n ot on ly decreased
bral oxygen and glucose consumption in the dog by hypotherm ia, pento- ICP, bu t it also m arkedly im proved blood flow to hypoperfused
barbital and lidocaine. Anesthesiology 1981;55:263.)
brain regions.41 Although large random ized control trials are lack-
ing, th e literat ure suggest s th at hyperton ic salin e is as effect ive
as m an n itol in low ering ICP42 an d m ore ben eficial th an m an n itol
for avoiding th e diu resis th at m ay follow m an n itol adm in ist ra-
u ed before th e du ra w as closed. How ever, a ran dom ized st udy t ion . If hyp erton ic salin e is u sed, elect rolytes m u st be m on itored
sh ow ed th at th e con t in u ed u se of N2 O after dural closure did n ot closely to avoid too rapid a rise in serum sodiu m .
in crease ICP.29 Prolonged exposu re to N2 O h as been im plicated Catech olam in es (e.g., p h enylep h rin e) are com m on ly u sed in
in an in creased in ciden ce of n au sea an d vom it ing as w ell as in a crit ically ill pat ien ts to m ain tain h em odyn am ic stabilit y an d in
clin ically sign ifican t vit am in B12 d eficien cy, w h ich cou ld lead to n eu rosurgical pat ien ts to augm en t cerebral perfusion pressure
m yelopathy.30 to im prove CBF. Alph a-adrenergic receptors are presen t in pial
Early st u dies of ket am in e suggested it s u se sh ou ld be con t ra- ar teries an d cerebral ar terioles. Ph enyleph rin e, n orepin eph rin e,
in dicated in n eu rosu rgical pat ien ts. Th ese st u dies dem on st rated an d dopam in e all in crease CBF in TBI pat ien t s. How ever, n orepi-
t h at ket am in e in creased CBF, ICP, an d CMR w h en given alon e n ep h rin e ap pears to do so m ost reliably, w ith a m ore favorable
in spon t an eously ven t ilat ing p at ien t s.31,32 Th ese effect s are n ow effect on region al cerebral oxygen at ion .43
th ough t to h ave been th e resu lt of a con cu rren t rise in PaCO2 . In d om et h acin abolish es t h e cerebrovascu lar resp on se to hy-
How ever, th e st igm a h as kept ketam in e from being w idely u sed p ercapn ia an d in duces vasocon st rict ion .44 Th e effect resu lt s from
in t raum at ic brain injur y (TBI) p at ien t s, desp ite m ore recen t evi- d irect in h ibit ion of p h osp h olip ase, p reven t ing t h e for m at ion of
den ce sh ow ing som e ben efit . For exam ple, invest igators h ave p rost aglan d in s (PGs), in clu d ing PGE2 . Alt h ough in d om et h acin
sh ow n that ketam in e m aintains cerebral perfusion pressure (CPP) appears to decrease ICP an d CBF w h ile im proving cerebral perfu-
w h ile it low ers ICP in ven t ilated an d sedated TBI pat ien ts.33,34 sion , n o large ran dom ized con t rol t rials h ave been con du cted to
Ketam in e’s favorable effect in pat ien t s w ith com prom ised in t ra- su p port it s u se in TBI p at ien t s.45 In addit ion to decreasing ICP
cran ial elastan ce is best ach ieved w ith sedat ion an d m ech an ical after a sin gle 30-m g d ose, in dom eth acin also act s as an an t i-
ven t ilat ion .35 As an N-m ethyl-D-asp ar t ate receptor an t agon ist , pyret ic, p oten t ially fu r t h er ben efit in g t h e p at ien t w it h n eu ro -
ket am in e m ay h ave sign ifican t n eu rop rotect ive p rop ert ies (Fig. logic inju r y.46 Oth er n on steroidal an t i-in flam m ator y dr ugs (e.g.,
7.6); it blocks glu t am ate release an d p reven t s fu r th er cellu lar in - ibu p rofen an d asp ir in ) d o n ot ap p ear to red u ce CBF.47,48 Th ese
jur y caused by glutam ate-in duced excitotoxicit y.35 Although clin i- ap p aren t ben efit s sh ou ld be balan ced cau t iou sly again st t h e

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112 I Development, Anatomy, and Physiology of the Central Nervous System

Fig. 7.6 Pharm acological effects reported for racem ic and S(+)-ketamine, of transcription factors is reduced (4). Proteins involved in apoptosis are
which are presum ed to be relevant for neuroprotection. After the onset less activated, which is associated with less fragm entation of DNA (5). Syn-
of brain injury, blockade of excessive stim ulation of N-m ethyl-D-aspartate aptic proteins are bet ter preserved (6), and the expression of growth pro-
(NMDA) receptors by ketam ine reduces Ca 2+ influx through the receptor teins (7) indicating regeneration in adult neurons is enhanced. Finally, the
channel (1). This reduction at tenuates supraphysiological increases in the prevention of pathological amplification of NMDA-receptor signaling results
assem bly and interaction of NMDA-receptor subunits, postsynaptic densit y in increased cellular survival, preserved cellular and synaptic integrit y, and
proteins, and other intracellular signaling system s such as protein kinases regenerative efforts (8). *Superiorit y of/effects induced by S(+)-ketam ine
(2). Thus, several kinase transduction cascades becom e less activated. The only. (Reprinted from Him m elseher S, Durieux ME. Revising a dogm a: ket-
result is improved preservation of m etabolism and m aintenance of the m i- am ine for patients with neurological injury? Anesth Analg 2005;101:
tochondrial transm embrane potential (3). In turn, pathological activation 524–534.)

Table 7.3 Summary of Neuromuscular Blocking Agents, Their Autonomic Effect, and Histamine Release

Histamine
Drug Class Autonomic Effect Release Notes

Succinylcholine Depolarizing Stim ulates autonom ic ganglia Slight Short acting, fast onset
and m uscarinic receptors
Cisatracurium Nondepolarizing None Slight Metabolism independent of
benzylisoquinolium renal/hepatic function
neuromuscular blocker
d-Tubocurarine Nondepolarizing Blocks autonom ic ganglia Moderate No longer in clinical use in the
benzylisoquinolium United States
neuromuscular blocker
Vecuronium Nondepolarizing steroidal None None Intermediate duration, slow
neuromuscular blocker onset
Pancuronium Nondepolarizing steroidal Blocks cardiac m uscarinic None Long acting
neuromuscular blocker receptors
Rocuronium Nondepolarizing steroidal None None Intermediate duration, fast
neurom uscular blocker onset

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7 Cerebrovascular Physiology 113

p oten t ial n egat ive effect s of in d om et h acin , in clu d ing w orsen -


in g ren al inju r y an d in creased risk of bleeding.

■ Effect of Temperature
Low ering body tem p erat u re by 1°C decreases CMRO2 ~ 7%. Al-
th ough an esth et ic agen t s redu ce on ly th e fu n ct ion al com p on en t
of n euron al en ergy ut ilizat ion , hypoth erm ia fu r th er decreases
CMR by decreasing th e basal en ergy requ irem en t . Th e ben eficial
Fig. 7.7 Estim ated segm ental cerebrovascular resistance. The resistance
effect s of d ecreased tem perat u re during isch em ia h ave been w ell through the long surface pial arteries is approxim ately the sam e as through
docum en ted in laborator y st u dies an d in p at ien ts w ith isch em ic the m uch shorter parenchym al penetrating arterioles. CW, Circle of Willis;
m yocardial injur y.49 How ever, the involved pathw ays are com plex, MCA, middle cerebral artery. (Reprinted from Carter LP, Spet zler RF, Ham il-
an d on ly recen tly has th e n at ure of th e un derlying m ech an ism s ton MG, eds. Neurovascular Surgery. New York: McGraw-Hill, 1995.)
com e to ligh t .50 See Ch apter 13 for a m ore detailed discussion of
in t raoperat ive hyp oth erm ia.
tan ce (Fig. 7.7). Norm oten sive pat ien ts h ave a m ean ar terial
Despite convin cing basic scien ce eviden ce, th e u se of hypo-
pressu re au toregu lator y range of 55 to 160 m m Hg, alth ough th e
therm ia rem ain s cont roversial in n eurosurgical practice. Evidence
exact low er an d u p per lim it s of au toregu lat ion rem ain con t ro-
for using m oderate to deep hypoth erm ia is m ost com pelling in
versial an d likely var y even am ong h ealthy people.54 Below th is
p at ien t s after ven t r icu lar fibr illat ion card iac ar rest .51 In d u cin g
range, blood flow decreases in a pressure-dependen t m anner, first
hypoth erm ia is also ben eficial in th e surgical t reat m en t of gian t
affect ing th e m ore vuln erable w atersh ed areas. In a h ealthy brain ,
an eur ysm s w h en circulator y arrest m ay be requ ired.52 How ever,
flow is con t rolled by arteriolar con st rict ion w h en the pressure
th e data are less con clu sive for pat ien ts w h o h ave h ad t raum at ic
rises an d by dilat ion w h en th e pressure falls. Au toregulat ion is a
brain or sp in e inju ries.
cru cial fun ct ion th at allow s com pen sat ion for variat ion s in pos-
t ure an d act ivit y. At th e h igh en d of th e au toregulat ion range,
approach ing 160 m m Hg, th e in creased blood flow can quickly
lead to th e form at ion of ed em a.
■ Perfusion Pressure, Blood Flow, In a diseased or t raum at ized brain , autoregulat ion m ay be
and Autoregulation lost , an d blood flow becom es pressu re-depen den t at all m ean
ar terial pressure levels. Th is loss can occur globally as in som e
Un derstan ding th e in terrelat ion sh ip bet w een ICP, CPP, an d auto-
cases of SAH or TBI, or it can occu r focally in th e su rrou n ding
regu lator y m ech an ism s is crit ical to m ain t ain ing favorable cere-
area of an in t racran ial lesion such as a brain t um or. In pat ien t s
bral physiological con dit ion s in th e n eu rosurgical pat ien t . CPP
w ith h ead inju r y, som e level of autoregulat ion can be restored
equ als m ean ar terial blood pressu re m in u s ICP or cen t ral ven ou s
w ith hyper ven t ilat ion .55
pressu re, depen ding on w h ich is greater. Becau se th e in t racra-
In a pat ien t w ith ch ron ic hyperten sion , th e vasculat ure com -
n ial space is rigid an d com pen sator y m ech an ism s are lim ited, an
pen sates, an d both th e h igh an d low er en d of th e m ean ar terial
addit ion to in t racran ial volu m e such as a m ass lesion , edem a, or
pressu re range sh ift s to th e righ t , inversely p rop or t ion al to th e
hydroceph alu s cau ses a n on lin ear in crease in ICP. Th e con cept
level of blood pressure control. With effective hypertension treat-
th at in t racran ial volu m e is fixed an d th at an in crease in any of it s
m en t , th e vasculat u re adapts an d th e au toregulator y range an d
con st it u en t s m u st be com pen sated by a m atch ing decrease in it s
blood p ressu re are n orm alized. Th e effect of an esth et ic dr ugs on
oth er con st it u en t s is referred to as th e Mon ro-Kellie doct rin e.
autoregulat ion is variable. In t raven ous agen ts such as propofol
an d opioids appear to preser ve autoregulat ion . How ever, h igh
Bridging Veins and Intracranial Pressure doses of volat ile an esth et ics h ave a decou pling effect th at abol-
ishes autoregu lat ion , resu lt ing in in creased CBF, despite decreas-
Br idgin g vein s are ord in ar ily op en , allow in g u n obst r u cted ve- ing m et abolic dem an ds.56
n ou s ou t flow . If ICP in creases, on e m igh t exp ect t h e vein s to
collapse, obst r u ct ing ou tflow an d adding to th e in t racran ial vol-
u m e. How ever, Yu et al53 dem on st rated th at bridging vein s do
n ot collapse; in fact , th ey dilate in respon se to in creased ICP. Th is ■ Environmental Effects on Cerebral
respon se suggest s th at ou tflow obst ruct ion occu rs in m ore dist al
d rain ing vein s. By in creasin g ICP, d ist al ven ou s ou t flow resis-
Blood Flow
t an ce in creases, w h ich p reven t s t h e br idging vein s from being Main t ain ing a PaO2 in th e n orm al range is alw ays ideal. How ever,
com p ressed an d obst r u cted . Th u s, t h e ou t flow from t h e h igh - m an ip u lat in g a p at ien t ’s PaCO2 can be on e of t h e few effect ive
pressu re in t racran ial ven ou s system to an area of low er p ressu re acute in ter ven t ion s available for th e t reat m en t of in creased ICP
is m ain tain ed. (Fig. 7.8).

Autoregulation PaCO2
Au toregu lat ion refers to th e brain’s abilit y to m ain t ain CBF over Ar terial CO2 part ial pressure can profoun dly affect CBF. In gen -
a range of perfu sion pressures by altering cerebrovascular resis- eral, for ever y 1 m m Hg ch ange in PaCO2 , CBF ch anges by ~ 2 m L/

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114 I Development, Anatomy, and Physiology of the Central Nervous System

Fig. 7.8 Effect of intracranial pressure (ICP), PaO2 , PaCO2 ,


and m ean arterial pressure (MAP) on cerebral blood flow. (Re-
printed from Hines RL, Marschall KE. Stoelting’s Anesthesia and
Coexisting Disease, 5th ed. Philadelphia: Saunders/ Elsevier,
2008. Copyright Elsevier.)

100 g/m in ute. An acute ch ange in PaCO2 from 40 to 20 m m Hg below 50 m m Hg, an aerobic m et abolism st ar t s an d CBF (an d
can decrease CBF by ~ 50%. W h en hyp ercap n ia is ext rem e an d cerebral blood volu m e) in creases dram at ically.
th e ar terioles reach th e poin t of m axim u m vasodilat ion , au to-
regu lat ion fails.
W h en CO2 rap idly diffu ses across th e BBB, vasoact ive effect s
are m ediated by pH ch anges in th e CSF surroun ding th e ar terio- ■ Cerebral Ischemia and Altered
lar w alls.57 Th is process is illu st rated by th e cerebral vasodilat ion
an d in creased CBF associated w ith hypercapn ic respirator y aci- Perfusion States
dosis. How ever, in pat ien ts w ith m etabolic acidosis, th is effect Th e com p lex cerebrovascu lar resp on se to isch em ia dep en d s on a
does n ot occu r becau se hydrogen ion s can n ot cross th e BBB. variety of factors: the m agnitude, duration, and location of an isch-
Rapidly decreasing the cerebral blood volum e of patien ts w ith em ic event; protective therapies applied before and after an event;
in creased ICP m ay be crit ical to th eir acu te m an agem en t. Hyper- an d th e effects of rapid rep erfusion after su rgical in ter ven t ion .
ven t ilat ing pat ien ts to low er th eir PaCO2 can rap idly d ecrease Th e m agn it u de an d du rat ion of isch em ia determ in e th e ex-
th eir CBF an d low er th eir ICP. In m ost pat ien t s th ese ben efit s are ten t of cellu lar dam age an d w h ich p rotect ive m ech an ism s are
lim ited by th e occu rren ce of cerebral isch em ia at PaCO2 levels of in it iated . For exam p le, in t h e p en u m bra zon e, com p en sator y
20 m m Hg or less as CBF falls below 25 m L/100 g/m in . Alth ough m ech an ism s con t rol th e balan ce bet w een ach ieving t im ely re-
hyper ven t ilat ion m ay be a lifesaving m easure in pat ien t s w ith perfu sion an d th e in it iat ion of ap optosis. In th e isch em ic region ,
crit ically elevated ICP, its rou t in e use is con t roversial58 an d prob - ar teriolar dilat ion occu rs, likely du e to in creasing aden osin e lev-
ably sh ou ld be m in im ized. els.59 Th en , w ith in m in u tes, ATP levels fall, affect ing th e abilit y of
The acute change in CBF caused by altering the PaCO2 is rapidly cells to properly m ain t ain crit ical Na +, K+, an d Ca 2+ ion gradien ts
attenuated by com pensatory m echanism s. Within 6 to 8 hours of th rough th eir ATP-depen den t ion ch an n els an d pum ps.
in st it ut ing hypocap n ia by hyper ven t ilat ion , th e bicarbon ate ion Clin ician s can t ake protect ive steps to low er en ergy require-
con cen t rat ion decreases an d th e pH of CSF an d CBF values ret u rn m en t s before an d during an isch em ic even t . For exam ple, th ey
to norm al. Thus, hyper ven tilation m ust be discontinued prom ptly can adm in ister an esth et ics at con cen t rat ion s th at resu lt in bu rst
to m in im ize rebou n d hyp erem ia an d in creased ICP. su p pression , in h ibit ing fu n ct ion al m etabolism an d redu cing en -
In areas of cerebral isch em ia, CO2 react ivit y is lost . An inverse ergy requ irem en t s to less t h an 50% of baselin e. Th ey also can in -
steal p h en om en on can th en occu r du ring hyp er ven t ilat ion . Th is du ce m ild to m oderate hypoth erm ia (30° to 33°C) to decrease
effect m ay in crease blood flow to th e isch em ic area as th e result basal m et abolic dem an d by 30 to 50%. By m odulat ing regulator y
of vasocon st rict ion in th e su rroun ding n orm al t issue. Conversely, cascades involved in BBB perm eabilit y an d gen e regu lat ion , hy-
w ith hypoventilation the vasodilator y effect of hypercapnia on the poth erm ia m ay offer addit ion al protect ion , even after inju r y h as
su rrou n ding t issu e m ay d ecrease th e blood flow to an already occurred.50
com prom ised isch em ic area. Patients w ith cerebrovascular insufficiency m ay develop areas
of low perfusion un able to ben efit from th e developm en t of col-
lateral vessels. Even t u ally, t h e focal blood flow redu ct ion ex-
Effect of PaO2 ceeds th e reser ve of th e collateral circulat ion . Th e pat ien t th en
Ar terial oxygen par t ial pressure h as lit tle effect on cerebrovascu- m ay develop sign s of isch em ia. Sim ilarly, in pat ien ts w ith a h igh -
lar ton e u n t il a fran k hyp oxic st ate develop s. On ce PaO2 decreases flow arterioven ous m alform at ion (AVM), blood flow in areas

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7 Cerebrovascular Physiology 115

su rrou n ding th e AVM can be com prom ised as a resu lt of a steal cerebral blood flow to an area oth er w ise ch ron ically adapted to
ph en om en on . a low perfusion state. Th e syn drom e often occurs in pat ien ts
W h en perfu sion is ret u rn ed to n orm al after su rgical in ter ven - w ith m oyam oya disease an d ath erosclerot ic occlusive cerebro-
t ion (e.g., carot id en darterectom y or h igh -flow AVM resect ion ), vascu lar disease 62 an d m ay be difficult to t reat .
hyp er p erfu sion syn d rom e (cerebral ed em a or even h em or-
rh age) m ay occu r.60 Spet zler an d colleagues 61 posited th e th eor y
of n orm al perfusion pressu re breakth rough , w h ich st ates th at
d esen sit ized ar ter ioles can n ot h an d le a su d den ret u r n to n or-
m al p er fu sion . Clin ically, t h e hyp er p er fu sion syn d rom e m an i-
■ Conclusion
fest s w it h a sign ifican t ip silateral h eadach e t h at m ay p rogress A th orough un derst an ding of cerebrovascular physiology is crit i-
to sign ifican t n eurologic sym ptom s as th e edem a w orsen s an d cal for th e care an d m an agem en t of pat ien t s w ith n eu rovascu lar
h em orrh age occurs. Th e syn drom e m ay occur after any n euro- disorders. Path ological st ates resu lt in alterat ion s of basic p hysi-
vascular surger y—including carotid endarterectom y, AVM, and ological param eters, an d th e n eurovascular team m ust be cogn i-
ext racranial to intracran ial (EC to IC) bypass surger y—that restores zan t of th ese alterat ion s to m in im ize m orbidit y in th e pat ien t .

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15. Hong KW, Pyo KM, Lee WS, Yu SS, Rh im BY. Pharm acological eviden ce t rous oxide for pat ien t s u n dergoing m ajor surger y: a ran dom ized con -
th at calciton in gen e-related pept ide is im plicated in cerebral autoregula- t rolled t rial. An esth esiology 2007;107:221–231
t ion . Am J Physiol 1994;266(1 Pt 2):H11–H16 31. Gard n er AE, Dan n em iller FJ, Dean D. In t racran ial cerebrosp in al flu id
16. Leffler CW, Parfenova H, Jaggar JH. Carbon m onoxide as an endogenous vas- p ressure in m an du ring ket am in e an esth esia. An esth An alg 1972;51:741–
cular m odulator. Am J Physiol Heart Circ Physiol 2011;301:H1–H11 745

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32. Takesh it a H, Okuda Y, Sari A. Th e effect s of ket am in e on cerebral circula- 47. Markus HS, Vallan ce P, Brow n MM. Differen t ial effect of th ree cyclooxy-
t ion an d m et abolism in m an. An esth esiology 1972;36:69–75 gen ase in hibitors on h um an cerebral blood flow velocit y an d carbon diox-
33. Bar-Joseph G, Guilburd Y, Tam ir A, Guilburd JN. Effect iven ess of ket am in e ide react ivit y. St roke 1994;25:1760–1764
in d ecreasing in t racran ial p ressu re in ch ild ren w it h in t racran ial hyp er- 48. Patel J, Rober t s I, Azzop ard i D, Ham ilton P, Edw ard s AD. Ran d om ized
ten sion . J Neu rosu rg Pediat r 2009;4:40–46 d ou ble-blin d con t rolled t rial com paring th e effect s of ibuprofen w ith in -
34. Mayberg TS, Lam AM, Mat t a BF, Dom in o KB, W in n HR. Ket am in e d oes dom eth acin on cerebral h em odyn am ics in p reterm in fan t s w ith p aten t
n ot in crease cerebral blood flow velocit y or in t racran ial pressu re du ring du ct u s ar teriosu s. Ped iat r Res 2000;47:36–42
isofluran e/n it rou s oxide an esth esia in pat ien t s un dergoing cran iotom y. 49. Delh aye C, Mah m oudi M, Waksm an R. Hypoth erm ia th erapy: n eurologi-
An esth An alg 1995;81:84–89 cal an d cardiac ben efit s. J Am Coll Cardiol 2012;59:197–210
35. Him m elseh er S, Durieu x ME. Revising a dogm a: ket am in e for pat ien t s 50. Zhao H, Stein berg GK, Sapolsky RM. Gen eral versus specific act ion s of
w ith n eurological injur y? An esth An alg 2005;101:524–534 t able m ild-m oderate hypotherm ia in at tenu at ing cerebral isch em ic dam age.
36. Clan cy M, Halford S, Walls R, Murphy M. In pat ien t s w ith h ead injuries J Cereb Blood Flow Met ab 2007;27:1879–1894
w ho un dergo rapid sequen ce in t ubat ion u sing su ccinylch olin e, does p re- 51. Hypoth erm ia after Cardiac Arrest St udy Group. Mild th erapeut ic hypo-
t reat m en t w ith a com pet it ive neu rom uscular blocking agen t im prove th erm ia to im p rove th e n eu rologic ou tcom e after cardiac arrest . N Engl J
outcom e? A literat u re review. Em erg Med J 2001;18:373–375 Med 2002;346:549–556
37. Lan ier W L, Milde JH, Mich en felder JD. Cerebral st im u lat ion follow ing suc- 52. Sch ebesch KM, Proesch oldt M, Ullrich OW, et al. Circulator y arrest an d
cinylch olin e in dogs. An esth esiology 1986;64:551–559 deep hypoth erm ia for th e t reat m en t of com plex in t racran ial an eu r ysm s—
38. Min ton MD, Grossligh t K, St ir t JA, Bedford RF. In creases in in t racran ial resu lt s from a single European center. Act a Neuroch ir (Wien ) 2010;152:
pressure from succinylcholine: prevention by prior nondepolarizing block- 783–792
ade. An esth esiology 1986;65:165–169 53. Yu Y, Ch en J, Si Z, et al. Th e h em odyn am ic respon se of th e cerebral bridg-
39. Kovarik W D, Mayberg TS, Lam AM, Math isen TL, Win n HR. Succinylch o- ing vein s to ch anges in ICP. Neurocrit Care 2010;12:117–123
lin e d oes n ot ch an ge in t racran ial p ressu re, cerebral blood flow velocit y, 54. Drum m ond JC. Th e low er lim it of autoregulat ion : t im e to revise our
or th e elect roen ceph alogram in pat ien t s w ith n eurologic injur y. Anesth th in king? An esth esiology 1997;86:1431–1433
An alg 1994;78:469–473 55. Rangel- Cast illa L, Lara LR, Gopin ath S, Sw an k PR, Valadka A, Rober t son C.
40. Dir inger MN, Scalfan i MT, Zazu lia AR, Vid een TO, Dh ar R, Pow ers W J. Cerebral hem odynam ic effects of acute hyperoxia and hyperventilation after
Effect of m ann itol on cerebral blood volum e in pat ien t s w ith h ead inju r y. severe traum atic brain injur y. J Neurotraum a 2010;27:1853–1863
Neurosurger y 2012;70:1215–1218, discussion 1219 56. St rebel S, Lam AM, Mat t a B, Mayberg TS, Aaslid R, New ell DW. Dyn am ic
41. Scalfan i MT, Dh ar R, Zazulia AR, Videen TO, Diringer MN. Effect of osm ot ic an d st at ic cerebral au toregu lat ion du ring isoflu ran e, desflu ran e, an d p ro-
agen t s on region al cerebral blood flow in t raum at ic brain injur y. J Crit pofol an esth esia. An esth esiology 1995;83:66–76
Care 2012;27:526 57. Vavilala MS, Lee LA, Lam AM. Cerebral blood flow an d vascu lar p hysiol-
42. Mor t azavi MM, Rom eo AK, Deep A, et al. Hyper ton ic salin e for t reat ing ogy. An esth esiol Clin Nor th Am erica 2002;20:247–264
raised int racran ial pressure: literat ure review w ith m et a-an alysis. J Neu- 58. Curley G, Kavan agh BP, Laffey JG. Hypocapn ia an d th e injured brain : m ore
rosurg 2012;116:210–221 h arm than ben efit . Crit Care Med 2010;38:1348–1359
43. Pfister D, St rebel SP, Stein er LA. Effect s of catech olam in es on cerebral 59. Ku lik T, Kusan o Y, Aron h im e S, Sandler AL, Win n HR. Regulat ion of cere-
blood vessels in pat ien t s w ith t raum at ic brain inju r y. Eur J An aesth esiol bral vasculat ure in norm al and ischem ic brain. Neuropharm acology 2008;
Suppl 2008;42:98–103 55:281–288
44. Pickard JD, Macken zie ET. In h ibit ion of p rost aglan d in syn th esis an d th e 60. Piepgras DG, Morgan MK, Sun dt TM Jr, Yan agih ara T, Mussm an LM. In t ra-
respon se of baboon cerebral circulat ion to carbon dioxide. Nat New Biol cerebral h em orrhage after carot id en dar terectom y. J Neurosurg 1988;68:
1973;245:187–188 532–536
45. Puppo C, Lopez L, Farin a G, et al. In dom ethacin an d cerebral autoregula- 61. Spet zler RF, Wilson CB, Wein stein P, Meh dorn M, Tow n sen d J, Telles D.
t ion in severe h ead injured pat ien t s: a t ran scran ial Doppler st u dy. Act a Norm al perfusion pressu re breakth rough th eor y. Clin Neurosu rg 1978;
Neurochir (Wien ) 2007;149:139–149, discussion 149 25:651–672
46. Jen sen K, Oh rst röm J, Cold GE, Ast rup J. Th e effect s of in dom eth acin on 62. Yam agu ch i K, Kaw am at a T, Kaw ashim a A, Hori T, Okada Y. Inciden ce an d
in t racran ial pressure, cerebral blood flow and cerebral m et abolism in pa- predictive factors of cerebral hyperperfusion after extracranial-intracranial
t ien t s w ith severe h ead injur y an d in t racran ial hyperten sion . Act a Neuro- byp ass for occlu sive cerebrovascu lar d iseases. Neu rosu rger y 2010;67:
ch ir (Wien ) 1991;108:116–121 1548–1554, discussion 1554

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Considerations for
Neurovascular Disease

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8 Neurovascular History and Examination
M. Yashar S. Kalani, Luis Pérez-Orribo, Gaurav Bhardw aj, Ian C. Francis, and Joseph M. Zabram sk i

Desp ite th e tech n ical advan ces in d iagn ost ic im aging over th e lar even t or act ivit y associated w ith th e on set? Is th ere anyth ing
past decades, clin ician s st ill dep en d h eavily on h istor y an d p hys- th at m akes th e sym ptom s bet ter or w orse?
ical exam in at ion w h en evalu at ing pat ien ts w ith cerebrovascu lar W hat w as the course of the sym ptom s? Did th ey p rogress, de-
disease. Th is poin t is em ph asized by on e of th e m ost com m on ly crease, or stay th e sam e? If th e sym ptom s ch anged, over w h at
seen p h rases in rad iology im aging rep or t s: “Correlat ion w it h in ter val did th e ch ange occur? Did th e sym ptom s w ax an d w an e?
clin ical h istor y is recom m en ded.” Nu m erou s r isk factors h ave If th e sym ptom s w ere tem p orar y, h ow long did th ey last?
been recogn ized an d st udied for vascular path ologies; on ly a Did the pat ient have an alterat ion in m otor or sensory func-
th orough h istor y an d exam can iden t ify t h e variou s factors an d t ion? Th e exam in er sh ould in quire specifically abou t a ch ange in
accom panying con dit ion s th at m ay be cru cial in determ in ing th e n eu rologic fu n ct ion , in clu ding focal w eakn ess; sen sor y ch anges;
proper recom m en dat ion s for th e in dividu al p at ien t . Alth ough difficu lt y w ith speech or u n derst an ding; visu al ch anges; an d a
differen t h istor y qu est ion s an d p hysical exam m an euvers m ay histor y of headache, nausea, vertigo, confusion, loss of conscious-
be n ecessar y for differen t vascular path ologies, th ere are som e n ess, an d seizure act ivit y.
com m on alit ies th at are discu ssed in det ail in th is ch apter. Does the pat ient have any m edical condit ion that predisposes
him or her to cerebrovascular disease? A review of th e pat ien t’s
m edicat ion m ay reveal im portan t risk factors th at m ay be m issed
in th e m edical h istor y. Kn ow ledge of th e pat ien t’s h istor y of hy-
per ten sion , diabetes, thyroid disease, cardiac disease, periph eral
■ Neurologic History vascu lar disease, or prior t ran sien t isch em ic at t ack or st roke m ay
In ter view ing pat ien ts w ith suspected cerebrovascular disease is aid in assessing risks for n eurovascular diseases. Fur th erm ore, a
n ot alw ays st raigh tfor w ard. Th e pat ien ts m ay n ot be able to pro- h istor y of periph eral vascu lar disease or periph eral vascular sur-
vide a clear h istor y an d, becau se of th e sp ecial n at u re of vascular ger y m ay lim it en dovascu lar access an d sh ould be n oted. Table
d isease, t h ey m ay ign ore or fail to n ot ice im p or t an t sym ptom s. 8.1 lists th e diseases associated w ith vascu lar disease or st roke.
In par t icular, pat ien t s w ith righ t h em isph ere im pairm en t m ay Is there a fam ily history of cerebrovascular disease? A fam ily
ign ore or deny n eurologic deficits. Pat ien ts w ith left h em isph ere h istor y of a cerebral an eur ysm or cavern ou s m alform at ion s in -
dam age m ay be u n able to provid e a clear an d u n derst an dable creases th e likelih ood th at th e pat ien t m ay h arbor th ese lesion s
h istor y. Neu rovascu lar deficits can cau se con fu sion or som n o- an d m ay alter th e t reat m en t paradigm . A fam ily h istor y of st roke
len ce, redu cing th e in ter view er’s abilit y to obtain a u sefu l h is- or predisposing con dit ion s to st roke (at rial fibrillat ion or h ear t
tor y, or th ese deficit s m ay even cau se com a, th u s preven t ing th e disease, for exam p le) in creases th e risk of th ese con dit ion s in th e
in ter view er from obt ain ing a h istor y d irect ly from t h e p at ien t . pat ien t .
It is im p or t an t to rem em ber t h at a carefu l n eu rologic h istor y Are there elem ents in the social history that m ay predispose the
sh ou ld in clu de in form at ion n ot on ly from th e p at ien t bu t also pat ient to vascular disease? Does th e pat ien t sm oke? Sm oking
from fam ily m em bers, param edical person n el, caregivers, an d h as been cited by m ult iple st udies as an in it iator an d propagator
even acquain t an ces of th e pat ien t . Som et im es, im por tan t in for- of vascu lar disease. Does th e pat ien t h ave a h istor y of alcoh ol or
m at ion com es from th ose w h o h ave obser ved th e pat ien t . W h en drug abu se? In creased, ch ron ic in t ake of alcoh ol h as system ic ef-
available, past m edical h istor y sh ou ld be obtain ed from th e pa- fects including injury to the liver and h em atopoietic system s that
t ien t’s prim ar y care p hysician an d fam ily m em bers. affect clot t ing cascades an d vascu lar in tegrit y, w h ereas dr ug
Th e follow ing basic qu est ion s sh ou ld be con sidered in obt ain - abuse, n ot ably th e use of st im ulan ts su ch cocain e an d am ph et-
ing a h istor y from all p at ien ts: am in es, h as been associated w ith an in creased risk of h em or-
How did the sym ptom s begin? Was t h e on set grad u al or rh age from an eu r ysm , ar terioven ous m alform at ion , an d spon t a-
su d d en ? n eou s in t racerebral h em orrh age secon dar y to vasculopathy.
W hat w as the pat ient doing w hen the sym ptom s began? Did Th e p at ien t sh ou ld be given an op p or t u n it y to d escr ibe h is
th e p at ien t aw aken w ith th e sym ptom s? Was th ere any p ar t icu - or h er sym ptom s w ith ou t p rom pt ing. An op en -en d ed qu est ion ,

119

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120 II Evaluation and Treatment Considerations for Neurovascular Disease

Table 8.1 Disorders that May Be Associated w ith Cerebrovascular Pathology

Disorder Mechanism

Hemorrhagic stroke
Cerebral amyloidoses
Icelandic t ype, Dutch t ype Intracerebral hemorrhages
Cerebral malformations
Bannayan-Zonana syndrome Cavernous malformations
Fam ilial arteriovenous malformations Arteriovenous m alformations
Fam ilial cavernous hemangiomas Cavernous malformations
Fam ilial intracranial aneurysms Aneurysms
Hereditary neurocutaneous hemangiomas Cavernous malformations
Polycystic kidney syndrome Aneurysms
Rendu-Osler syndrom e Telangiectasia
Von Hippel–Lindau syndrome Cerebellar hemangioblastoma
Connective tissue disorders
Ehlers-Danlos syndrome Aneurysms, arteriovenous fistula
Marfan syndrom e Aneurysms
Pseudoxanthoma elasticum Aneurysms
Factor deficiencies
Factor VII deficiency Hemorrhage
Factor VIII deficiency (hemophilia A) Hemorrhage
Factor IX deficiency (hemophilia B) Hemorrhage
Factor X deficiency Hemorrhage
Factor XI deficiency Hemorrhage
Factor XIII deficiency Hemorrhage
Hereditary platelet disorders Hemorrhage
Miscellaneous
Fibromuscular dysplasia Aneurysms, arteriovenous malformations
Moyamoya disease Intraventricular hemorrhage, subarachnoid hem orrhage
Neurocutaneous syndromes
Neurofibromatosis Aneurysms
Tuberous sclerosis Ectasia of arteries
Thrombotic stroke
Red cell disorder
Sickle cell anemia Thrombosis, intimal hyperplasia
Sickle cell C disease Thrombosis, intimal hyperplasia
Sickle cell trait Thrombosis, intimal hyperplasia
Primary polycythemia Thrombosis
Coagulation protein deficiencies
Antithrombin III deficiency Thrombosis (prim ary venous)
Heparin cofactor II deficiency* Thrombosis (prim ary venous)
Protein C deficiency Thrombosis (prim ary venous)
Protein S deficiency* Thrombosis (prim ary venous)
Abnormalities of fibrinolysis
Dysfibrinogenemia* Thrombosis
Factor XII deficiency* Thrombosis
Plasminogen activator deficiency* Thrombosis
Plasminogen deficiency Thrombosis
Prekallikrein deficiency* Thrombosis
Dyslipoproteinemias Accelerated atherosclerosis
Connective tissue disorders
Ehlers-Danlos syndrome Dissection
Marfan syndrom e Dissection
Pseudoxanthoma elasticum Arterial stenosis; coronary disease
Cardiac disorders
Fam ilial atrial myxoma Cardiac emboli
Hereditary cardiomyopathy Cardiac emboli
Hereditary conduction disorders Cardiac emboli, arrhythm ias
Mitral valve prolapse Cardiac emboli, endocarditis

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8 Neurovascular History and Exam ination 121

Table 8.1 (continued )


Disorder Mechanism

Neurocutaneous syndromes
Neurofibromatosis Obstruction of vessels by neurofibrom as; intracranial arterial stenosis and occlusion
Tuberous sclerosis Emboli associated with cardiac rhabdomyomas; intracranial arterial stenosis
Miscellaneous
Fabry’s disease Premature coronary disease; thromboembolism
Fam ilial hemiplegic migraine Uncertain
Fibromuscular dysplasia Thromboemboli; dissection
Homocystinuria Thrombosis
MELAS Uncertain
Moyamoya disease Uncertain
Abbreviation: MELAS, m itochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes
Sources: Data from Hart and Kanter,32 Testai and Gorelick,33 Strouse et al,34 Meschia et al,35 Natowicz and Kelley,36 and Mackey et al.37
*Indicates an association of the disorder with stroke that is rare or uncertain.

su ch as “W hy did you com e to th e h osp ital/office today for eval- Blood Pressure
u at ion ?” is often h elp fu l. Becau se th e p at ien t m ay n ot associate
Th e role of hyp erten sion as a m ajor con t ribu t ing factor in cardio-
h is or h er sym ptom s w it h cerebrovascu lar disease, t h e exam -
vascular diseases is w ell established. Over tim e, chronic hyperten-
in er sh ou ld t ailor qu est ion s to obt ain sp ecifics regard ing t h e
sion is associated w ith p rogressive dam age to sm all perforat ing
follow ing:
arteries leading to w hite m at ter changes of leukoencephalopathy,
1. Ch anges in beh avior lacu n ar in farcts, an d cogn it ive im pairm en t in clu ding d em en t ia.
2. Con fusion or loss of orien tat ion Alth ough th e d efin it ion of “n orm al” or physiological blood pres-
3. Difficu lt y w ith m em or y, ju dgm en t , or cogn it ion su re is con st an tly being redefin ed, cu rren t st an dard s suggest
4. Tingling, n u m bn ess, or loss of sen sat ion in th e lim bs or face th at a systolic blood pressu re of 95 to 120 m m Hg an d diastolic
5. Paralysis, w eakn ess, or clum sin ess of th e face or lim bs blood pressu re of 60 to 80 m m Hg are w ith in th e n orm al range.
6. Visual sym ptom s, in clu ding part ial or com plete loss of vision Hyper ten sion , hypoten sion , or th ostat ic ch anges, or asym m et ries
in on e eye, loss of vision to on e side, blu rred vision , or dou - of blood pressure m ay provide clues as to th e locat ion an d exten t
ble vision . Posit ive visual ph en om en a m ay also be presen t, of vascu lar disease.
including form ed hallucinations, “sparkling lights,” or colors. Evaluation of blood pressure should begin by m easuring blood
7. Im paired un derstan ding or speaking. Th e clin ician sh ou ld pressu re in both arm s w ith th e pat ien t seated. A clear asym m e-
differen t iate dysar th ria (slu rred sp eech ) from ap h asia (th e t r y, w ith a redu ced pressu re in on e arm , suggest s disease of th e
in abilit y to fin d th e correct w ord or th e u se of in correct su bclavian or brach ial ar teries. If th e redu ced p ressu re is in th e
w ords). If langu age difficu lt y is rep or ted, th e p at ien t sh ou ld left arm , a su bclavian sten osis an d “steal” n eed to be con sidered .
also be qu est ion ed regarding w rit ing an d reading. If sym ptom s of dizzin ess or syn cope/n ear syn cope are repor ted,
8. Dysp h agia (difficu lt y sw allow ing) blood pressures should be recorded w ith the patient in the stand-
9. Ver t igo, dizzin ess, or balan ce difficu lt y ing, seated, an d sup in e posit ion s. Orth ost at ic hypoten sion is de-
10. Decreased level of con sciou sn ess, in clu ding leth argy, som - fin ed as a m in im u m decrease of 20 m m Hg systolic pressure or
n olen ce, or com a 10 m m Hg diastolic pressures w ith a ch ange of posit ion . Usu ally,
11. Seizu re act ivit y th ere is a com p en sator y in crease in th e p u lse rate. Or th ost at ic
12. Headach es hypoten sion is associated w ith auton om ic failure (e.g., pat ien ts
13. Nausea or vom it ing w ith diabetes an d periph eral n europathy); h ear t disease an d de-
creased cardiac out put; an d com plicat ion s of an t ihyper ten sive
an d diu ret ic m edicat ion s, p ar t icu larly in th e elderly.1
An ot h er im p or t an t m an euver w h ile m easu r ing a p at ien t ’s
■ Neurovascular Examination blood pressure is th e determ in at ion of th e an kle–brach ial in dex
Several elem en t s of t h e n eu rovascu lar exam in at ion are com - (ABI; Fig. 8.1). Per ip h eral vascu lar d isease (PVD) is a good in d i-
m on to all vascu lar p at h ologies. A p hysician car in g for a p at ien t cat ion of cerebral vascu lar p at h ology, as sim ilar et iologies are
w it h a suspected cerebrovascular disease sh ould perform th or- resp on sible for bot h p rocesses. Th e blood p ressu re in t h e low er
ough cardiop ulm on ar y, op h th alm ologic, an d p eriph eral ext rem - ext rem it ies is u su ally h igh er th an th ose in th e u pp er ext rem it ies.
it y exam s in addit ion to th e n eu rologic exam . Below w e h igh ligh t W h en th e blood p ressu re reading in th e an kles drops below t h e
t h e cr it ical n eu rovascu lar exam com p on en t s th at sh ou ld be reading in th e arm s, PVD sh ou ld be su spected. An ABI less th an
tested in all p at ien t s. Ad dit ion ally, w e h ave in clu d ed sp ecific 0.9 is con sisten t w ith PVD; ABI values below 0.8 in dicate m oder-
exam con siderat ion s for pat ien t s w ith com m on cerebrovascu lar ate isch em ic disease an d th ose below 0.5 im ply severe isch em ic
path ologies. disease.

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122 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 8.1 Norm al resting ankle-brachial indices (ABIs)


dem onstrating m ultiphasic Doppler waveform s. DP, dor-
salis pedis, PT, posterior tibial.

Pulses Th e su p rat roch lear ar ter y (also called fron t al ar ter y) receives
collateral flow p red om in an t ly from t h e su p er ficial tem p oral,
Palp at ion in all fou r ext rem it ies of d ist al an d p roxim al vessels facial, or in fraorbit al ar ter ies, in t h at ord er of frequ en cy. Th e
sh ou ld be p er for m ed w h en exam in ing all p at ien t s w it h a su s- su praorbital ar ter y receives collateral flow from th e superficial
pected vascular p ath ology. W h en th e focu s is isch em ic cerebro- tem poral arter y, a term in al bran ch of th e extern al carot id ar ter y.
vascu lar disease, th e exam in er sh ould palpate th e vessels of th e Flow is n orm ally an tegrade (com ing ou t of th e orbit) in th ese
u pper ext rem it ies, n eck, an d face, in clu d ing th e sup raorbit al ar- vessels. Hen ce, a dim in ish ed pulse in th e supraorbital or su pra-
teries, suprat roch lear ar teries, superficial tem poral ar teries, ca- t roch lear ar ter y is con sisten t w ith an ip silateral sten osis in th e
rot id vessels p roxim ally at th eir bifurcat ion , su bclavian arteries oph th alm ic, in tern al, or com m on carot id ar teries. W h en sign ifi-
above and below the clavicles, brachial arteries, and radial arteries can t sten osis is p resen t in th e in tern al carot id ar ter y, th ese ar-
(Fig. 8.2). Ar teries sh ou ld be p alpated bilaterally, an d sim ultan e- teries m ay ser ve as collateral ch an n els from th e extern al carot id
ou sly, looking for differen ces in t im ing of filling or am plit ude. ar ter y an d flow m ay be reversed. By altern ately com pressing
Usu ally, an asym m et r y of th e pu lsat ion is m ore im por t an t th an th ese vessels as th ey en ter th e orbit an d h igh er on th e foreh ead,
th e absolute force or am p lit ud e of th e p u lsat ion . th e direct ion of flow can be assessed (Fig. 8.2).2 Th e su p rat roch -
Depen ding on th e p at ien t’s h abit u s, n orm al ar teries m ay be lear ar ter y or su praorbit al arter y m ay also be p alpated w h ile
difficu lt to p alpate, an d th is tech n iqu e alon e is n ot sen sit ive or th e superficial tem poral, facial, or in fraorbital ar teries are com -
sp ecific en ough to d iagn ose sign ifican t carot id ar ter y d isease. pressed; an adequ ate p u lse th at d im in ish es sign ifican tly w h en
In cases of com plete in tern al carot id ar ter y occlusion , a n orm al pressu re is ap plied to th ese extern al carot id bran ch es suggest s
pulsation is frequently tran sm it ted from the com m on carotid and a sten osis in th e ip silateral carot id oph th alm ic system . Alth ough
adjacen t extern al carot id ar teries. Th e carot id ar ter y sh ould be palp at ion of th e facial pu lses m ay p rovide valu able in form at ion ,
palp ated both proxim ally an d dist ally to th e bifu rcat ion , to eval- th is tech n iqu e requ ires exp erien ce an d dep en ds on th e exam in er
u ate for alterat ion s in flow. In th e absen ce of an aort ic sten osis, a for it s success as a diagn ost ic tool.
carot id bru it is likely related to localized ath erom atou s disease.2 Th ree differen t p at tern s of carot id disease are con sisten t w ith
A dim in ish ed or absen t carot id p u lse is frequ en tly du e to tor t u - an asym m et ric superficial tem poral ar ter y pulsat ion : (1) ipsilat-
osit y in th e vessel an d less frequen tly due to vascular occlusion . eral com m on carot id sten osis/occlu sion ; (2) ip silateral extern al
In cases of d im in ish ed p u lse, a com p lete exam sh ou ld in clu d e carot id ar ter y sten osis/occlu sion ; an d (3) con t ralateral in tern al
fu r t h er p alp at ion m ed ially an d laterally lookin g for a tor t u ou s carot id sten osis/occlu sion w ith in creased collateral flow th rough
vessel. t h e exter n al carot id system resu lt in g in an in creased p u lse in
Palp at ion of th e facial pu lses m ay p rovide clu es regarding ex- t h e su p erficial tem poral ar ter y on th e diseased side. If th e su p er-
t racran ial carot id occlu sive d isease.3 Su p rat roch lear an d su p ra- ficial tem poral ar ter y is ten der or pain ful to palpat ion in an older
orbit al ar ter ies are ter m in al bran ch es of t h e op h t h alm ic ar ter y. in dividu al, tem p oral ar terit is sh ou ld be suspected.

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8 Neurovascular History and Exam ination 123

Fig. 8.2a,b Locations to palpate for com m on pulses in the (a) head and neck and
(b) the extrem ities. In the head and neck, com m on locations for pulse palpation in-
clude the supraorbit al, supratrochlear, superficial tem poral, angular, and the carotid
arteries. In the extrem ities, pulses can be palpated at the subclavian, brachial, radial,
fem oral, popliteal, posterior tibial, and dorsalis pedis arteries. (Courtesy of Barrow Neu- b
rological Institute.)

Th e aor t a an d bilateral fem oral arteries sh ou ld be p alpated as th e orbit s, fron t al region , tem p oral region , an d atlan to-occip it al
w ell as th e distal low er-ext rem it y pu lses. Ath erosclerot ic dis- region . Orbital bruit s can in dicate con t ralateral in tern al carot id
ease of th e aort a occasion ally presen ts w ith spin al cord or cauda sten osis.4 Auscultat ion of bruit s over th e cran ial vessels m ay also
equin a sign s an d sym ptom s. Dim in ish ed fem oral pu lses or a pu l- h elp to iden t ify carot id-cavern ous fist u las an d oth er dural ar te-
sat ile abdom in al m ass can be im por t an t sign s, suggest ing vascu - rioven ou s fist u las. On rare occasion s, au scu lt at ion w ill iden t ify
lar path ology. bruits associated w ith intracranial arteriovenous m alform ations.
Au scu lt at ion of th e n eck sh ou ld be perform ed in it ially w ith
th e p at ien t ’s h ead in a n eu t ral posit ion an d th e pat ien t breat h ing
Auscultation of the Heart and Vasculature qu ietly. To avoid an in adver ten t Valsalva m an euver, it is bet ter to
Th is p or t ion of th e exam sh ou ld begin w ith a carefu l au scu lt a- ask th e pat ien t to briefly “stop breath ing” rath er th an to “h old
t ion of th e h ear t both to iden t ify u n derlying cardiac con dit ion s you r breath .” If n o bru it is h eard, th en occasion ally on e can be
that m ay cont ribute to stroke an d to detect m urm urs that m ay be elicited by t u rn ing th e h ead to on e side. It is im p or tan t to listen
t ran sm it ted to th e n eck an d con fu sed w ith carot id bru it s. Bru its over th e expected locat ion of th e bifu rcat ion of th e carot id ar-
m ay be produ ced by valvu lar disease, localized areas of arterial ter y, usually located just below th e angle of th e m an dible, as w ell
sten osis, in creased flow th rough n orm al vessels, an d vascu lar as p oster ior to t h e ster n ocleid om astoid m u scle. To d ist ingu ish
m alform at ion s. carot id ar ter y br u it s from t ran sm it ted card iac m u r m u rs, it is
Fig. 8.3 sh ow s th e sites of au scu ltat ion in th e cerebrovascular h elpful to m ove th e steth oscope slow ly from th e clavicle along
circulat ion . Au scultat ion sh ou ld in clude th e ver tebral, carot id, th e carot id ar ter y. Tran sm it ted m urm urs ten d to becom e m ore
an d su bclavian areas for bruit s. Auscult at ion of th e skull involves eviden t in th e m idpor t ion or distal carot id.

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124 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 8.3a,b Locations to auscultate in the (a) head and neck and (b) chest
for the cardiac exam. 1, subclavian artery; 2, vertebral artery; 3, carotid
artery bifurcation; 4, internal carotid artery; 5, posterior auricular artery;
6, ophthalm ic artery; 7, supratrochlear/orbital artery; 8, transverse facial
artery; 9, internal m axillary artery; 10, frontal branch of the superficial
temporal artery; 11, parietal branch of superficial temporal artery; 12, oc-
cipital artery; 13, location of aortic valve auscultation; 14, location of pul-
m onic valve auscultation; 15, Erb’s point; 16, location of tricuspid valve
auscultation; 17, location of m itral valve auscultation. (Courtesy of Barrow
Neurological Institute.)

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8 Neurovascular History and Exam ination 125

In gen eral, t h e d u rat ion , lou d n ess, an d frequ en cy of br u it s of the central and paracentral scotom ata. Altitudinal field defects
in crease w ith th e degree of vascu lar sten osis.5 A bru it develops are usu ally em bolic an d ret in al in n at ure. Alth ough glaucom a is
w h en th e lum en is decreased by 50%in diam eter or 75%in cross- th e m ain cau se of scotom at a, th ey are also com m on m an ifest a-
sect ion al area. As sten osis progresses, bru it s gradu ally becom e t ion s of isch em ic ret in al or opt ic n er ve disease. A scotom a in th e
h igh er pitch ed. In gen eral, ar terial br uits are audible in systole presen ce of an afferen t pu pillar y defect in dicates an opt ic n er ve
an d exten d in to diastole on ly w h en th e cross-sect ion al area of lesion . An ter ior isch em ic opt ic n eu rop at hy is t h e m ost likely
sten osis reach es 80% to 90%. As th e sten osis get s ver y t igh t , vol- cau se in th is case.
um e and frequency dim inish. The bruit m ay disappear w ith high- Pat ien ts w ith h em ian opic defects m ay com plain of m on ocu-
grade sten osis. lar visu al d ist u rban ces (Fig. 8.4). W ith t h e except ion of bitem -
Th e sen sit ivit y an d specificit y of a carot id br u it is variable p oral abn or m alit ies, a h em ian op ia p oin t s to a lesion p oster ior
w ith a w ide range, so th is in direct m eth od of diagn osing sten osis to th e opt ic ch iasm . In m ost cases, in congr u ou s h om onym ou s
h as been w idely replaced by color duplex ult rasoun d.6 It is im - h em ian op ia occu rs w it h lesion s bet w een t h e opt ic ch iasm an d
por t an t to n ote th at n ot all pat ien ts w ith carot id sten osis h ave lateral gen icu late body, or lesion s in t h e gen icu late body. Gen -
bruit s. Th e frequen cy of br uits in creases w ith in creasing sten o- erally, congru ous h em ian opia are th e result of lesion s posterior
sis, bu t even in pat ien ts w ith h igh -grade sten osis, on ly a m in or- to th e lateral gen icu late body. If th e defect is h igh ly congr uous,
it y m ay h ave br u its. In a classic st u dy, Ingall et al7 foun d th at on ly u su ally it represen ts a lesion of th e visu al cortex. An in ferior qua-
33% of pat ien t s w ith isch em ic sym ptom s an d carot id sten osis of dran tan opia m ost often rep resen t s a lesion of th e su perior opt ic
greater th an 50% h ad br u its. radiat ion in th e pariet al lobe. A su perior quadran t an opia com -
In t racran ial bru its are n ot a sen sit ive sign of int racran ial vas- m on ly poin t s to a lesion of Meyer’s loop, th e in ferior opt ic radia-
cu lar disease bu t m ay at t im es p rovid e h elp fu l d iagn ost ic in - t ion in th e tem p oral lobe. In farct , in t raparen chym al h em orrh age,
for m at ion . Alth ough ocular br uits are th e m ost com m on br uits, an d m ass effect from ar terioven ous m alform at ion are th e m ost
th ey m ay also be h eard over th e p ariet al, m astoid -occipit al, an d com m on vascu lar cau ses of lateral gen icu late, opt ic radiat ion ,
tem poral skull. Th e site of a br uit over th e skull does n ot corre- and occipital gray m at ter injur y. Aneur ysm s of the posterior com -
late w ell w ith th e site of an in t racran ial abn orm alit y. Gian t an eu - m un icat ing an d cerebral arteries can rarely affect th e opt ic t ract s
r ysm s are occasion ally associated w it h br u it s,8 an d br u it s are an d lateral gen icu late body.
n oted in m ore t h an h alf of p at ien t s w it h carot id-caver n ou s fis- Aneur ysm s of the anterior cerebral and com m unicating arter y
t u las.9 Au scu ltat ion of th e facial an d cran ial vessels m ay h elp in com plex, as w ell as an eu r ysm s of th e p araclin oidal an d su pracli-
th eir iden t ificat ion . n oidal segm en ts of th e carot id ar ter y, alth ough rare, are th e m ost
To perform a correct auscultat ion of th e orbit , th e physician com m on cerebrovascu lar cau ses of a bitem p oral h em ian op ia or
sh ou ld in st ru ct th e pat ien t to close h is or h er eyes, an d th e m em - qu adran t an opia.12
bran e of th e steth oscope sh ould be placed over th e eyelid. Asking
th e patien t to open th e con t ralateral eye w ill elim in ate th e m u s-
External Ocular Exam
cle ar t ifact . An ocu lar bru it suggest s th e existen ce of collateral
flow associated w ith ext racran ial sten osis or occlu sion . Th is m ay It is im por tan t to be m eth odical in determ in ing th e abn orm al
act u ally be th e m ost com m on cause of an ocular br uit . Ocular side du ring th e extern al eye exam in at ion . Obtain ing a h istor y of
bruit s m ay also occu r w ith carot id cavern ous fist u las, m en ingio- ocular asym m et r y an d even exam in ing past an d recen t ph oto-
m as,10 an d th e cran ial radiat ion of lou d cardiac m u rm urs.11 grap h s can be im p or t an t in d ecid in g w h et h er ocu lar fin d in gs
are relevan t to t h e p at ien t ’s p resen t ing con d it ion . A review of
ptosis cases fou n d th e m ost com m on cau se to be m yogen ic
Ophthalmologic Examination (42%), follow ed by apon eurot ic (35%), m ixed (16%), an d n euro-
A com plete oph th alm ologic exam in at ion is a crit ical com p on en t logic (7%).14 How ever, a t r ue ptosis of th e upper lid on on e side is
of any cerebrovascu lar exam . Th is sh ou ld in clu d e test in g of vi- consistent w ith an ipsilateral third cran ial n er ve palsy or Horner’s
su al acu it y an d visu al field s in each eye, exam in at ion of ext ra- syn drom e. Com m on ocu lom otor n er ve p alsy resu lts in ptosis,
ocu lar m ovem en t s, an d in sp ect ion of t h e eyelid , conju n ct iva, w h ich can be caused by vascu lar, isch em ic, n eoplast ic, dem yelin -
cornea, iris, pupil, and lens. Ophthalm oscopic exam ination of the at ion , in flam m ator y, an d t rau m at ic p roblem s.15–18 In an isocoria
ocular fun di sh ould also be perform ed, ideally w ith th e pat ien t’s of > 2 m m , n euroim aging is n eeded to r ule out a lesion of th e
pup ils dilated. posterior com m un icat ing ar ter y.19–21 Ptosis in pat ien ts w ith m y-
asth en ia gravis is variable th rough out th e day an d can even al-
tern ate sides.18
Visual Acuity and Visual Fields
A ch ron ic ocular isch em ia due to severe carot id ar ter y disease
Classically visual acu it y h as been m easu red by u sing th e Sn ellen m ay be m an ifest as ven ou s engorgem en t an d a red injected ap -
ch ar t placed at 20 feet; 12 h ow ever, du ring recen t d ecades, n ew pearan ce of th e conju n ct iva an d ep isclera. Ven ou s engorgem en t
system s w ith in creased sen sit ivit y for m easu ring visual acu it y, m ay also be seen in th e set t ing of fist ulas an d sh ould illicit fur-
su ch as adapt ive opt ics, h ave been developed.13 ther w orkup as indicated. Th e corn ea can becom e edem atous an d
In th e con text of vascular lesion s, dim in ish ed acuit y can be cloudy an d th e vessels of th e iris m ay be dilated, an d a visible
du e to an terior segm en t isch em ia (corn ea, iris, or len s), p osterior n eovascular process called rubeosis iridis m ay occur. Th is n eo-
segm en t ischem ia (retina), or optic n er ve ischem ia. Patients w ith vascu lar izat ion m ay lead to glau com a bein g on e of th e m ost
vascu lar lesion s of th e carot id system can presen t w ith m on ocu- ser iou s com plicat ion s of ch ron ic ocular isch em ia an d m ay cause
lar dim in ish ed visu al acu it y, for exam ple alt it u din al field defect s subsequ en t opt ic n er ve dam age w ith visual field loss.

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126 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 8.4 Expected visual field cuts associated with lesions along the optic anopsia caused by lesion in the optic tract; e,f, right inferior (e) and right
tract: a, loss of vision in left eye caused by injury to the optic nerve; b, left superior (f) quadrantanopsias caused by defects in the optic radiations;
nasal hem ianopsia caused by a perichiasmal lesion; c, bitemporal hem i- g, right hom onym ous hemianopsia with macular sparing caused by lesion
anopsia caused by a lesion at the optic chiasm ; d, right hom onym ous hem i- in the visual cortex. (Courtesy of Barrow Neurological Institute.)

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8 Neurovascular History and Exam ination 127

Pupil Examination en t p u pillar y defect p oin t s to a lesion of th e opt ic n er ve an d is


rarely seen w ith ret in al defects.
Th e pu p illar y exam in at ion sh ou ld be don e p assively first , w ith
th e exam in at ion room ligh t s on an d d im m ed. An isocoria m ay be
Funduscopic Examination
physiological or path ological. In physiological an isocoria, p u p il-
lar y resp on ses to ligh t are n orm al. Path ological an isocoria is du e Du r ing t h e n eu rovascu lar exam in at ion , t h e evalu at ion of t h e
to dam ages to th e efferen t p ar t of th e p u p illar y path w ay, n ot af- fu n d u s of t h e eye is essen t ial. Th e evalu at ion sh ou ld in clu d e
feren t dam age. It is greatest in th e dark an d is m ost apparen t in exam in at ion for ocu lar isch em ia, ret in al em boli, hyp er ten sive
th e first 5 secon d s of dark.12,22 An isocoria is th e m ost im p or t an t or diabet ic ret in opathy, ret in al isch em ia, or ret in al h em orrh age
passive p u p illar y sign to look for, even th ough it is com m on in suggest ive of in t racran ial h em orrh age (Fig. 8.5).
n orm al pat ien t s. In term it ten t an isocoria of 0.4 m m or greater
m ay occur in 40% of n orm al pat ien t s.23 Pat ien t s w ith Horn er’s
Extraocular Movements
syndrom e presen t w ith unilateral ptosis, alth ough bilateral ptosis
occurs rarely. Th e ptosis is du e to injur y to th e oculosym path et ic Th e basic p rin ciples of ext raocu lar m ovem en t s m ay assist clin i-
path w ay from th e hyp oth alam u s to lu ng apex to th e in tern al ca- cian s in localizing cerebrovascu lar disease in th eir p at ien t s.
rot id ar ter y. Clin ical exam in at ion is su fficien t to diagn ose Horn - A fixed conjugate lateral gaze suggest s a st r uct u ral lesion of
er’s syn drom e if th ere is a reverse ptosis an d n onp hysiological eith er th e cerebral h em isph ere on th e side of th e direct ion of th e
anisocoria.18 Th e abn orm alit y m ay be anyw here in a three-neuron gaze or of th e con t ralateral pon s involving th e sixth n er ve n u-
sym pathetic pathw ay from the hypoth alam us, th rough the brain - cleu s or p aram edian p on t in e ret icu lar form at ion . Conjugate eye
stem to th e low er cer vical sp in al cord, t h rough th e p araver tebral deviat ion occu rs in ~ 20%of h em isp h eric st rokes. It is m ore com -
sym path et ic ch ain , to th e su p erior cer vical ganglion , an d fin ally m on after righ t h em isph ere lesion s th an left h em isph ere lesion s
to th e pupillar y dilator m uscle.24 An isocoria in pat ien ts w ith an d m ay be seen w it h fron t al, tem p oral, an d p ar iet al lesion s.
Horn er’s syn drom e is w orse in dim ligh t ing w ith a p resen tat ion Dim in ish ed ver t ical gaze u su ally resu lt s from a lesion of t h e
of “dilation lag.”25 Preganglionic Horner’s syndrom e can be caused t h alam us or brain stem . Dim inished upw ard gaze m ay result from
by isch em ic or h em orrh agic lesion s of th e hypoth alam us, brain - lesion s of th e p osterior com m issu re, u n ilateral th alam ic or m id-
stem , or cer vical cord. Acu te carot id th rom bosis, carot id dissec- brain tegm en t u m , bilateral p retect al area, or d orsal p er iaqu e-
tion , and isch em ia of th e superior cer vical ganglia 26 can also cause d u ct al gray m at ter. Isolated dow nw ard gaze p alsy is ver y rare
Horn er’s syndrom e. Overall, h ow ever, Horner’s syndrom e is m ore an d is usually caused by a m idbrain lesion . Ver t ical gaze palsies
likely to be due to cen t ral n er vou s system isch em ia th an to in - m ay be th e result of isch em ia, direct effect of h em orrh age, m ass
volvem en t of th e carot id plexu s.24 effect from fu siform an eu r ysm s, or vasosp asm .29
In a com atose or obt unded patient, pupillary defects asso ciated Diplopia w ith th ird or fou r th cran ial n er ve lesion s is usually
w ith ptosis an d lim itat ion of adduct ion (m edial rect us palsy) obliqu e, w ith h orizon t al an d ver t ical com pon en ts. Horizon t al
m ay be an im portan t sign of early un cal h ern iat ion . Associated diplop ia poin t s to a sixth n er ve lesion . Sim ply p u t , diplop ia w ors-
sign s of ten torial h ern iat ion m ay in clu de bilateral ptosis, in ter- en s w h en th e p at ien t looks in th e direct ion of th e m ot ion of th e
nuclear oph thalm oplegia, and vertical gaze paresis. In brain death, paret ic m u scle. For exam ple, h orizon tal diplop ia th at in creases
th e p u p ils can be m idp osit ion or d ilated an d u n react ive to ligh t .27 w hen a pat ien t at tem pts to look to th e righ t im plicates th e righ t
Th e m ost com m on locat ion s for an eu r ysm s th at w ill cau se lateral rect u s m u scle an d abducen t n er ve. Obliqu e diplopia th at
oculom otor palsy are th e posterior com m un icat ing ar teries. Pto- in creases w ith in torsion of th e righ t eye im plicates th e superior
sis is often a con sp icu ou s sign an d a m ore frequ en t com p lain t obliqu e m uscle an d t roch lear n er ve.
th an d iplop ia w ith th ird n er ve lesion s. App roxim ately 50%of p a- Disorders of eye m ovem ent are com m on in patients w ith both
t ien ts w ith an eu r ysm s in th is locat ion p resen t w ith a th ird n er ve isch em ic an d h em orrh agic lesion s of th e posterior circulat ion .
p alsy.28 Less com m on locat ion s in clu d e t h e basilar ar ter y an d Com plete pupillary paralysis usually accom panies eye m ovem en t
in t racaver n ou s an eu r ysm s. Pat ien t s w it h carot id caver n ou s fis- abn or m alit ies an d ptosis, bu t occasion al cases h ave been re-
t u las m ay p resen t w it h t h ird n er ve p alsies, u su ally w it h ot h er ported in w h ich th ere w as at least relat ive sp aring of th e pu p il
accom panying cran ial n er ve palsies, an d eye fin dings, in clu ding early in th e clin ical course of an an eur ysm .30 A pat ien t w ith com -
ch em osis an d pu lsat ing exop h th alm os. plete th ird n er ve p alsy an d a fixed p u p il sh ou ld be evalu ated for
A u nilateral defect of pupillar y closure w ill be accen t uated in th e p resen ce of an an eu r ysm . Isolated p u p il-sp aring th ird n er ve
a w ell-lighted room . Light stim ulation of the abnorm al eye causes palsies, esp ecially in older in dividu als, sh ou ld be obser ved care-
a con sensual pupillar y respon se w ith out a direct respon se. In th e fu lly, but w ith th e availabilit y of m odern non invasive im aging
absen ce of any oth er sign of a th ird n er ve lesion , th is suggest s a tech n iques th ese pat ien t s sh ould probably be evaluated fur th er
pup illar y sph in cter m u scle abn orm alit y. Absen t p upillar y clo- to ru le ou t an eu r ysm s or oth er in t racran ial path ologies.
su re, a sluggish p u pil m ay be seen in pat ien ts w ith iris isch em ia Cavern ou s sin u s con dit ion s u su ally p resen t w ith involvem en t
from an terior segm en t isch em ia, or sp h in cter m u scle r u pt u re of m ore th an on e ocular cran ial n er ve. Occasion ally th ere is an
from direct eye t raum a. It m ay also be related to previou s eye isolated n er ve or a sixth n er ve lesion com bin ed w ith Horn er’s
su rger y, com m on ly cat aract su rger y. syn drom e. Th e p rogression of cran ial n er ve dysfu n ct ion to in -
Th e Marcu s- Gu n n p h en om en on (an afferen t p u p illar y d efect) volve the third, fourth, fifth (first and second divisions), and sixth
is detected by th e u se of th e “sw inging flash ligh t” test . In st ru ct- n er ves an d even t u ally th e opt ic n er ve is sim ilar in cavern ous ar-
ing th e pat ien t to look in t h e distan ce th rough ou t th e pu pillar y terioven ous fist ulas an d in t racavern ous an eur ysm s. Th e feat u res
exam in at ion p reven t s th e accom m odat ion -convergen ce m iosis th at m ay dist ingu ish th e t w o are exoph th alm os an d ch em osis,
reflex from con fou n ding th e effect of ligh t st im u lat ion . An affer- w h ich are usually m uch m ore pron ou n ced w ith fist ulas.12

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128 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 8.5a–e Funduscopic evaluation provides the exam iner with a wealth
of inform ation regarding the patient’s existing vascular condition. (a) Fun-
duscopic im age from a patient with a norm al retina who has m inim al, age-
appropriate vascular changes. (b) Funduscopic im age from a patient with
increased intracranial pressure; note the blunting of the optic disk. (c) Fun-
duscopic dem onstration of Terson syndrom e–related retinal hem orrhage
in the set ting of subarachnoid hem orrhage. (d) Funduscopic im age from
a diabetic patient with retinal branch vein occlusion and hem orrhage. Note
the dot and blot hemorrhage pat terns in the fovea. (e) Right central retinal
artery occlusion and cherry red spot visible on funduscopic im age. Note
narrowing and nicking of arteries suggestive of hypertension. (b: Reprinted
from Koc K, Anik I, Altintas O, Ceylan S. Endoscopic optic nerve decompres-
sion for idiopathic intracranial hypertension in t wo cases: case report. Minim
Invasive Neurosurg 2008;51:72–75, with permission from Georg Thieme
Verlag KG Stut tgart. a,c–e: Courtesy of Barrow Neurological Institute.)

b c

d e

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Table 8.2 Glasgow Coma Scale (GCS): The Most Routinely Used Scale for Assessing Degree of Consciousness in Patients

GCS Scoring Components

Eye Opening (E) Verbal Response (V) Motor Response (M)


4 = Spontaneous 5 = Normal conversation 6 = Normal
3 = To voice 4 = Disoriented conversation 5 = Localizes to pain
2 = To pain 3 = Words, but not coherent 4 = Withdraws to pain
1 = None 2 = No words, only sounds 3 = Decorticate posture
1 = None 2 = Decerebrate
1 = None
Total GCS Score = E + V + M
Source: Teasdale G, Jennet t B. Assessm ent of coma and im paired consciousness: a practical scale. Lancet 1974;2: 81–84.

Examination of an Obtunded Patient com p u ted tom ography (CT), a lu m bar pu n ct u re m u st be p er-
form ed to both iden t ify red blood cells in th e cerebrospin al fluid
Alth ough m any pat ien ts are referred to a n eu rovascular surgeon
an d to rule out oth er cau ses of com a.
by t h eir p r im ar y care p hysician s for w orku p of p at h ology, in
Im aging is a crit ical part of th e w orkup for th e obt un ded pa-
som e sit u at ion s p at ien t s m ay p resen t em ergen t ly. Sp ecific ex-
t ien t w h o p resen t s w ith possible vascu lar path ology. Th e in it ial
am in at ion com p on en t s sh ou ld be in clu d ed in assessm en t s of
im aging m odalit y that is m ost frequently used rem ains a basic CT,
obt u n ded pat ien ts.
but CT angiography h as becom e th e diagn ost ic st udy of ch oice
Th e evalu at ion of an obt u n ded p at ien t sh ou ld begin w ith th e
for th e em ergen cy evaluat ion of pat ien ts presen ting w ith sus-
basics of crit ical care, w h ich en tail securing th e air w ay (as n eces-
pected st roke or su barach n oid h em orrh age. In th e pat ien t w ith
sar y) an d resu scitat ing th e p at ien t to en su re p erfu sion of t issu es.
ischem ic stroke, CT angiography should include both the head and
On ce th e air w ay is secu red, at ten t ion is t urn ed to an assessm en t
n eck vessels. At th e au th ors’ in st it ut ion , th e em ergen cy evalua-
of th e global level of con sciousn ess. Alth ough several scales are
t ion of isch em ic st roke p at ien t s in clu des CT perfu sion . A d et ailed
u sed in terch angeably, th e m ost w idely used is th e Glasgow Com a
discu ssion of variou s im aging m odalit ies is presen ted elsew h ere
Scale (GCS).31 It assign s p oin t s to eye op en ing, verbal com m u n i-
in th is book.
cat ion , an d m otor resp on se (Table 8.2). Th e GCS score ranges
Th e decision to t reat a p at ien t is dep en den t on th e p at ien t’s
from 3 to 15. A score of 3 to 8 is defin ed as a com atose st ate w ith
w ish es, t h e clin ical exam , an d t h e resu lt s of im aging st u d ies.
im plicat ion s for t reat m en t . Pat ien ts w ith a GCS score of 8 or less
Pat h ology-sp ecific con sid erat ion s an d a d et ailed d iscu ssion of
usu ally requ ire close obser vat ion an d con siderat ion of th e place-
var iou s t reat m en t m odalit ies are p resen ted in t h e ap p licable
m en t of an extern al ven t ricular drain to m on itor in t racran ial
ch apters in th is text .
pressu re as n ecessar y.
In addit ion to an assessm en t of con sciousn ess, th e pat ien t
sh ou ld u n d ergo a focu sed an d t h orough n eu rovascu lar exam i-
n at ion in clu ding assessm en t of cran ial n er ves an d m otor an d
sen sor y m odalit ies. In evaluat ing a pat ien t w ith subarach n oid
■ Conclusion
h em orrh age, special at ten t ion m ust be paid to m en ingeal sign s. Th e in t rodu ct ion of im aging tech n iqu es h as greatly decreased
Evaluat ion of p erip h eral p u lses is im p or tan t for all p at ien t s w h o vascu lar pract it ion ers’ relian ce on physical exam an d h istor y for
m ay u n dergo en dovascu lar in ter ven t ion . diagn osing cerebrovascu lar disease. How ever, d esp ite tech n ical
On ce a p ract it ion er h as evalu ated t h e p at ien t , rou t in e labo - advan cem en ts, th e h istor y an d physical exam rem ain an im por-
rator y st u d ies in clu d in g a com p lete blood cou n t , com p lete tan t par t of th e evaluat ion of n eurosurgical pat ien ts. An accurate
m et abolic p an el, coagu lat ion p an el, an d asp irin an d clop idogrel h istor y an d exam in at ion can both iden t ify path ology an d lim it
resp on d er assays sh ou ld be obt ain ed . In p at ien t s in w h om sub - th e differen t ial diagn osis.
arach n oid h em orrh age is suspected but n ot eviden t on rout in e

References
1. Novak V, Hajjar I. Th e relat ion sh ip bet w een blood pressure an d cogn it ive ter y sten osis: a system at ic review an d m et a-an alysis. J Vasc Surg 2005;
fu n ct ion . Nat Rev Cardiol 2010;7:686–698 41:962–972
2. Toole JF. Cerebrovascular Disorders, 4 ed. New York: Raven Press; 1990 7. Ingall TJ, Hom er D, W h isn an t JP, Baker HL Jr, O’Fallon W M. Predict ive
3. Caplan LR. Th e fron t al-ar ter y sign —a bedside in dicator of in ternal carot id valu e of carot id br u it for carot id ath erosclerosis. Arch Neu rol 1989;46:
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4. Sm ith JH, Fugate JE, Claassen DO. Pearls & Oy-sters: th e orbit al bruit: a 8. Fox JL. In t racran ial An eur ysm s. New York: Springer-Verlag; 1983
poor m an’s angiogram . Neu rology 2009;73:e81–e82 9. Ellis JA, Goldstein H, Con n olly ES Jr, Meyers PM. Carot id-cavern ous fist u-
5. Sp en ser MP, Reid JM. Cerebrovascu lar Evalu at ion w it h Dop p ler Ult ra- las. Neurosu rg Focu s 2012;32:E9
soun d. Th e Hague: Mar t in us Nijh off; 1981 10. Dalsgaard-Nielsen T. St u dies on in t racran ial vascular soun ds. Act a Psych ol
6. Jah rom i AS, Cin à CS, Liu Y, Clase CM. Sen sit ivit y an d specificit y of color Neurol Scan d 1939;14:69
du p lex u lt rasou n d m easu rem en t in th e est im at ion of in tern al carot id ar- 11. MacKen zie I. Th e in t racran ial br uit . Brain 1955;78:350–368

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12. Liu GT, Galet t a SL. Th e n eu ro-op h t h alm ologic exam in at ion (in clu d in g 26. Sears ML, Kier EL, Ch avis RM. Horn er’s syn drom e caused by occlu sion of
com a). Oph th alm ol Clin North Am 2001;14:23–39, vii th e vascu lar su p p ly to sym p ath et ic ganglia. Am J Op h th alm ol 1974;77:
13. Roorda A. Adapt ive opt ics for st udying visual fun ct ion : a com preh en sive 717–724
review. J Vis 2011;11:7 27. W ijd icks EF. Deter m in ing brain deat h in adu lt s. Neu rology 1995;45:
14. Baggio E, Ruban JM, Boizard Y. [Et iologic causes of ptosis about a series of 1003–1011
484 cases. To a n ew classificat ion ?]. J Fr Oph t alm ol 2002;25:1015–1020 28. Son i SR. An eur ysm s of th e posterior com m un icat ing ar ter y an d ocu lom o-
15. Tan H. Bilateral ocu lom otor p alsy secon dar y to p seu d ot u m or cerebr i. tor p aresis. J Neu rol Neu rosu rg Psych iat r y 1974;37:475–484
Pediat r Neu rol 2010;42:141–142 29. Leigh RJ, Zee DS. Th e Neu rology of Eye Movem en t . Ph iladelph ia: Davis;
16. Bah m an i Kash kouli M, Kh alatbari MR, Yahyavi ST, Borgh ei-Razavi H, 1983
Solt an -Sanjari M. Pit uit ar y apoplexy presen t ing as acute pain ful isolated 30. Nadeau SE, Trobe JD. Pu pil sparing in oculom otor palsy: a brief review.
u n ilateral t h ird cran ial n er ve p alsy. Arch Iran Med 2008;11:466–468 An n Neurol 1983;13:143–148
17. Beleza P, Mach ado A, Soares-Fern an des J, et al. Isolated oculom otor n er ve 31. Teasdale G, Jen n et t B. Assessm en t of com a an d im paired con sciousn ess.
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2008;66:254–255 32. Har t RG, Kan ter MC. Hem atologic disorders an d isch em ic st roke. A selec-
18. Black EH, Nesi FA, Calvan o C, Gladstone GJ, Levin e MR. Nesi’s Oph th alm ic t ive review. St roke 1990;21:1111–1121
Plast ic an d Reconst ruct ive Surger y, 3rd ed. New York: Springer; 2012 33. Test ai FD, Gorelick PB. In h erited m et abolic disorders an d st roke par t 1:
19. Brazis PW. Isolated palsies of cranial n er ves III, IV, an d VI. Sem in Neurol Fabr y disease an d m itoch on drial m yopathy, en ceph alopathy, lact ic acido-
2009;29:14–28 sis, an d st rokelike episodes. Arch Neurol 2010;67:19–24
20. Akagi T, Miyam oto K, Kash ii S, Yosh im ura N. Cause an d progn osis of n eu- 34. St rouse JJ, Lan zkron S, Urrut ia V. Th e epidem iology, evaluat ion an d t reat-
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cases of oculom otor palsy. Jpn J Oph thalm ol 2008;52:32–35 2011;4:597–606
21. Cullom ME, Savin o PJ, Sergot t RC, Bosley TM. Relat ive pupillar y sparing 35. Mesch ia JF, Nalls M, Mat arin M, et al; Siblings With Isch em ic St roke St udy
th ird n er ve p alsies. To ar teriogram or n ot? J Neu roop h th alm ol 1995;15: Invest igators. Siblings w ith isch em ic st roke st udy: result s of a gen om e-
136–140, discu ssion 140–141 w ide scan for st roke loci. St roke 2011;42:2726–2732
22. Pilley SF, Th om pson HS. Pupillar y “dilat at ion lag” in Horner’s syn drom e. 36. Natow icz M, Kelley RI. Men delian et iologies of st roke. An n Neurol 1987;
Br J Oph th alm ol 1975;59:731–735 22:175–192
23. Lam BL, Th om pson HS, Corbet t JJ. Th e prevalen ce of sim ple an isocoria. 37. Mackey J, Brow n RD Jr, Moom aw CJ, et al; FIA an d ISUIA Invest igators.
Am J Oph th alm ol 1987;104:69–73 Un r u pt u red in t racran ial an eu r ysm s in th e Fam ilial In t racran ial An eu r ysm
24. Giles CL, Hen d erson JW. Hor n er’s syn d rom e: an an alysis of 216 cases. an d In tern at ion al St u dy of Un rupt ured In t racran ial An eur ysm s coh or t s:
Am J Oph th alm ol 1958;46(3 Par t 1):289–296 d ifferen ces in m u lt ip licit y an d locat ion . J Neu rosu rg 2012;117:60–64
25. Walton KA, Bu on o LM. Horn er syn drom e. Curr Opin Ophth alm ol 2003;14:
357–363

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9 Intraoperative Evaluation of Blood Flow
Sepideh Am in-Hanjani and Fady T. Charbel

Evaluat ion of blood flow during cerebrovascular surger y is an w ave of u lt rasou n d em it ted from th e t ran sdu cers crosses th e
im por t an t com pon en t of su ccessfully execu t ing th e operat ive vessel to boun ce off th e acoust ic reflector. It is received by th e
plan . Th e in form at ion con t ribu tes to decision m aking an d con - oth er t ran sducer an d converted in to an elect rical sign al from
firm s in t raoperat ive success. Th e u t ilit y of in t raoperat ive flow w h ich th e flow detect ion un it derives an accu rate m easure of
m easurem en t s is m ost eviden t in th e set t ing of cerebral revascu- t ran sit t im e (th e t im e it takes th e u lt rasou n d w ave to t ravel from
larizat ion an d an eu r ysm su rger y. Th e ch apter review s th e tools on e t ran sducer to th e oth er). Th e t ran sit t im e is affected by th e
an d specific st rategies for u t ilizing flow m easu rem en t s, par t icu - m ot ion of blood flow ing th rough th e vessel, an d th e differen ce
larly quan t itat ive vessel flow m easu rem en t s. bet w een upst ream an d dow n st ream t ran sit t im e is used to m ea-
sure blood flow in m illim eters p er m in u te (m L/m in ).
Th e p robe is m an u fact u red in a variet y of sizes (1.5, 2, an d
3 m m ) to accom m odate in t racran ial vessels ran ging from 1 to
■ Techniques for Intraoperative 3 m m . Larger sizes suit able for ext racran ial cerebral vessels are
Evaluation of Blood Flow also available. Com pared w ith th e older tech n ique of elect ro-
m agn et ic flow probes, w h ich requires precise fit of th e vessel
Many tech n iqu es aim ed at d eterm in ing th e st at u s of cerebral an d direct con tact w ith th e probe, th e ult rason ic flow probe
blood flow in t raoperat ively h ave been described. Th ese tools fall does n ot requ ire a t igh t fit or direct con tact . Th e sp ace bet w een
in to physiologically based tech n iqu es th at at tem pt to assess h e- th e vessel an d en circling probe can be filled w ith an u lt rason ic
m odyn am ics directly, eith er th rough evalu at ing paren chym al cou plan t su ch as gel or salin e w ith ou t com prom ising flow m ea-
perfu sion or blood vessel flow, or th rough in direct m ean s by as- su rem en t s. Fu rth erm ore, th e accu racy of elect rom agn et ic flow -
sessing elect rophysiological fu n ct ion . Addit ion al im aging-based m et r y can be affected by t h e h em atocr it level or vessel w all
tech n iqu es aim ed at visu alizing vessel p aten cy, su ch as conven - th ickn ess, n eith er of w h ich affect s m easu rem en t s of t ran sit t im e.
t ion al an d video in docyan in e green (ICG) angiography, are also Th e accu racy of th e u lt rason ic flow p robe h as been est ablish ed
valu able in t raoperat ively. Each tech n iqu e h as relat ive advan t ages w ith both in vit ro an d in vivo test ing.3
an d disadvan t ages, w h ich m u st be em ployed select ively to obt ain
m axim al ben efit du ring cerebrovascular su rger y.
Parenchymal Perfusion Monitoring
Paren chym al m on itor in g tech n iqu es in clu d e d evices for exam -
Direct Vessel Measurement in ing t h er m al d iffu sion an d t issu e oxim et r y. Th e for m er u ses
An assessm en t of blood flow w ith in specific vessels can be ob - a p robe p laced direct ly w it h in t h e p aren chym a an d relies on
t ain ed u sing Dop p ler u lt rason ograp hy. Th is tech n iqu e is u sed m easu ring th e th erm al con du ct ivit y of th e t issu e, from w h ich
to calcu late flow velocit y based on t h e frequ en cy sh ift of sou n d in form at ion regarding blood flow can be derived.4,5 Th e lat ter
w aves as th ey reflect off flow ing blood. In t raoperat ively, m icro- u ses n ear-in frared spect roscopy, w h ich is based on th e relat ive
vascu lar Doppler ult rason ography can provide real-t im e assess- absorpt ion proper t ies of oxy- an d deoxyh em oglobin to provide
m en t of vessel p aten cy.1 Th e sm all size of th e p robe (as sm all as m easu res of cerebral t issu e oxygen at ion .6,7 Th e prim ar y draw -
1 m m ) m akes it easy to use in th e op erat ive field. Th e p robe also back of th ese tech n iques is th e lim ited region of t issue th at can
can be used rap idly an d rep et it ively. How ever, th e device p ro- be assessed. Fur th erm ore, th e subcor t ical t issu es or rem ote t is-
vides a qualit at ive assessm en t of th e presen ce or absen ce of sue territories can n ot be m on itored .
blood flow, rath er th an a quan t it at ive m easure of it s act ual flow.
Th erefore, n on occlu sive com p rom ise of a vessel is m ore difficu lt
Electrophysiological Monitoring
to detect. Specific velocit y criteria and Doppler signal profile char-
acteristics potentially can be used to provide m ore quantitative Elect rophysiological m on itoring of evoked poten t ials is a tech -
data, but the interpretations int roduce increased com plexit y. n ique used to detect an d aver t cerebral isch em ia during cerebro-
In con t rast , a m icrovascular ult rason ic flow probe (Ch arbel vascu lar su rger y.8 Both sen sor y an d m otor evoked poten t ials
Micro-Flow p robe, Tran son ics System s In c., Ith aca, NY) can m ea- h ave been u sed for th is purpose. A decrem en t or loss of th ese
su re blood flow directly an d qu an t it at ively. Th is probe u ses th e poten t ials ser ves as an in d icat ion of isch em ia an d acts as a su r-
prin cip le of t ran sit t im e to m easu re flow in vessels, in depen den t rogate m arker for cerebral blood flow. How ever, th is m odalit y
of t u rbulen ce or flow -velocit y profile.2,3 Th e device con sist s of is rest ricted to sensorim otor fun ct ion s. Th us, it can be pron e to
t w o u lt rason ic t ran sdu cers an d an acou stic reflector, w h ich form false n egat ives depen ding on th e vascular territor y of in terest .
a C-sh aped probe th at is placed aroun d th e vessel of in terest . A Furth erm ore, th e m on itoring is labor in ten sive an d it s in tegrit y

131

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132 II Evaluation and Treatment Considerations for Neurovascular Disease

can be influenced by anesthetic technique. In the absen ce of frank Flow Measurement in Aneurysm Surgery
isch em ia, th e elect rophysiological in form at ion also provides n o
Beyon d com p lete obliterat ion of th e an eur ysm , th e prim ar y goal
in dicat ion of act u al vessel sten osis or lu m in al com prom ise.
of an eur ysm surger y is to avoid com prom ise of th e paren t an d
associated vessels. In adver ten t vessel com p rom ise rem ain s a
Vessel Imaging sou rce of m orbidit y associated w ith op erat ive m an agem en t of
an eu r ysm s. Many of th e tech n iqu es d iscu ssed earlier in t h is
Tradit ion ally, determ in at ion of vessel paten cy after cerebrovas- ch apter can be u sefu l bu t h ave in h eren t lim it at ion s as n oted .
cular in ter ven t ion s h as relied h eavily on visualizat ion of th e ves- Direct quan t itat ive flow m easurem en t is a robust an d reliable
sel w ith conven t ion al angiograp hy. In t raop erat ive angiograp hy m eth od for avert ing com prom ise of paren t an d bran ch vessels.
is w idely used 9,10 and offers unique advantages for visualizing the Th ese m easu rem en t s can easily be com bin ed w ith tech n iqu es
en t ire cerebrovascu lar t ree, beyon d th e field of su rgical exp osu re su ch as video ICG angiography to assess p erforators an d conven -
or d irect visu alizat ion . It can be p ar t icu larly u sefu l for id en t i- t ion al angiography to assess for an eu r ysm rem n an ts.
fying h id d en an eu r ysm al rem n an t s or resid u al ar ter ioven ou s
m alform at ion s an d fist u las. How ever, th ere are also con st rain t s
in h eren t to p erform ing angiogram s in th e operat ing su ite: th e Technique
requirem en t for person n el an d equ ipm en t an d th e p oten t ial in -
Th e gen eral ap p roach to flow m easu rem en t for an eu r ysm su r-
creased tech n ical difficu lt y of perform ing select ive vessel cath e-
ger y is as follow s (Fig. 9.1).14 After th e an eu r ysm an d associated
terizat ion im posed by th e operat ive posit ion ing of th e pat ien t .
vessels are exposed, baselin e flow s are m easured in vessels at
Intraoperat ively, convention al angiography also prolongs surgery
risk for com prom ise. To do so, a p or t ion of th e vessel of in terest
an d in t roduces exposure to an addit ion al invasive procedure an d
w ide en ough to accept th e probe is dissected free, an d th e probe
ion izing radiat ion. Beyon d th e rap idit y of dye clearan ce th rough
is placed aroun d th e vessel. Th e flexible con n ect ion of th e p robe
the vessels, lit tle can be deduced about the act ual flow in vessels.
to it s h an dle allow s th e in st rum en t to be placed from m ult iple
An oth er im aging m odalit y th at h as quickly becom e stan dard
d ifferen t t rajector ies, even th rough sm all cran iotom ies an d in
during cerebrovascular su rger y is video ICG angiography. Th is
deep locat ion s. Th e target vessels var y based on th e locat ion of
tech n ique relies on in t raven ous inject ion of ICG dye, w h ich is
t h e an eu r ysm , for exam p le, th e M2 bran ch es for a m id dle cere-
t h en visu alized as in t ravascu lar flu orescen ce w it h in t h e blood
bral ar ter y (MCA) an eu r ysm , or t h e M1 an d A1 bran ch es for a
vessel by illu m in at in g t h e op erat ive field w it h n ear-in frared
paraclin oid in tern al carot id ar ter y (ICA) an eu r ysm . Th e p robe
ligh t .11,12 ICG angiography is a u sefu l tool, en abling visu alizat ion
sh ou ld be p laced far en ough from th e base of th e an eu r ysm to
of sm all perforator vessels n ot assessable by conven t ion al angi-
avoid th e an eur ysm clips from blocking access on ce th ey h ave
ograp hy. It is also easy an d qu ick to u se. Th is m odalit y can on ly
been applied. How ever, th e abilit y to adjust th e probe t rajector y
assess vessels directly exposed in th e operat ive field. Alth ough
m ean s th at th is issue rarely poses a problem . After baselin e m ea-
ICG can be rep eated , a 5- to 10-m in u te delay is t ypically requ ired
su rem en t s of flow h ave been obtain ed, th e an eu r ysm is clip p ed .
to w ash out the prior injection adequately. Furtherm ore, alth ough
Vessel flow is th en rem easured to con firm th at flow h as been
vessel p aten cy can be con fir m ed , ICG visu alizat ion d oes n ot
preser ved in th e bran ch vessels.
p rovide a direct or quan t it at ive assessm en t of flow. New er tech -
n iqu es are being developed to qu an t itate th e ICG sign al an d to
provide an in d icat ion of region al cerebral blood flow.13 Special Considerations
Occasion ally, access to t h e d ist al bran ch es of an an eu r ysm can
be lim ited by space or by th e desire to avoid excessive m an ipula-
t ion arou n d th e an eu r ysm dom e in cases of r u pt u red an eu r ysm s.
■ Intraoperative Flow Measurement In such cases, flow in th e bran ch es can be m easured in directly.
Direct qu an t it at ive m easurem en t of vessel flow in t raoperat ively, For exam p le, m easu rem en t of M1 flow p rovid es an in dicat ion
as en abled by devices su ch as an ult rason ic flow probe, can pro- of th e aggregate flow in th e M2 bran ch es an d can be u sed as th e
vide valu able data for decision m aking an d for assessing th e suc- baselin e m easurem en t . For an terior com m un icat ing ar ter y an -
cess of a su rgical in ter ven t ion . From a tech n ical perspect ive, th e eu r ysm s (ACoA), flow in th e A2s can be m easu red in direct ly by
u se of th e p robe requ ires th at a p or t ion of t h e vessel of in terest placing th e p robe on th e ip silateral A1 w h ile a tem porar y clip is
be d issected free so t h at t h e p robe can be h ooked arou n d t h e ap plied to th e con t ralateral A1.
vessel u n d er d irect vision . Th e field arou n d t h e p robe is filled Measu rem en t of flow from vessels sm aller th an h alf th e di-
w ith salin e. Blood flow is m easured an d recorded on a flow st rip am eter of th e probe m ay n ot be accu rate. Th erefore, th e relat ive
th at illu st rates both th e w aveform an d t h e m ean , m a xim u m , an d sizing of the probe is im portant . Furtherm ore, given that th e w idth
m in im u m flow. Th e m ean flow reading is ut ilized for com pari- of th e sm allest probe is 1.5 m m , ver y sm all vessels (< 1 m m ) are
son s before an d after in ter ven t ion . Measu rem en t s can be p er- n ot am en able to reliable m easu rem en t . Th erefore, vessels su ch
for m ed rep et it ively an d qu ickly as n eed ed t h rough ou t su rger y. as t h e p oster ior com m u n icat ing ar ter y (PCoA) or an ter ior ch o -
Ch an ges in p hysiological p aram eters can affect cerebral vessel roidal arter y can on ly be assessed w ell if th eir caliber is w ith in
flow. Sp ecifically, alterat ion s in blood pressu re, en d-t idal carbon th is range.
dioxide, an d an esth et ic m an euvers (su ch as bu rst su p p ression ) For com p lex, or in cases of large or ath erosclerot ic, an eu r ysm s
lead to physiologically expected flow alterat ion s. Th erefore, it is th at n eed m u lt ip le clip s to ach ieve com p lete obliterat ion , m ea-
im por t an t to m easu re flow u n der steady an esth et ic con dit ion s surem en t of flow w it h in t h e bran ch es after each su ccessive clip
to avoid m isin terpret at ion of any ch anges. ap p licat ion is an im por tan t m eth od to detect flow com prom ise.

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9 Intraoperative Evaluation of Blood Flow 133

a b

c d

Fig. 9.1a–d Flow m easurem ent in aneurysm surgery dem onstrated in a postischem ic hyperperfusion. (d) Flow measurem ents also can be used to
proxim al internal carotid artery (ICA) aneurysm. (a) Flow was m easured in assess the adequacy of collateral flow during temporary clipping of the ICA,
the prim ary distal branch, the middle cerebral artery (MCA), before clip- as dem onstrated, or to determ ine the safet y of parent vessel occlusion.
ping. (b) After clipping the flow in the MCA was m easured again, and a (From Am in-Hanjani S, et al. The utilit y of intraoperative blood flow m ea-
significant (> 50%) reduction was noted. (c) The clip was repositioned and surement during aneurysm surgery using an ultrasonic perivascular flow
flow returned to baseline. Often a temporary increase in flow is encoun- probe. Neurosurgery 2006;58:ONS-306. Reprinted with perm ission from
tered im m ediately after the clip is repositioned, consistent with transient Wolters Kluwer Health.)

Doing so allow s th e clip to be rep osit ion ed in a focu sed in divid- tain ed. A vasodilator y ch allenge can be ach ieved in t raoperat ively
u al m an n er w ith ou t th e n eed to rep lace th e en t ire clip con st ruct by in ducing hypercapn ea, an d en suring an appropriate in crease
after th e an eu r ysm base h as been recon st ru cted (Fig. 9.2). in flow follow ing a 10 m m Hg in crease in en -t idal CO2 .
Flow m easu rem en t s also can be u sed to assess th e adequ acy
of collateral flow an d toleran ce to prolonged tem porar y clipping
Interpretation
or even perm an en t vessel sacrifice. Th is scen ario is m ost t ypical
w ith proxim al ICA an eur ysm s w h ereby m easurem en t of flow in On a practical basis, the threshold for identification of vessel com -
th e M1 after tem p orar y occlu sion of th e ICA can be u sed to de- prom ise w hen com paring baseline and postclipping flow is > 25%
term in e if flow is m ain tain ed via th e ACoA or PCoA collaterals redu ct ion in flow. Th is th resh old w as ext rapolated from st udies
(Fig. 9.1d). Th is con cept can be exp an d ed to p er for m a clip oc- dem on st rat ing an elevated risk of cerebral isch em ia in p at ien ts
clu sion test if t h e n eed for p er m an en t vessel sacr ifice ar ises u n - w ith a > 25% reduct ion in cerebral blood flow at th e t im e of ca-
expectedly. Even if th ere is n o decrem en t in flow after a clip is rot id occlusion .15–17 It is corroborated by dat a th at in dicate th at
applied, a provocat ive vasodilator y ch allenge, akin to th e pro- an 80% n arrow ing of th e cross-sect ion al diam eter of a vessel is
vocat ive ch allenges used during balloon occlusion test ing (BOT), n eeded to decrease flow 25%.18 Most n eu rosu rgeon s w ou ld con -
can be ap plied to en su re th at cerebrovascu lar reser ve is m ain - sider th is degree of n arrow ing to be clin ically sign ifican t .

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134 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 9.2a–c Angiographic im ages from a 54-year-old woman with an


11-mm middle cerebral artery (MCA) aneurysm. Evidence of a slight enlarge-
m ent on follow-up im aging prompted the recom m endation for surgical
treatm ent. (a) Preoperative anterior view of angiogram dem onstrating ir-
regular right MCA aneurysm. (b) Preoperative three-dimensional angiogram,
posterior view of the aneurysm , dem onstrated M2 branches incorporated
into aneurysm neck. (c) Postoperative anterior view dem onstrated com -
plete clipping of the MCA using a stacked clip strategy assisted by repeated
intraoperative flow m easurem ents to m aintain patency of the M2 branches.
c (Courtesy of Sepideh Am in-Hanjani, Universit y of Illinois at Chicago.)

Using th is th resh old, a ret rosp ect ive st u dy of m ore th an 100 Flow Measurement in Cerebral
an eur ysm surgeries foun d th at flow m easurem en t s resulted in Revascularization Surgery
clips being rep osit ion ed in ~ 25% of cases.19 Fur th erm ore, th e
m easu rem en t s guided d ecision m aking in several cases by h elp - Cerebral revascu larizat ion can be ach ieved via ext racran ial-to-
ing to avoid u n n ecessar y clip rep osit ion ing in th ree pat ien ts an d intracranial (EC-to-IC) bypass surgery in appropriate patients. Var-
by allow ing safe vessel sacrifice in an oth er th ree pat ien ts. Using ious approach es u sing don or an d recipien t vessels, in terp osit ion
th e flow -based st rategy, n o u n expected large vessel occlusion s grafts, an d an astom otic tech n iques can be used. Decision m aking
or st rokes w ere en cou n tered. regarding th e specific t ype of bypass depen ds on m ultiple factors,

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9 Intraoperative Evaluation of Blood Flow 135

in clu ding th e availabilit y an d su it abilit y of sp ecific don or an d from t h e fragile basal collaterals t h em selves or from p seu d o -
recipien t vessels. Evalu at ing th e su ccess of th e bypass in t raop - an eu r ysm s th at develop on th ese deep vessels. Th e disease is
erat ively, n ot ju st in term s of p aten cy bu t also th e adequ acy of p rogressive an d it s m ed ical m an agem en t h as m ost ly been in -
it s fun ct ion based on flow m easurem en ts, is crit ical. Th e clin ical effective. Con sequ en tly, su rgical revascularization is con sidered
in d icat ion s for p er for m ing an EC-to-IC byp ass fall u n d er t w o th e t reat m en t of ch oice.24 Alth ough in direct revascularizat ion
gen eral categories: flow augm en tat ion for t reat m en t of cerebral tech n iques, em ploying on lay syn angioses, h ave proven ver y suc-
isch em ia, an d flow rep lacem en t for preser vat ion of flow du ring cessful in th e pediat ric populat ion , direct revascularizat ion w ith
vessel sacrifice (t ypically for t reat m en t of com plex an eur ysm s).20 bypass (alon e or in com bin at ion w ith on lay tech n iqu es) m ay
For both in dicat ion s, in t raoperat ive flow evalu at ion is an im por- offer m ore ben efit for adult pat ien t s.25,26
tan t com p on en t in execu t ing byp ass su rger y su ccessfu lly. Intraoperative blood flow m easurem ents during flow-augm en-
tat ion bypass can h elp opt im ize su rgical outcom es by allow ing
direct assessm en t of flow th rough th e byp ass an d p rovid es a
Bypass for Flow Augmentation
good p redictor of longer term bypass fun ct ion an d paten cy.27
A flow -augm en t at ion byp ass is aim ed at im p roving cerebral
blood flow to redu ce th e risk of cerebral isch em ia. It h as been
Technique
u sed to t reat con dit ion s su ch as m oyam oya disease an d ath ero-
sclerot ic cerebrovascu lar occlu sive disease of both th e an terior Bypass procedu res for flow augm en tat ion t ypically u se th e su-
an d posterior circulat ion . Bypass for ath erosclerot ic disease re- p erficial tem p oral ar ter y (STA) as a con du it to t h e MCA or, oc-
m ains lim ited in the w ake of random ized trials, m ost recently the casion ally, th e occipital ar ter y (OA) for revascularizat ion of th e
Carot id Occlu sion Su rger y St u dy (COSS), w h ich failed to dem on - posterior circu lat ion . In su ch set t ings, large in terp osit ion grafts
st rate th e efficacy of EC-to-IC byp ass com p ared w ith m edical u sin g t h e sap h en ou s vein or rad ial ar ter y are m ost ly avoid ed
m an agem en t of pat ien t s w ith sym ptom at ic carot id occlusion because of th e poten t ial for hyperperfusion h em orrh age from
an d h em odyn am ic com prom ise based on posit ron em ission to- ch ron ically isch em ic brain t issu e.28 Th e p rocedu re is u n der t aken
m ograp hy.21 How ever, th e st udy m eth odology m ay n ot h ave tar- in t h e stan dard fash ion , w ith th e don or vessel dissected an d pre-
geted th e pat ien ts at h igh est risk,22 an d th e risk of perioperat ive pared for an astom osis. Flow is th en m easu red at t w o poin t s in
st roke w as h igh er t h an opt im al. Th e overall im p licat ion is th at th e operat ion :
bypass is n ot a rout in e in ter ven t ion for pat ien ts w ith an in it ial
1. Th e cut flow of th e in sit u don or (STA or OA) is m easured by
isch em ic even t . How ever, selected pat ien t s w ith severe h em ody-
cut t ing th e vessel distally an d m easuring th e m a xim al carr y-
n am ic com prom ise an d recurren t sym ptom s despite m axim al
ing capacit y of th e vessel in th e absen ce of dow n st ream resis-
m edical th erapy m ay st ill w arran t un dergoing a bypass at an ex-
t an ce (Fig. 9.3a).
perienced center w ith appropriately low rates of perioperative
2. After th e an astom osis is com pleted an d th e tem porar y clips
m orbidit y.23
h ave been released, th e bypass flow in th e don or vessel is
Moyam oya disease represen ts progressive sten o-occlusive dis-
m easured (Fig. 9.3b).
ease of th e supraclin oid ICA an d its bran ch es. It is accom pan ied
by developm en t of a n et w ork of fin e basal collaterals. Th e t ypical In pat ien t s w ith isch em ic t issue, th e resist an ce in th e cor t ical
p resen t at ion is isch em ia from h em odyn am ic com p rom ise in recipien t bed w ould be exp ected to be low secon dar y to ch ron ic
t h e set t ing of in ad equ ate collaterals. Hem orrh age also can resu lt hypoperfusion an d result an t com pen sator y vasodilat ion . Subse-

a b

Fig. 9.3a,b Intraoperative flow m easurements perform ed in


flow-augm entation bypass. (a) Cut flow of donor superficial
temporal artery (STA) or occipital artery (OA) vessel. (b) Bypass
flow of graft after anastom osis. (Courtesy of Sepideh Am in-
Hanjani, Universit y of Illinois at Chicago.)

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136 II Evaluation and Treatment Considerations for Neurovascular Disease

quently, the bypass flow would be expected to approxim ate the cut m en t of skull base t u m ors involving m ajor vessels.31 Alth ough
flow of th e don or vessel. Th is rat io can be qu an t ified as follow s: sacrifice of m ajor vessels su ch as th e carot id ar ter y m ay be toler-
ated w ith ou t isch em ia, as m any as 30%of pat ien ts are vu ln erable
Cu t-flow in dex = Byp ass flow (m L/m in )/Cu t flow (m L/m in )
to isch em ia an d st roke.32 Th is p ercen tage of p at ien t s w arran ts
Th is sim ple in dex p rovid es in sigh t in to th e overall success of th e revascu larization w ith bypass. Furth erm ore, young patien ts w ith
bypass. A cu t-flow in dex n ear 1.0 in dicates a h igh ly successful th e risk of de n ovo an eu r ysm s over t im e an d p at ien t s w ith exis-
procedu re. ten t con t ralateral an eur ysm s also m ay w arran t a bypass before
vessel sacrifice.
Special Considerations Toleran ce to carot id sacrifice can best be evaluated w ith en do-
Th e d on or vessel can be p ron e to vasospasm du ring th e in it ial vascular BOT.33 Several criteria, in cluding clin ical, angiograph ic,
dissect ion an d p rep arat ion of th e vessel. It is im port an t to relieve elect rop hysiological, an d p erfu sion im aging fin dings, even in th e
any spasm to obtain an accurate cut-flow m easu rem en t . Spasm set t ing of p rovocat ive test ing w ith in du ced hyp oten sion , can be
can be relieved by w rap p ing th e vessel in a p ap averin e-soaked u sed to assess toleran ce to carot id occlusion . For pat ien t s w h o
cot tonoid after initial dissection. The cut flow of the donor is pro- fail BOT, th e resu lt s can h elp in form decision m aking regarding
portional to the length of the donor as predicted by Poiseuille’s th e m ode of revascu larizat ion . Pat ien t s w h o dem on st rate over t
law. Th u s, byp ass flow m ay act u ally exceed cu t flow if th e don or clin ical failu re based on rap id n eu rologic declin e lack all m ajor
vessel is trim m ed sh or ter after in it ial flow m easurem en t but be- collaterals an d requ ire rep lacem en t of t h e en t ire carot id flow
fore th e an astom osis is p erform ed. w ith a large in terposit ion graft con duit . Pat ien t s w ith lesser de-
grees of failu re m ay requ ire sm aller graft s or in sit u p ed icled
d on ors su ch as th e STA or OA. For com plex or fusiform an eu-
Interpretation
r ysm s of m ore distal in t racran ial vessels such as th e MCA or it s
Th e cu t-flow in dex ser ves as a u sefu l in dicator of byp ass fu n c- bran ch es, a replacem en t bypass is often required to aver t st roke
t ion . A low cu t-flow in dex can resu lt from in t rin sic or ext rin sic in th e territor y of th e vessel su bjected to acute occlusion for an -
errors, w h ich can be classified an d in terpreted as follow s. A t yp e eu r ysm t reat m en t becau se collaterals to term in al vessels ten d to
1 error sign ifies th at th e pat ien t’s h em odyn am ic stat us w as n ot be in adequate.
com p rom ised to a sign ifican t degree, resu lt ing in a lack of flow Th ere are a variet y of opt ion s for don or graft s for an EC-to-IC
dem an d on th e graft . Recogn it ion of th is t ype of error does n ot bypass for flow replacem en t . In sit u pedicled grafts such as th e
h elp alter th e op erat ive p lan . How ever, th e in form at ion can h elp STA ten d to h ave a h igh er paten cy an d longer longevit y rates
m odify future indications for perform ing the procedure. A t ype 2 com pared w ith in terposit ion graft s. Th ey also requ ire on ly on e
error sign ifies a tech n ical problem w ith th e graft . A t yp e 2A error an astom osis, m aking th em th e preferred opt ion w h en appropri-
involves issues w ith th e don or vessel su ch as ath erom a or calci- ate. Tradit ion ally, decision m aking about th e ch oice of appropri-
ficat ion s w ith in th e vessel or iat rogen ic inju r y during dissect ion . ate graft con du it h as been based on presu m ed flow an d carr ying
A t ype 2B error is a problem w ith th e an astom osis itself such as cap acit y in differen t don or t yp es. Sap h en ou s vein graft s are con -
th rom bosis at th e su t u re lin e. A t ype 2C error is a p roblem w ith sidered high flow, radial arter y grafts are considered in term ediate
graft ou tflow, eith er d u e to th e poor caliber of th e recipien t ves- flow, an d in sit u pedicle grafts such as STAs an d OAs are con sid-
sel or to a diseased recip ien t vascu lar bed w ith p roxim al occlu - ered low flow. How ever, direct in t raoperat ive flow m easu rem en t
sion or sten osis lim it ing ou tflow. provides a m ore robust basis for this im portant choice.34 Further-
Recogn it ion of th ese problem s can be aided by u sing video m ore, flow m easurem en ts provide ult im ate verificat ion of th e
ICG angiography to pinpoin t th e sou rce of th e problem such as success of th e bypass st rategy em ployed.
th rom bosis w ith in th e graft or an astom osis. Absen ce of su ch oc-
clu sion s sh ou ld raise con cern abou t a t yp e 2C error. Th is in for-
Technique
m at ion can guide in t raoperat ive act ion s, such as reopen ing an d
revising an an astom osis to rect ify a t ype 2B error or con sid ering Th ere are several in t raop erat ive flow m easu rem en t s relevan t for
a secon d bypass to a separate recipien t in th e case of t ype 2A or decision m aking related to a flow -rep lacem en t byp ass: th e flow
2C errors. In a st u dy of 51 flow -augm en tat ion bypasses, th e cut- through th e distal vessels associated w ith the aneur ysm , cut flow
flow in dex correlated w ell w ith long-term su ccess of th e bypass, in th e in sit u don or vessels (STA or OA) to determ in e it s adequacy
w ith a cut-flow in dex < 0.5 predict ing 50% paten cy com pared for flow replacem en t , an d flow in th e bypass con duit after com -
w ith 92%paten cy w h en th e cu t-flow in dex w as ≥ 0.5.27 Bypasses plet ion of th e an astom osis an d occlu sion of th e paren t vessel to
w ith a low cu t-flow in dex are often paten t at su rger y. Th e p re- verify adequ ate rep lacem en t.35
dictive value of th e cut-flow index highlights th e notion th at m ere Based on th is paradigm , w h en carot id sacrifice is n eeded for
an atom ic paten cy is n ot as usefu l in defin ing a successful proce- t reat m en t of p roxim al ICA an eu r ysm s, blood flow is m easu red in
dure as quan t itat ive in t raoperat ive bypass flow m easu rem en t s. th e dist al ICA if feasible or oth er w ise in t h e M1 (an d A1 if th e
an terior cerebral ar ter y [ACA] territor y is at risk). On ce baselin e
flow h as been m easured, th e carot id is tem porarily occluded
Bypass for Flow Replacement
w ith a clip an d th e flow is rem easured in th e distal vessels. Th e
A flow -replacem en t bypass is perform ed in the set ting of planned decrem en t in blood flow (th e flow deficit) in dicates th e am ou n t
vessel sacrifice, as en coun tered w ith com plex in t racran ial an eu- of blood flow th at m ust be provided by th e bypass con du it to
r ysm s th at are n ot am en able to direct su rgical or en dovascular allow th e vessel to be sacrificed safely (Fig. 9.4). For m ore dist al
obliteration w ithout parent vessel com prom ise.29,30 Occasionally, an eur ysm s, flow in th e vessel it self or its im m ediate bran ch es is
flow -replacem en t bypass is also in dicated w ith aggressive t reat- m easured (th e distal territor y flow ) an d in dicates th e flow th at

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9 Intraoperative Evaluation of Blood Flow 137

Fig. 9.4a–c The steps for using intraoperative flow m easurem ents to im - (c) After the bypass, perm anent proxim al occlusion of the vessel is per-
plement a flow-replacement bypass for proximal internal carotid artery (ICA) form ed. Graft patency is confirm ed by flow m easurem ent. In this illustra-
aneurysm s. (a) Following exposure of the cervical ICA and intracranial ves- tion, due to the large size of the interposition conduit, the graft flow can
sels, baseline flow in the M1 is m easured. If necessary, the A1 flow also can even exceed the previously m easured flow deficit to approxim ate full flow
be m easured if the anterior cerebral artery territory has no collateral flow within the native carotid artery. As long as the flow m atches or exceeds the
through the anterior com m unicating artery. (b) With a tem porary clip flow deficit, the territory has been revascularized successfully. (From Am in-
on the cervical ICA, flow in the M1 (and A1, if appropriate) is remeasured. Hanjani S, Alaraj A, Charbel FT. Flow-replacem ent bypass for aneurysm s:
In this example, flow dropped from 70 m L/m in to 20 m L/m in indicating a decision-m aking using intraoperative blood flow m easurem ent s. Acta
flow deficit of 50 mL/m in. The superficial temporal artery cut flow is m ea- Neurochir (Wien) 2010;152:1021–1032. Reprinted with perm ission from
sured. If flow is inadequate to supply the flow deficit, an interposition graft Springer.)
is placed from the external carotid artery to the m iddle cerebral artery.

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138 II Evaluation and Treatment Considerations for Neurovascular Disease

th e byp ass m u st provide (Fig. 9.5). On ce th e flow deficit or dist al an d 9.7). In th is m an n er, th e ch oice of graft can be t ailored to th e
territor y flow h as been establish ed, th e flow capacit y of acces- flow replacem en t n eeded. At th e com plet ion of th e bypass, re-
sible in sit u pedicle graft s (STA or OA depen den t on an eu r ysm gardless of w h eth er an STA, OA, or in terposition graft is used, th e
locat ion ) can be determ in ed by m easu ring th e cu t flow of th e flow in th e graft is m easured to con firm th at th e bypass is pro-
vessel. viding adequate flow. Adequ ate flow is equ al to t h e flow deficit
or dist al territor y flow th at w as m easured at baselin e. Th is m ea-
su rem en t p rovides a fin al qu an t itat ive con firm at ion of su ccess,
Interpretation
n ot on ly of th e tech n ical aspects of th e surger y but also of th e
If th e cut flow m easu red is adequate to provide th e n eeded flow, bypass st rategy overall. It is th us superior to purely an atom ic in -
th e sim p ler in sit u p edicled graft can be u t ilized. Oth er w ise, an form at ion gain ed from video ICG or conven t ion al in t raoperat ive
in terp osit ion radial arter y or vein graft m u st be used (Figs. 9.6 angiography alon e.

b c

Fig . 9.5a–c The steps for using intraoperative flow m easurem ent s to (c) The aneurysm is obliterated by trapping the aneurysm al M1 segment.
im plem ent a flow-replacem ent bypass for term inal aneurysm s. (a) A fusi- The final patency and adequacy of the bypass are confirm ed by m easuring
form M1 aneurysm is illustrated. Flow m easured in both M2 branches totals graft flow, which, at 65 m L/m in provides complete flow replacem ent to the
65 m L/m in. The cut flow of the superficial tem poral artery (STA) is m ea- distal middle cerebral artery territory. (From Am in-Hanjani S, Alaraj A,
sured and is found to approxim ate this distal territory flow at 60 m L/m in. Charbel FT. Flow replacement bypass for aneurysms: decision-making using
(b) Anastom osis is perform ed bet ween the STA and an M3 branch. Initial intraoperative blood flow m easurem ents. Acta Neurochir (Wien) 2010;152:
patency of the bypass is confirmed by measuring the flow in the bypass 1021–1032. Reprinted with perm ission from Springer.)
graft, but it is expected to be low given that the parent vessel is still open.

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9 Intraoperative Evaluation of Blood Flow 139

a
b

Fig. 9.6a–c A 27-year-old man with a family history of cerebral aneurysms


presented with headaches and a large partially throm bosed aneurysm of
the distal M1. At surgery, the aneurysm was found to be partially fusiform .
Flow in the branches of the m iddle cerebral artery (MCA), representing the
distal territory flow, m easured 51 m L/m in. The superficial temporal artery
(STA) cut flow was 127 m L/min and thus adequate for revascularization of
the dist al territory. An STA-to-MCA bypass was perform ed with occlusion
of the M1 proxim al to the aneurysm . The final bypass flow m easured 45
m L/m in, approxim ating the distal territory flow and confirm ing successful
flow replacement. (a) Preoperative angiographic anteroposterior view of
the right internal carotid artery injection of the aneurysm shows filling of a
portion of the aneurysm , just proxim al to the MCA bifurcation. (b) Pre-
operative coronal view of computed tom ography angiogram dem onstrates
the throm bosed component of the aneurysm (arrows). (c) Postoperative
angiographic anteroposterior view of right external carotid artery injection
dem onstrates the patent STA bypass with filling of the MCA branches and
occlusion of the aneurysm . (Courtesy of Sepideh Am in-Hanjani, Universit y
c of Illinois at Chicago.)

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140 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

Fig. 9.7a,b A 53-year-old wom an with a recurrent giant left ophthalm ic vein graft was placed from the STA stump to the m iddle cerebral artery
aneurysm , previously stented and coiled m ultiple times, experienced pro- (MCA). The initial flow through the graft was only 3 mL/m in with the ICA
gressive visual loss. Angiography showed an isolated hem isphere without open. With proxim al occlusion of the ICA, flow through the graft increased
evidence of an anterior com m unicating artery and posterior com municat- to 62 m L/m in, m atching the flow deficit as measured. (a) Preoperative an-
ing artery. Clinically, she failed preoperative balloon occlusion testing soon giographic anteroposterior view of the partially coiled and stented right
after balloon inflation. At surgery, flow in the A1 and M1 m easured 62 m L/ ophthalm ic artery aneurysm . (b) Postoperative angiographic anteroposte-
m in and dropped m arkedly to 2 m L/m in upon temporary internal carotid rior view of the STA to short vein graft filling the MCA and anterior cerebral
artery (ICA) occlusion, indicating a flow deficit of 60 m L/m in. The superfi- artery territories. (Courtesy of Sepideh Am in-Hanjani, Universit y of Illinois
cial temporal artery (STA) branch cut flow was inadequate, but the cut flow at Chicago.)
of the large STA stump was 120 m L/m in. Therefore, a short interposition

flow m easurem en t com plem en t oth er operat ive adjun cts such
■ Conclusion as conven t ion al/video ICG angiography an d elect rophysiological
In t raoperat ive direct vessel flow m easu rem en ts provide im por- m on itoring. Furth erm ore, flow -assisted con cepts an d tech n iques
tan t in form at ion for decision m aking an d for opt im izat ion of can be im p lem en ted qu ickly an d easily in to th e cerebrovascu lar
cerebrovascular surger y for th e t reat m en t of an eur ysm s an d th e surgeon’s tool kit .
creation of an EC-to-IC bypass. The techniques and philosophy for

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t ive m icrovascular Doppler sonography in an eur ysm su rger y. Neu rosur- an d t issue oxygen at ion . Br J An aesth 2009;103(Suppl 1):i3–i13
ger y 1997;40:965–970, discussion 970–972 8. Sch ram m J, Koht A, Schm idt G, Pechstein U, Tan iguch i M, Fah lbu sch R.
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flow probe: tech n ique an d applicat ion in n eurosurger y. Neurol Res 1998; an eu r ysm s w ith evoked p oten t ial m on itor ing. Neu rosu rger y 1990;26:
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3. Lu ndell A, Bergqvist D, Mat t sson E, Nilsson B. Volum e blood flow m ea- 9. Tang G, Caw ley CM, Dion JE, Barrow DL. In t raoperat ive angiography dur-
su rem en t s w ith a t ran sit t im e flow m eter: an in vivo an d in vit ro variabil- ing an eur ysm su rger y: a prospect ive evalu at ion of efficacy. J Neu rosurg
it y an d validat ion st udy. Clin Physiol 1993;13:547–557 2002;96:993–999
4. Choksey MS. Cortical therm al clearance as a predictor of im m inent neuro- 10. Klopfen stein JD, Spet zler RF, Kim LJ, et al. Com p arison of rou t in e an d se-
logical deterioration. Cerebrovasc Brain Metab Rev 1996;8:230–271 lect ive u se of in t raop erat ive an giograp hy d u r in g an eu r ysm su rger y: a
5. Carter LP. Su rface m on itoring of cerebral cort ical blood flow. Cerebrovasc prospect ive assessm ent . J Neu rosurg 2004;100:230–235
Brain Met ab Rev 1991;3:246–261 11. de Oliveira JG, Beck J, Seifer t V, Teixeira MJ, Raabe A. Assessm en t of flow
6. Calderon-Arnulphi M, Alaraj A, Am in-Hanjani S, et al. Detection of cerebral in perforat ing arteries during in t racran ial an eur ysm surger y using in t ra-
isch em ia in n eurovascular surger y using quan t it at ive frequen cy-dom ain operat ive n ear-in frared indocyan in e green videoangiography. Neurosur-
n ear-in frared spect roscopy. J Neu rosurg 2007;106:283–290 ger y 2007;61(3, Suppl):63–72, discussion 72–73

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9 Intraoperative Evaluation of Blood Flow 141

12. Raabe A, Nakaji P, Beck J, et al. Prospect ive evaluat ion of surgical m icro- 24. Kuroda S, Houkin K. Moyam oya disease: cu rren t con cept s an d fut ure per-
scope-integrated in t raoperat ive near-in frared in docyan in e green video- spect ives. Lan cet Neurol 2008;7:1056–1066
angiography during an eur ysm surger y. J Neurosurg 2005;103:982–989 25. Houkin K, Kuroda S, Ish ikaw a T, Abe H. Neovascularizat ion (angiogenesis)
13. Kam p MA, Slot t y P, Turow ski B, et al. Microscope-in tegrated quan t it at ive after revascu larizat ion in m oyam oya disease. W h ich tech n iqu e is m ost
analysis of in t raoperat ive in docyan in e green fluorescen ce angiography useful for m oyam oya disease? Act a Neurochir (Wien ) 2000;142:269–276
for blood flow assessm en t: first experien ce in 30 pat ien t s. Neu rosurger y 26. Bang JS, Kw on OK, Kim JE, et al. Quan t it at ive angiograph ic com parison
2012;70(1, Suppl Operat ive):65–73, discussion 73–74 w ith the OSIRIS program bet w een the direct an d in direct revasculariza-
14. Am in -Hanjan i S, Ch arbel FT. Flow -assisted surgical tech n ique in cerebro- t ion m odalit ies in adult m oyam oya disease. Neurosurger y 2012;70:625–
vascular surger y. Surg Neurol 2007;68(Suppl 1):S4–S11 632, discussion 632–633
15. Ch arbel FT, Zh ao M, Am in -Hanjan i S, Hoffm an W, Du X, Clark ME. A 27. Am in -Hanjan i S, Du X, Mlin arevich N, Meglio G, Zh ao M, Ch arbel FT. Th e
p at ien t-sp ecific com puter m odel to predict outcom es of th e balloon oc- cut flow in dex: an in t raoperat ive predictor of th e success of ext racranial-
clusion test . J Neurosurg 2004;101:977–988 in t racranial bypass for occlusive cerebrovascular disease. Neu rosurger y
16. Ecker t B, Th ie A, Car vajal M, Groden C, Zeum er H. Predict ing h em ody- 2005;56(1, Su p pl):75–85, discu ssion 75–85
n am ic isch em ia by t ran scran ial Doppler m on itoring during th erapeut ic 28. St iver SI, Ogilvy CS. Acute hyper perfusion syn drom e com plicat ing EC-IC
balloon occlu sion of th e in tern al carot id ar ter y. AJNR Am J Neu roradiol bypass. J Neurol Neurosurg Psychiat r y 2002;73:88–89
1998;19:577–582 29. Kalan i MY, Zabram ski JM, Nakaji P, Spet zler RF. Bypass an d flow reduct ion
17. Jaw ad K, Miller D, Wyper DJ, Row an JO. Measurem en t of CBF an d carot id for com plex basilar an d ver tebrobasilar jun ct ion an eur ysm s. Neurosur-
arter y pressure com pared w ith cerebral angiography in assessing collateral ger y 2013;72:763–775, discussion 775–776
blood supply after carot id ligat ion. J Neurosurg 1977;46:185–196 30. Kalan i MY, Zabram ski JM, Hu YC, Spet zler RF. Ext racran ial-in t racran ial
18. Spen cer MP, Reid JM. Quant it at ion of carot id sten osis w ith con t in uous- bypass an d vessel occlu sion for th e t reat m en t of u n clip pable gian t m id dle
w ave (C-W) Dop pler u lt rasou n d. St roke 1979;10:326–330 cerebral ar ter y an eu r ysm s. Neu rosu rger y 2013;72:428–435, d iscu ssion
19. Am in -Hanjan i S, Meglio G, Gat to R, Bauer A, Ch arbel FT. Th e ut ilit y of 435–436
in t raoperat ive blood flow m easurem en t during an eur ysm surger y using 31. Kalan i MY, Kalb S, Mar t irosyan NL, et al. Cerebral revascularizat ion and
an u lt rason ic p erivascu lar flow p robe. Neu rosu rger y 2008;62(6, Su pp l 3): carot id ar ter y resect ion at th e skull base for t reat m en t of advan ced h ead
1346–1353 an d n eck m align an cies. J Neu rosu rg 2013;118:637–642
20. Ch arbel FT, Guppy KH, Ausm an JI. Cerebral revascularizat ion : superficial 32. Nish ioka H. Result s of the t reat m en t of in t racran ial an eur ysm s by occlu-
tem poral m iddle cerebral arter y an astom osis. In : Sekh ar LN, Fessler RG, sion of the carotid artery in the neck. J Neurosurg 1966;25:660–704
eds. Atlas of Neurosurgical Tech n iqu es. New York: Thiem e; 2006 33. Eckard DA, Purdy PD, Bon te FJ. Tem porar y balloon occlusion of th e carot id
21. Pow ers W J, Clarke W R, Gr ubb RL Jr, Videen TO, Adam s HP Jr, Derdeyn CP; arter y com bined w ith brain blood flow im aging as a test to predict toler-
COSS Invest igators. Ext racran ial-in t racran ial bypass surger y for st roke an ce prior to perm an en t carot id sacrifice. AJNR Am J Neuroradiol 1992;
prevention in hem odynam ic cerebral ischem ia: the Carot id Occlusion Sur- 13:1565–1569
ger y St udy ran dom ized t rial. JAMA 2011;306:1983–1992 34. Ash ley W W, Am in -Hanjan i S, Alaraj A, Sh in JH, Ch arbel FT. Flow -assisted
22. Carlson AP, Yon as H, Ch ang YF, Nem oto EM. Failure of cerebral h em ody- surgical cerebral revascularizat ion. Neurosurg Focus 2008;24:E20
n am ic select ion in gen eral or of specific posit ron em ission tom ography 35. Am in -Hanjan i S, Alaraj A, Ch arbel FT. Flow replacem en t bypass for an eu-
m eth odology?: Carot id Occlusion Surger y St udy (COSS). St roke 2011;42): r ysm s: decision -m aking using in t raoperat ive blood flow m easurem en t s.
3637–3639 Act a Neuroch ir (Wien ) 2010;152:1021–1032, discussion 1032
23. Am in -Hanjan i S, Ch arbel FT. Is ext racran ial-in t racran ial bypass surger y
effect ive in cer t ain pat ien t s? Neurol Clin 2006;24:729–743

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10 Neuroanesthesia
Alana M. Flexm an and Pekka O. Talke

Th e p rovision of an esth esia for n eu rovascu lar su rger y is based au toregu lat ion globally or region ally. Sim ilarly, ot h er var iables
on th e com plex in teract ion s bet w een cerebrovascu lar physiol- u n der an esth esia su ch as hypercapn ia, hypoth erm ia, an d som e
ogy an d th e un ique surgical an d an esth esia requirem en t s for th is an esth et ic agen ts can im pair th e abilit y of th e brain to autoregu-
pat ien t pop u lat ion . Th is ch apter review s th e effects of an esth esia late cerebral blood flow.1 On ce au toregu lat ion is disr u pted, cere-
on cerebral physiology an d n europhysiological m on itoring an d bral blood flow is lin early related to system ic blood pressure, an d
th e preop erat ive evaluat ion of th ese p at ien t s. Fin ally, th e an es- excessive h em odyn am ic derangem en ts m u st be avoided.
th esia con siderat ion s for specific n eu rovascu lar proced u res, both In t raven ou s an esth et ic agen ts such as propofol an d th iopen -
in an d out of th e op erat ing room , are review ed. tal con st rict cerebral blood vessels an d suppress CMRO2 w h ile
Alth ough n eu rop hysiology an d ph arm acology are u n iversally preser ving flow -m et abolism cou pling. As a resu lt , th ese agen ts
th e sam e, n eu roan esth esia tech n iqu es are n ot . Cu rren t eviden ce redu ce cerebral blood flow an d ICP. Propofol also preser ves cere-
does n ot clearly su p port on e specific an esth esia regim en over bral autoregulation in healthy patients, although this effect m ight
an oth er, an d an esth esia m an agem en t is often guided by in st it u- n ot exten d to areas of injured brain .1 Ben zodiazep in es an d opi-
t ion al preferen ce an d fam iliarit y. Opt im al resu lt s are m ost likely oid m edicat ion s reduce cerebral blood flow an d CMRO2 bu t to a
to be ach ieved by a team of experien ced n eurosurgeon s, n euro- m u ch lesser degree th an p rop ofol or barbit u rates. Dexm edeto-
an esth esiologists, an d n urses w h o use dr ugs an d tech n iques th at m id in e redu ces cerebral blood flow an d CMRO2 an d h as n o effect
are fam iliar an d con sisten t w ith th e gen eral prin cip les of n eu ro- on ICP. Overall, in t raven ous an esth esia using an esth et ic drugs
an esth esia. su ch as p rop ofol, in com bin at ion w ith an op ioid, provides favor-
able ch anges in cerebral blood flow an d CMRO2 an d is often u sed
for n eurosurgical pat ien t s.
Volatile anesthetic agents (sevofluran e, desflurane, isoflurane)
h ave im por tan t effects on CMRO2 , cerebral au toregu lat ion , an d
■ Anesthesia and Cerebral Blood Flow cerebral blood flow. All volat ile anesth et ics are poten t cerebral
Cerebral blood flow is an im por t an t determ in an t of in t racran ial vasodilators an d th erefore in crease ICP at h igh er doses. All vola-
p ressu re (ICP) an d in t raop erat ive brain ed em a. W h en a p at ien t t ile an esth et ics disru pt cerebral au toregu lat ion , redu ce CMRO2
is u n d er an esth esia, cerebral blood flow is m odu lated by m u l- in a d ose-d ep en d en t fash ion , an d at ten u ate flow -m et abolism
t iple factors, in clu ding p ar t ial pressu re of carbon dioxide (PaCO2 ), cou p lin g at h igh er d oses (> 1.5–2 m in im u m alveolar con cen t ra-
par t ial pressu re of ar terial oxygen (PaO2 ), cerebral m et abolic rate t ion [MAC]).1 Sevoflu ran e is th ough t to preser ve cerebral auto-
(CMRO2 ), cerebral au toregu lat ion , an d an esth et ic agen t s. Hyp er- regu lat ion to a greater exten t th an do oth er volat ile an esth et ics
ven t ilat ion an d reduct ion of PaCO2 are often u sed in t raopera- an d th us m ay be preferable.1
t ively to acu tely redu ce ICP th rough a redu ct ion in cerebral blood Nit rou s oxide h as several th eoret ical disadvan t ages, in clu ding
flow. Bet w een 20 an d 80 m m Hg, PaCO2 an d cerebral blood flow m ild in creases in cerebral blood flow an d CMRO2 as w ell as exac-
are linearly related w ith a 3 to 4%change in cerebral blood flow for erbat ion of p n eu m ocep h alu s after closu re of th e sku ll.3 Despite
ever y 1 m m Hg change in PaCO2 .1 The effect of PaCO2 on cerebral th ese con cern s, th e u se of n it rou s oxide h as n ot been correlated
blood flow is m ediated th rough ch anges in th e pH of th e perivas- w ith poor clin ical outcom es, an d it con t in ues to be used at m any
cular cerebrospin al fluid an d last s 6 to 8 h ours due to in creases in st it ut ion s. Overall, volat ile an est h et ic agen t s h ave th eoret ical
in bicarbon ate levels in th e cerebrospin al fluid.2 Excessive an d disadvantages over in traven ous agents for patients w ith increased
prolonged hyper ven t ilat ion (PaCO2 < 30 m m Hg) is t ypically ICP or decreased in t racran ial com plian ce.
avoided du e to th e risk of cerebral isch em ia. Conversely, cerebral Th e u se of etom idate an d ket am in e du ring n eu rosurger y is
blood flow in creases expon en t ially w ith sign ifican t reduct ion s con t roversial. In earlier st u dies ket am in e in creased CMRO2 an d
in PaO2 below ~ 50 m m Hg. CMRO2 closely in fluen ces cerebral cerebral blood flow. Traditionally, these agents have been avoided
blood flow through a process of flow -m etabolism coupling. Flow - in patients w ith decreased intracranial com pliance, although their
m et abolism cou p ling en su res th at ch anges in CMRO2 are accom - effect s m ay be at ten u ated in th e presen ce of oth er an esthet ic
pan ied by a propor t ion al ch anges in cerebral blood flow. drugs.4 Etom idate redu ces CMRO2 an d cerebral blood flow, an d
Au toregu lat ion is a p rotect ive m ech an ism th at m ain t ain s it provides a stable h em odyn am ic p rofile. Despite th is favorable
ad equate cerebral blood flow at a m ean ar terial blood pressure profile, etom idate h as disadvan tages. Etom idate h as exacerbated
of 50 to 150 m m Hg in th e h ealthy adu lt brain . Th e safe lim it s of cerebral isch em ic injur y in experim en t al an im al m odels an d in a
autoregu lat ion m ay be sh ifted by factors su ch as ch ron ic hyper- clin ical t rial of p at ien t s u n dergoing an eu r ysm clip ping, p ossibly
ten sion an d an em ia. In t racran ial injur y or path ology can disrupt du e to in h ibit ion of n it ric oxide syn th ase.5,6 For th ese reason s,

142

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10 Neuroanesthesia 143

th e u se of etom idate in p at ien t s u n dergoing n eu rologic p roce- given to redu ce cerebral sw elling, alth ough th eir effects m ay be
dures h as fallen from favor. delayed.

■ Management of Intracranial ■ Fluid Administration for


Hypertension Neurosurgical Patients
Many pat ients in need of in tracranial vascular n eurosurger y have Th e opt im al flu id adm in ist rat ion for n eu rosu rgical p at ien t s re-
overt sign s an d sym ptom s of in creased ICP, an d even asym ptom - m ain s con t roversial. Lit tle guidan ce is provided by th e cu rren t
at ic pat ien ts m ay h ave decreased in t racran ial com plian ce. In t ra- literat u re, alth ough several th eoret ical p rin cip les are com m on ly
cran ial hyper ten sion , often related to edem a of th e cerebral t is- u sed. Glucose-con t ain ing solut ion s are avoided due to th e p o-
su e or in t racran ial bleeding, n ot on ly com p rom ises blood flow to ten t ial det rim en tal effects of hyperglycem ia on th e injured brain .
th e brain bu t creates su bopt im al operat ing con dit ion s an d in - Hypotonic fluids are also avoided due to the transfer of free w ater
creases th e risk of m align an t in t raoperat ive brain sw elling. Sub - in to brain t issue an d th e t h eoret ical risk of cerebral edem a.12 Al-
du ral p ressu re in dep en den tly p redicts in t raop erat ive brain th ough lact ated Ringer’s solu t ion is sligh t ly hyp oton ic, it is used
sw elling after th e d u ra m ater is op en ed.7 Non operat ive st rategies routinely w ithout know n com plications. Hyperosm olar solutions
to reduce in t racran ial hyper ten sion are an essen t ial com pon en t su ch as m an n itol an d hyp er ton ic salin e are com m on ly u sed to
of th e an esth esia m an agem en t of n eu rovascu lar surger y. redu ce cerebral w ater con ten t an d ICP related to w ater m oving
Th e in t racran ial com par t m en t is com posed of brain t issu e, ce- out of brain t issu e.12 In sen sible losses an d u rin ar y ou t p u t sh ou ld
rebral blood volum e, cerebrospinal fluid, and pathological lesions. be replaced, especially in pat ien t s given m an n itol or oth er di-
St rategies to redu ce ICP m u st t arget on e of th ese com pon en t s u ret ics. We t ypically replace at least h alf of th e m an n itol-in duced
(Table 10.1). Cerebral blood flow m ay be m odified rapidly through u rin e ou t pu t w ith int raven ou s fluids. Th eoret ically, in t ravascu-
several m ech an ism s, w h ich are often m an ip u lated du ring an es- lar volu m e rep lacem en t sh ou ld n ot in crease brain ed em a as long
th esia for n eu rosu rger y. Hyp er ven t ilat ion , w h ich is frequen tly as n orm al or elevated seru m osm olarit y is m ain tain ed.12
used, effect ively redu ces in t raop erat ive brain bu lk an d ICP.8 Th e Occasionally, iso-oncotic colloid solutions containing album in
cerebral vasocon st rict ive effect s of in t raven ous an esth et ic agen t s or syn t h et ic st arch es are u sed, alt h ough few clin ical t r ials su p -
su ch as propofol are often u sed to redu ce cerebral blood flow. p or t t h eir u se over cr yst alloid solu t ion s in n eu rosu rgical p a-
Cerebral ven ou s congest ion sh ou ld be m in im ized by elevat ing t ien ts, an d som e eviden ce suggest s p oten t ial h arm to p at ien t s
th e h ead an d avoiding com p ression of in tern al jugu lar vein s. Th e w ith t raum at ic brain injur y w h o receive album in solu t ion s.14
con t ribu t ion of posit ive en d-exp irator y p ressu re to ICP is con t ro- Furth er research is required to con firm th ese fin dings an d to de-
versial, alth ough low levels (less th an ICP) appear to be safe.9 term in e w h eth er th ese results are applicable to oth er n eurosur-
Man n itol an d hyp er ton ic flu ids draw brain w ater in to t h e in t ra- gical pat ien t s, in cluding n eurovascu lar pat ien ts. Syn th et ic st arch
vascu lar com par t m en t an d also effect ively reduce brain t issue solu t ion s h ave been associated w ith an in creased risk of coagu -
volum e an d ICP.10,11 High does of m an n itol sh ould be used cau- lopathy, w h ich could h ave disast rous con sequen ces in n eu rosur-
t iou sly becau se hypon at rem ia, hyp erkalem ia, congest ive h ear t gical pat ien ts.15
failu re, an d sign ifican t dehydrat ion can resu lt .10,12 Fu rosem id e is Tran sfu sion th resh olds in p at ien t s w h o are n eu rologically
often used in com bin at ion w ith m an n itol to reduce in t racran ial com prom ised du e to in t racran ial h em orrh age, t rau m a, or su r-
hyper ten sion , alth ough th e efficacy of th is drug is n ot clearly es- ger y rem ain un kn ow n . In obser vat ion al st udies of pat ien ts w ith
t ablish ed .13 Fu rosem id e m ay act by red u cing brain w ater an d su barach n oid h em orrh age, both an em ia an d blood t ran sfu sion
th e production of cerebrospin al fluid.12 Fin ally, steroids are often w ere associated w ith poor n eurologic outcom es.16,17 It is u n clear,
h ow ever, w h eth er an em ia is a m arker of poor outcom e or causes
poor ou tcom e. Fu r th erm ore, blood t ran sfu sion is associated w ith
com p licat ion s su ch as in fect ion , acu te lu ng inju r y, h em olysis,
Table 10.1 Anesthesia Strategies to Reduce Intracranial Pressure
an d im m u n osuppression an d sh ou ld be avoided if possible.18 A
Intracranial recen t st udy dem on st rated th at h em oglobin levels below 9 g/dL
Component Strategy w ere associated w ith eviden ce of cerebral t issu e hypoxia,19 an d
Cerebral blood volume Hyperventilation th is m ay be a reason able t h resh old u n t il fu r th er research is com -
Avoid hypoxemia pleted . Excessive t ran sfu sion sh ou ld be avoided becau se an ele-
Avoid excessive hypertension vated hem atocrit can increase blood viscosit y and reduce cerebral
Total intravenous anesthesia blood flow.
Elevation of the head
Avoid compression of internal jugular veins
Brain tissue volume Osmotic diuretics
Hypertonic saline ■ Anesthesia and Cerebral Protection
Furosemide Th e goals of cerebral p rotect ion du ring an esth esia are to preven t
Steroids
prim ar y an d secon dar y cerebral inju r y related to in adequ ate ce-
Cerebrospinal fluid Furosemide
rebral blood flow an d oxygen deliver y an d to supp ress epilept ic
Carbonic anhydrase inhibitors
act ivit y. Secon dar y n eurologic inju r y is th ough t to result from

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144 II Evaluation and Treatment Considerations for Neurovascular Disease

several factors in clu ding apoptosis, in flam m at ion , in h ibit ion of clin ical p rogn osis or if th ey p lay a cau sat ive role. How ever, a con -
protein synthesis, and oxidative stress, all of w hich m ay be poten - ser vat ive ap proach suggest s both sh ou ld be avoided in pat ien ts
tial t arget s for n eu roprotect ive th erapies after an acu te isch em ic w ith cerebral injur y.
insult.5 Several strategies, including hypotherm ia, adm inistration Evid en ce to d em on st rate clin ical n eu rop rotect ion from sp e-
of an esth et ic agen ts, an d im plem en tat ion of st rict glucose con - cific an est h esia tech n iqu es or from t h e u se of p eriop erat ive
t rol, h ave been prop osed.4,5,20,21 hyp ot h erm ia is lim ited . Given t h is u n cer t ain t y, som e cen ters
Th e p oten t ial n eu rop rotect ive effect of an esth et ic agen t s h as con t in u e to advocate n eu rop rotect ive st rategies. Regard less of
been th e focus of a sign ifican t am ou n t of research . Many an es- th e an esth esia tech n iqu e ch osen , th e an esth esia p rovid er sh ou ld
t h et ic d r ugs, in clu d in g barbit u rates, p rop ofol, ket am in e, etom i- m ain tain adequate cerebral perfu sion pressure, m in im ize ICP,
date, d exm ed etom id in e, an d volat ile an est h et ics, h ave been an d avoid hyperglycem ia to m in im ize cerebral inju r y.
selected as p oten t ial n eu rop rotect ive agen t s given t h eir abilit y
to profou n d ly su p p ress t h e cerebral m et abolic rate or p rod u ce
an isoelect ric elect roen cep h alograp h ic (EEG) w aveform . In p ar-
t icular, barbit u rates h ave been con sidered th e “gold stan dard” ■ Neurophysiological Monitoring
for n eu roprotect ion after early st u dies sh ow ed th eir abilit y to
profou n dly su p p ress th e EEG an d to im p rove long-term n eu ro-
and Anesthesia
logic ou tcom e in an im al m od els.20 Su bsequ en t an im al st u d ies Intraoperative neurophysiological m onitoring has had a significant
have produced con flicting results. Although barbiturates can pro- effect on an esth esia tech n iqu es during n eu rovascular surger y.
du ce an isoelect ric EEG an d su p press m etabolic rate by ~ 50%, Evoked poten t ial (sen sor y an d m otor), EEG, an d elect rom yogra-
th ese ben efit s m ay be in effect ive in th e set t ing of severe global phy (EMG) m on itoring can be u sed du ring n eu rovascu lar su r-
isch em ia or m u lt iple isch em ic in sults w h en th e EEG becom es ger y d ep en d in g on t h e an atom ic st r u ct u res at r isk. An est h esia
isoelect ric w ith in m in u tes of cessation of cerebral blood flow.20 m an agem en t is often a balan ce bet w een ad equ ate an est h esia
Furth erm ore, variat ion s in th e severit y of th e isch em ic in sult , d ept h , opt im izing op erat ing con d it ion s, an d facilit at ing in t ra-
duration of neuroprotective th erapy, an d follow -up care likely ac- op erat ive n eu rop hysiological m on itor ing. Given t h e p oten t ial
count for conflicting results.21 Clinical trials have not supported a con flict s am ong t h ese goals, good com m u n icat ion bet w een th e
clinically relevant neuroprotective effect for any anesthetic agen t, surger y an d an esth esia team s is essen t ial.
in clu ding barbit urates. Th e In tern at ion al Hypoth erm ia during All an est h et ic agen t s h ave t h e p oten t ial to red u ce t h e am p li-
An eu r ysm Su rger y Trial (IHAST) fou n d n o associat ion bet w een t u d e an d to in crease t h e laten cy of som atosen sor y evoked p o -
im proved ou tcom es an d th e use of sup plem en t al n europ rotec- ten t ials (SSEPs) an d m otor evoked p oten t ials (MEPs). At h igh
t ive drugs (th iop en tal or etom idate) du ring tem p orar y clip ping con cen t rat ion s (> 1 MAC), volat ile an est h et ic agen t s (sevoflu -
in cerebral an eu r ysm su rger y, eith er w ith or w ith ou t m ild hypo- ran e, desflu ran e, isofluran e) abolish SSEPs an d MEPs.31 At low
th erm ia.22 Overall, cu rren t eviden ce does n ot support a n euro- con cen t rat ion s (< 0.5 MAC), th ese agen t s h ave m in im al effect on
protect ive role for an esth et ic agen t s in clin ical pract ice. SSEP an d MEP m on itoring, especially in p at ien t s w ith n o n eu ro-
Hypotherm ia also redu ces CMRO2 . Ext rem e hypotherm ia w ith logic deficits.31 How ever, even at low doses volat ile an esth et ic
cardiac arrest h as been u sed su ccessfu lly du ring n eon at al an d agen t s h ave som e d et rim en tal effect s on SSEPs an d MEPs. Ni-
adult cardiovascular surger y an d du ring in t racran ial gian t an eu - t rou s oxide also red u ces th e am plit u de an d in creases th e laten cy
r ysm surger y.5,23 Alth ough u se of p rofou n d hyp oth erm ia w ith of SSEPs an d MEPs.31
cardiac arrest is associated w ith sign ifican t risk, it s u se m ay be Op ioid s (fen t anyl, rem ifen t an il, su fen t an il, alfen t an il) an d
ju st ified in sp ecific cases. Several clin ical st u d ies h ave invest i- p rop ofol in fu sion s h ave m in im al effect s on SSEPs an d MEPs at
gated th e u se of m ild to m od erate hyp ot h er m ia as a n eu rop ro - t yp ical d oses. Prop ofol su p p resses MEPs an d SSEPs at h igh
tect an t in h u m an s. Use of m od erate hyp ot h er m ia h as been d oses or w h en ad m in istered as a bolu s d ose. A tot al in t rave-
sh ow n to p rovide n eu rop rotect ion in p at ien t s after card iac ar- n ou s an esth esia tech n iqu e u sing prop ofol an d op ioid in fu sion s,
rest .24 Th e IHAST st u dy, a large ran dom ized, prospect ive, m ult i- w ith or w it h ou t a sm all d ose of a volat ile an est h et ic, h as m in i-
cen ter st udy in pat ien t s u n dergoing cerebral ar ter y an eur ysm m al effect on SSEP an d MEP m on itoring, an d is th e m ost com -
su rger y, sh ow ed n o hyp oth erm ia-related ben efit s.25 On th e con - m on ly u sed an esth esia tech n iqu e du ring n eu rovascu lar su rger y
t rar y, th e st u dy foun d an in creased risk of bacterem ia in hyp o- at ou r in st it u t ion .
t h er m ic p at ien t s. More research is requ ired to d eter m in e t h e Dexm ed etom id in e is an in t raven ou s an est h et ic agen t w it h
p at ien t p op u lat ion t h at w ou ld m ost ben efit from t h erap eu t ic m in im al effect on SSEPs at low er d oses.32,33 At h igh er d oses
hypoth erm ia. d exm ed etom id in e h as d et r im en t al effect s on SSEPs. Th e effect
Alt h ough lim ited evid en ce su p p or t s t h e rou t in e u se of hy- of dexm edetom idin e on MEPs is st ill con t roversial. Use of dex-
p ot h er m ia or an est h et ic n eu rop rotect ive agen t s, st rong associ- m edetom idin e during n eurovascular surger y is part ially lim ited
at ion s h ave been d ocu m en ted bet w een hyp er t h er m ia an d p oor d u e to it s h em odyn am ic effect s (hyp oten sion , bradycard ia).
neurologic outcom e.26,27 Sim ilarly, hyperglycem ia correlates w ith Ket am in e h as m in im al effects on SSEPs an d MEPs but is often
p oor ou tcom e in acu te isch em ic st roke an d sh ou ld likely be avoided during in t racran ial surger y du e to its poten t ial to in -
avoided.28,29 Fu r th erm ore, in hyp erglycem ic p at ien t s isch em ic crease ICP. Use of n eu rom uscular blocking drugs abolish es EMGs
region s expan d com p ared w ith n orm oglycem ic pat ien ts.5 A pro- an d MEPs. Any an esth esia tech n ique can be used during EEG
spect ive, ran dom ized t rial evaluat ing w h eth er t igh t glucose con - m on itoring. Due to lim ited availabilit y of th iopen tal, h igh -dose
t rol im proved ou tcom es failed to sh ow a ben efit , bu t th e st at ist i- propofol is used to ach ieve bu rst su pp ression if required.
cal pow er of th e st u dy w as low.30 Cu rren tly, it is u n clear w h eth er In addit ion to th e an esth et ic agen ts, SSEP, MEP, EMG, an d EEG
hyp erglycem ia an d hyp er t h erm ia are m erely m arkers of p oor m on itoring is in fluen ced by oth er perioperative physiological

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10 Neuroanesthesia 145

even ts such as hypotension, hypoth erm ia, electrolytic im balances, u n d ergoin g en d ovascu lar p roced u res involvin g an t icoagu lat ion
an d ICP. Of th ese, m ain tain ing adequate cerebral perfusion pres- and contrast dye should have baseline coagulation and renal func-
su re to opt im ize (collateral) cerebral blood flow likely h as t h e t ion docu m en ted. A h em oglobin level an d blood grou p w ith an -
h igh est p oten t ial to affect ou tcom e. Neu rop hysiological m on i- t ibody screen ing sh ou ld be obt ain ed for any p rocedu re in w h ich
torin g sh ou ld be ap p lied select ively given t h e p oten t ial d isad - sign ifican t blood loss cou ld occu r. Cardiac invest igat ion s su ch as
van t ages such as addit ion al operat ing room t im e an d expen se as an elect rocardiography, ech ocardiography, or invasive test ing for
w ell as lip an d tongu e inju ries. coron ar y ar ter y disease sh ou ld be dict ated by a p at ien t’s sym p -
tom s an d fun ct ion al capacit y an d perform ed in accordan ce w ith
curren t guidelin es. For elect ive procedures, all pat ien t com or-
bidit ies, par t icularly cardiovascular disease, sh ou ld be opt im ized
before proceeding w ith th e proposed surgical procedure.
■ Preoperative Evaluation Th e anesthesiologist advises on m edicat ions th e patient should
Th e p reoperat ive assessm en t of p at ien t s for n eu rovascu lar su r- con t in u e u p to th e day of su rger y an d w h eth er any addit ion al
ger y sh ould focus on both th e in dicat ion for th e procedu re as m edicat ion s w ill be adm in istered. For exam ple, certain an t ihy-
w ell as p oten t ial coexist ing d iseases. In ad dit ion to th e u su al per ten sive m edicat ion s su ch as angioten sin -conver t ing en zym e
an esth esia h istor y an d physical exam in at ion , th e preoperat ive in h ibitors sh ou ld be w it h h eld before t h e sch edu led p roced u re
evalu at ion in cludes a carefu l assessm en t of th e p at ien t’s presen t to avoid refractor y hypoten sion un der gen eral an esth esia. An t i-
com p lain t , d iagn osis, an d cu r ren t n eu rologic st at u s. Pat ien t s ep ilept ic m edicat ion s sh ou ld be con t in u ed th rough ou t th e p eri-
sh ou ld be qu est ion ed an d exam in ed for evid en ce of in creased operat ive period to m in im ize th e risk of perioperat ive seizures.
ICP, focal n eu rologic d eficit s, an d seizu res. Pat ien t s sh ou ld be Th e n eed for prem edicat ion (before th e pat ien t en ters th e op er-
screen ed for card iovascu lar an d resp irator y com orbid it ies com - ating room ) is determ ined by patien t and surgical considerations.
m on in t h is p at ien t p op u lat ion . Many p at ien t s w it h cerebro - Many patien ts receive sm all doses of int ravenous ben zodiazepines
vascular diseases h ave a h istor y of hyper ten sion , sm oking, an d to reduce an xiet y. Sedat ive agen t s sh ould be u sed w ith caut ion
oth er vascu lar risk factors. Th ese p at ien t s m ay be at in creased in p at ien t s w ith eviden ce of in creased ICP given th e risk of n eu -
risk for cardiovascu lar com plicat ion s su ch as m yocard ial isch - rologic deteriorat ion w ith hyp oven t ilat ion .
em ia an d arrhyth m ias. Less frequ en tly, in t racran ial vascu lar le-
sion s su ch as an eu r ysm s or ar terioven ou s m alform at ion s (AVMs)
m ay be a com pon en t of a m u lt iorgan syn drom e such as collagen
vascu lar disease or h eredit ar y h em orrh agic telangiectasia. Th e ■ Anesthesia Considerations for
patien t’s baseline blood pressure an d any vasoactive m edication s Aneurysm and Arteriovenous
sh ou ld be n oted becau se th is in form at ion gu ides in t raoperat ive
h em odyn am ic m an agem en t .
Malformation Surgeries
Th e p reop erat ive assessm en t of p at ien t s u n dergoing resec- Pat ien ts w ith an u n ru pt u red an eur ysm or a rupt u red an eu r ysm
t ion or em bolizat ion of an in t racran ial vascu lar lesion su ch as an w ith or w ith out vasospasm presen t an esth esiologist s w ith dif-
an eur ysm or AVM is based on w h eth er th e lesion is ru pt ured or feren t con cern s an d ch allenges. How ever, for all pat ien ts sch ed-
in t act . In tact vascu lar lesion s m ay becom e sym ptom at ic w ith u led for in t racran ial an eu r ysm su rger y, th e an esth esia goals are
focal neurologic deficits or w ith seizures resulting from local m ass to preven t sudden in creases in blood pressure to avoid an eur ys-
effect or vascular steal. In t racran ial h em orrh age, w h eth er su b - m al rupt ure; to facilitate surgical exposure by reducing ICP; an d
arach n oid or in t racerebral, can cau se m ult iple n eurologic com - to m aintain adequate cerebral perfusion pressure to prevent tem -
plications including increased ICP, vasospasm , hydrocephalus, and p orar y clip , vasosp asm , or ret ractor p ressu re-in d u ced cerebral
seizu res. Pat ien ts m u st be screen ed for n on n eu rologic com plica- isch em ia.
t ion s in clu ding cardiac arrhyth m ias, cardiac failu re, n eu rogen ic Pat ien t s w ith u n ru pt u red an eu r ysm s are often n eurologically
pu lm on ar y edem a, elect rolyt ic abn orm alit ies, an d dissem in ated in t act w ith n orm al ICP an d m ay seek elect ive su rgical t reat m en t .
in t ravascu lar coagu lat ion . Th ese com p licat ion s m ay h ave im - In ad d it ion to avoid ing hyp er ten sive ep isod es, t h e an est h esia
p licat ion s for bot h t h e t im in g of su rger y an d an est h esia m an - focu s is on red u cing in t racran ial blood volu m e an d brain w ater
agem en t , in clu d in g t h e n eed for ad d it ion al invasive m on itor ing con ten t to en able good su rgical exp osu re w it h m in im al brain
an d p ostoperat ive ven t ilat ion . Excessive hyp er ten sion sh ou ld be ret ract ion . Pat ien t s w ith ru pt ured an eur ysm s h ave a h igh risk of
avoided in pat ien t s at risk for rebleeding, w h ereas perm issive rebleeding, an d blood pressure is m ain t ain ed at or sligh t ly below
hyper ten sion m ay be used in pat ien t s w ith vasospasm an d a se- baselin e values. Becau se th ese pat ien t s also m ay h ave in creased
cu red an eur ysm . ICP, hypoten sion is avoided to m ain tain adequate cerebral perfu -
Th e an esthesiologist should assess any available diagnostic im - sion p ressu re. Pat ien t s w ith both r u pt u red an eu r ysm s an d cere-
aging st udies for evidence of in creased ICP an d significan t brain bral vasospasm are the m ost challenging for the anesthesiologists.
edem a. Even asym ptom at ic pat ien ts w ith large space-occu pying In creases in blood pressure m ay result in a rebleed, an d even a
lesion s are at risk of p eriop erat ive decom p en sat ion du e to lim - tem porar y reduct ion of blood pressure m ay resu lt in in adequ ate
ited reser ve in in t racran ial com plian ce. Th e locat ion an d size of cerebral blood flow. Because an eur ysm surger y involves a w ide
th e vascu lar lesion sh ou ld be n oted to evalu ate th e p oten t ial for range of st im u li, blood p ressu re con t rol n eeds con t in uou s close
in t raoperat ive bleeding. If available, th e paten cy of collateral cir- at ten t ion .
culat ion sh ould be assessed if tem porar y region al isch em ia is to Neurologically intact patients m ay receive prem edication (1–2
be em ployed because the anesthesiologist can augm ent system ic m g in t raven ou s m idazolam ). In du ct ion of an esth esia, in t u bat ion ,
blood p ressu re du ring p eriods of p oten t ial isch em ia. All pat ien ts ap plicat ion of Mayfield pin s an d skin in cision are kn ow n st im uli

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146 II Evaluation and Treatment Considerations for Neurovascular Disease

th at m ay in du ce hyp er ten sion . Hyper ten sive ep isod es are u su - to relatively low cerebral perfusion pressure m ay be unable to ac-
ally at tenuated w ith use of large loading doses of n arcot ics (fen - com m odate h igh er cerebral p erfu sion pressu re after th e AVM is
tanyl, rem ifen tan il), propofol boluses, an d/or labet alol. Narcot ic elim in ated . Hyp er ten sion m ay resu lt in brain sw elling, a cat a-
(fen t anyl 2 µg/kg/h r) an d p rop ofol (100 µg/kg/m in ) in fu sion - st roph ic ru pt ure of poten t ial residu al AVM t issu e, or both .
based anesth esia, w ith or w ith out a sm all am ou n t (< 0.5 MAC) of
a volat ile an esth et ic, is used to m ain t ain an esth esia. Th is an es-
t h esia tech n iqu e is also con sisten t w it h n eu rop hysiological
m on itoring. In t raar terial blood p ressu re m on itoring is h elp fu l in ■ Anesthesia for Interventional
rap id d etect ion of blood p ressu re ch an ges an d is frequ en t ly in i-
t iated before en d ot rach eal in t u bat ion . Eu volem ia an d m ild in -
Neuroradiology Procedures
t raop erat ive hyp er ven t ilat ion (p CO2 30–35 m m Hg) are p ar t of In t racran ial en d ovascu lar p roced u res are t h e fastest grow in g
m odern neuroanesthesia. Most patients receive intravenous m an - n eu rosu rgical p roced u re.35 Com m on ly p er for m ed p roced u res
n itol (0.5–1 g/kg), dexam eth ason e (10 m g), an d an an t ibiot ic at in clu de th e en dovascu lar t reat m en t of an eu r ysm s, AVMs, an d
th e begin n ing of th e op erat ion . du ral fist u las an d p reoperat ive em bolizat ion of t u m ors.36 Pa-
An esth esia m ain ten an ce w ith a propofol in fusion is frequen tly tients presenting to the neurointer ventional radiology suite range
associated w ith in t raoperat ive hypoten sion . To m ain tain h em o- from h ealt hy elect ive ou t p at ien t s to cr it ically ill p at ien t s from
dyn am ic st abilit y an d adequ ate cerebral perfusion pressure, a t h e in ten sive care u n it (ICU). Provid in g an est h esia for n eu ro -
vasopressor in fusion m ay be u sed. In addit ion to in t raoperat ive in ter ven t ion al procedures is gu ided by several gen eral con sider-
drain age of cerebrosp in al flu id, several tech n iqu es are u sed to at ion s as w ell as th ose sp ecific to th e pat ien t an d procedure.
redu ce brain volu m e (see above). Most p at ien ts are ext ubated in Most in ter ven t ion al su ites are rem ote from th e m ain op erat-
th e operat ing room at th e en d of su rger y. Em ergen ce hyper ten - ing room s. A poten t ial delay in accessing addit ion al em ergen cy
sion is at ten uated by p rophylact ic u se of labetalol. equ ip m en t or person n el th erefore m u st be factored in to th e an -
Th e m ost frequ en t com p licat ion is in t raoperat ive ru pt u re of esth esiologist’s plan . Access to th e pat ien t du ring th e procedu re
an an eur ysm . Most in t raoperat ive an eur ysm r upt ures occur dur- is lim ited . Tran sferring th e pat ien t to t h e post an esth esia recov-
ing su rgical m an ip u lat ion of th e an eur ysm . Pat ien ts sh ould h ave er y u n it or ICU m ay be p rolonged an d sh ou ld on ly be u n der t aken
at least t w o large-bore in t raven ou s lin es an d an in t raar terial on ce por t able m on itors an d em ergen cy air w ay equipm en t are
catheter to aid and guide int ravascular volum e resuscitation . Dur- available. Th e an est h esia goals for all n eu roin ter ven t ion al p ro-
ing th e ap plicat ion of tem porar y clips, cerebral perfusion p res- cedures in clude facilitat ing postoperat ive n eurologic assessm en t
su re is m ain tain ed at or above baselin e blood pressu re valu es to w it h t h e u se of m in im al lon g-act ing an est h et ic agen t s. Neu ro-
in crease collateral p er fu sion to isch em ic areas. How ever, if th e in ter ven t ion al p roced u res are associated w it h m in im al in t ra-
h em orrh age is severe en ough th at the su rgeon is un able to see an d postoperat ive discom for t; th erefore, long-act ing opioids are
th e n eu rovascu lar an atom y, blood p ressu re m ay be tem porarily avoid ed .
low ered to redu ce th e rate of h em orrh age. Recen t rep or ts sug- An esth esia for n euroin ter ven t ion al procedures are t ypically
gest u se of aden osin e for blood pressure con t rol an d tem porar y accom plish ed w ith local an esth esia an d sedat ion or gen eral an -
in du ct ion of bradycardia or asystole.34 esth esia. Th e ch oice of an esth et ic is based on a decision bet w een
Preparat ion an d an esth esia m an agem en t of p at ien t s for AVM th e in ter ven t ion alist an d an est h esiologist an d varies dep en ding
su rger y are sim ilar to th ose of an eu r ysm su rger y w ith a few ex- on th e an t icipated pat ien t cooperat ion , com plexit y an d durat ion
cept ion s. Because m any pat ien t s h ave h ad a diagn ost ic or th era- of t h e p roced u re, an d in st it u t ion al p referen ce. Neu roin ter ven -
peutic (em bolization) neurointerventional procedure before AVM t ion al p roced u res often requ ire br ief p er iod s of ap n ea for opt i-
su rger y, th e surgeon an d an esth esiologist h ave a good u n der- m al im agin g. Ap n ea is accom p lish ed eit h er w ith an aw ake co -
st an ding of t h e an atom y of th e AVM, in clu ding th e risk of m ajor op erat ive pat ien t or w ith gen eral en dot rach eal an esth esia w ith
in t raop erat ive h em orrh age. Alth ough AVMs are frequ en tly asso- m uscle relaxat ion . If gen eral an esth esia is required, th e air w ay is
ciated w it h an eu r ysm s, in t raop erat ive h em orrh age is seldom t ypically secured w ith en dot rach eal in t u bat ion (versus supra-
associated w ith hyper ten sive episodes. Th us, in t raar terial cath - glot t ic air w ay d evices, e.g., lar yngeal m ask air w ay) becau se t h e
eters are often inserted after anesth esia is induced. Central venous an est h esiologist h as lim ited access to th e p at ien t d u r ing t h e
cath eters are seldom u sed—on ly if a m assive blood loss is ex- p rocedure. Neuroin ter ven t ion al procedu res require a m ot ionless
pected or du e to oth er pat ien t com orbidit ies. pat ien t becau se m ovem en t at crit ical ju n ct u res can p recipitate
An esth esia m ain ten an ce is t ypically ach ieved w ith propofol m icrocath eter-in duced vessel perforat ion or spasm . Local an es-
an d n arcot ic in fu sion s w ith or w ith out a sm all am oun t of volat ile th esia is associated w ith less hypoten sion an d facilit ates n euro-
an esth et ic allow ing n eu rophysiological m on itoring. Blood pres- logic test ing, alth ough it risks respirator y dep ression , aspiration ,
su re m ay be su p p or ted u sing a p h enylep h rin e in fu sion . Neu ro- an d p at ien t m ovem en t .36 Typ ically, sm all in ter m it ten t in t rave-
m uscu lar relaxat ion is used to facilitate en dot rach eal in t ubat ion n ous boluses of m idalozam (1–2 m g) an d fen tanyl (25–50 µg) are
an d m ay be used during AVM resect ion as long as it is does n ot sufficien t for an esth esia.
con flict w ith n europ hysiological m on itoring. Alth ough invasive m onitoring is less frequen tly used in th e
Euvolem ia sh ou ld be m ain t ain ed in an t icip at ion of a p oten t ial n eu roin ter ven t ion al suite th an in th e operat ing room ,37 it is
intraoperative hem orrhage. Cerebral perfusion pressure should be often required for careful perioperat ive h em odyn am ic m anage-
kept h igh en ough to m in im ize ret ractor-in duced isch em ia. Post- m en t of pat ien ts w ith in t racran ial vascular lesion s, h em orrh age,
op erat ive blood p ressu re con t rol is cr it ical. Au toregu lat ion of or st roke because sign ifican t h em odyn am ic ch anges can be seen
“n orm al” vascular beds n ear th e AVM th at h ave been accustom ed d u r ing in d u ct ion an d em ergen ce from an est h esia. Treat m en t

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10 Neuroanesthesia 147

of cerebral vasospasm after subarach n oid h em orrh age m ay also


cau se h em odyn am ic ch anges; balloon angiop last y often cau ses ■ Anesthesia Considerations for
hyper ten sion , w h ereas in t raar terial inject ion of vasodilators in to Operations in the Posterior Fossa
th e cerebral vessels is associated w ith redu ct ion s in blood pres-
su re.38,39 Fin ally, invasive m on itoring is u sefu l in th e even t of Th e n eu roan esth esia p rin ciples an d tech n iqu es for p osterior
com p licat ion s such as ar terial dissect ion or ru pt u re. fossa surger y are sim ilar to th ose for su praten torial su rger y, w ith
En dovascu lar n eu roin ter ven t ion al procedu res often requ ire several specific considerations. Man ipulation of th e cran ial n er ves
an t icoagulat ion . Th e an esth esiologist an d in ter ven t ion alist m ust an d brain stem can be associated w ith sign ifican t in t ra- an d post-
clearly com m u n icate abou t th e t im ing an d dose of h ep arin re- operat ive h em odyn am ic ch anges, in cluding asystole. For som e
qu ired for th e p rocedu re. Th e ad m in ist rat ion of an t icoagu lat ion procedu res on th e posterior fossa, placing th e pat ien t in th e sit-
sh ou ld be con firm ed verbally by th e an esth esiologist an d is often t ing p osit ion p rovid es good su rgical exposu re bu t is associated
m onitored w ith point-of-care testing (e.g., activated clot ting tim e) w ith m any com plicat ion s. Th e sit t ing posit ion is associated w ith
becau se in t racerebral em boli can h ave disast rous con sequ en ces. n er ve inju ries, in creased h em odyn am ic labilit y, air w ay injuries,
In th e even t of an in t racran ial bleed, th e an esth esiologist w ill ad- an d, m ost im p or tan tly, ven ou s air em bolism . Ven ous air em bo-
m in ister protam in e to reverse th e effects of th e h eparin . lism can occu r any t im e during surger y, from skin in cision to clo-
During en dovascu lar coiling of an in t racran ial an eur ysm , th e su re, w h en th e vein s in th e op erat ive site h ave n egat ive p ressu re.
an esth esiologist sh ould pay con t in uous at ten t ion to blood pres- Sp ecific m on itoring is u sed to detect in t raop erat ive ven ou s air
su re an d h ear t rate. Su dden in creases in blood p ressu re or su d- em bolism (en d t id al CO2 , p record ial Dop p ler u lt rason ograp hy,
den decreases in h ear t rate can reflect in t racran ial h em orrh age an d a m ult i-orifice cen t ral ven ous cath eter). Paradoxical ven ous
an d sh ould im m ediately be com m un icated to th e rest of th e team . air em bolism (t h rough a r igh t -to-left sh u n t ) can cau se st roke
Em bolizat ion of large AVMs m ay be associated w ith p u lm on ar y or m yocard ial in farct ion . Pat ien t s sh ou ld u n d ergo a p reop era-
com p licat ion s. Em bolizat ion m ater ial m ay p ass t h rough large t ive ech ocardiogram to determ in e if th ey h ave a p aten t foram en
sh u n t s in t h e AVM an d en d u p in p u lm on ar y vascu lat u re. Th e ovale. If so, th e sit t ing posit ion sh ou ld be avoided. Placing an
resu lt ing in crease in pu lm on ar y dead sp ace m ay h ave det rim en - an esth et ized pat ien t in the sit t ing posit ion w ill cause blood to
tal effects on oxygen at ion an d ven t ilat ion . pool in th e legs an d th u s relat ive hyp ovolem ia (low cardiac pre-
load). Liberal in t raven ou s flu ids, leg com p ression d evices, an d
vasopressors are u sed to m ain tain adequ ate cerebral perfu sion
pressure. For t u n ately, th e use of th e sit t ing posit ion for posterior
■ Anesthesia for Pediatric fossa surger y h as dim in ished, alth ough so h as th e experien ce of
an esth esiologists in m an aging th e risks associated w ith th e sit-
Neurovascular Procedures t ing posit ion w h en it is u sed.
Many of th e p r in cip les t h at gu id e p rovision of an est h esia for Alth ough t ran sesoph ageal ech ocardiography is th e m ost sen -
ad u lt n eu rosu rger y ap p ly to ch ild ren , w it h several ad d it ion al sit ive m on itor for ven ou s air em bolism , it requ ires addit ion al
con siderat ion s. Neon ates, in fan t s, an d ch ildren h ave sign ifican t specialized exper t ise an d m ay be im pract ical. Precordial Doppler
an atom ic an d physiological differen ces com pared w ith adults u lt rason ography is sen sit ive for detect ing in t racardiac air bub -
an d ideally sh ould be m an aged by specialist pediat ric an esth esia bles, but few an esth esiologists h ave sign ifican t experien ce w ith
providers. An atom y an d p hysiology ch ange sign ifican tly du ring th is device. A su dden fall in en d-t idal CO2 also suggest s a ven ou s
early ch ildh ood. An in fan t’s h ead is large in propor t ion to th e rest air em bolism but is n ot as specific as th e Doppler fin dings. In th e
of th e body. Fur th erm ore, an in fan t’s h ead receives a h igh er per- even t of a ven ous air em bolism , a fall in en d-t idal CO2 is often
cen t age of card iac ou t p u t com p ared w it h ad u lt s. Th is feat u re, associated w ith a con com itan t in crease in ar terial CO2 du e to in -
in addit ion to a sm aller absolute blood volum e, can often resu lt creased pulm on ar y dead space caused by obst r uct ion of pulm o-
in significant intraoperative blood loss. Cerebral autoregulation in n ar y blood vessels by air bubbles. Hem odyn am ic ch anges are a
ch ildren exist s over a n arrow er an d low er range t h an in adu lt s late sign of ven ous air em bolism .
an d requires t igh t h em odyn am ic con t rol. Neurosurgical proce- On ce a ven ous air em bolism is recogn ized, th e m ost im por-
du res in th is pop u lat ion t yp ically requ ire invasive m on itoring t an t p ar t of m an agem en t is to p reven t fu r t h er en t rain m en t of
an d good in t raven ous access to facilitate volum e resu scitat ion . air at th e surgical site. Good com m un icat ion an d an experien ced
Prem edicat ion w ith oral m idazolam an d in h alat ion al in d u ct ion team are n ecessar y to m in im ize risks du ring th ese procedures.
w ith sevoflu ran e are often used . Un like adu lts, ven ous an d ar te- Th e conven t ion al steps of “flooding th e field” an d low ering th e
rial can n u lat ion is often don e after in du ct ion of an esth esia an d pat ien t’s h ead m ay be n ecessar y, bu t th ese m an euvers are n ot
m ay be tech n ically ch allenging in sm all p at ien t s. alw ays pract ical. Gen tle pressu re on th e jugular vein s in creases
Many of th e n eu rovascu lar su rger y procedu res in pediat ric ven ou s pressure in th e h ead an d n eck an d m ay h elp the su rgeon
pat ien ts involve ar terioven ou s sh u n ts. A h igh p rop or t ion of th e to locate th e source of ven ous air em bolism . An esth esia m an age-
ch ild’s cardiac ou t p u t m ay go th rough th ese sh u n ts an d result in m en t of an in t raoperat ive ven ous air em bolism in clu des apply-
h igh -out put cardiac failure at th e t im e of th e procedure. Closing ing 100%oxygen . If in use, n it rou s oxide sh ou ld be discon t in u ed.
th e sh u n t m ay resu lt in sign ifican t in t raoperat ive h em odyn am ic Su pp or t ive m an agem en t for cardiovascu lar collap se an d severe
in st abilit y. Th e p resen ce of path ological sh un ts an d p ersisten t hypoxem ia is th e m ain stay of th erapy.
fet al sh u n t s in crease t h e r isk of p aradoxical ven ou s air em boli A plan for em ergen ce from an esth esia an d ext ubat ion sh ould
in p ediat ric pat ien ts. Con sequ en tly, all in t raven ous lin es sh ou ld be d iscu ssed w it h t h e su rgeon at t h e con clu sion of p osterior
be de-aired carefu lly. fossa su rger y. Brain stem com p ression , ed em a, cran ial n er ve

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148 II Evaluation and Treatment Considerations for Neurovascular Disease

dysfunction, and possible hem orrhage into the posterior fossa m ay su re. To defin e baselin e blood p ressu re valu es, w e p lace an in t ra-
resu lt in an in abilit y to p rotect th e air w ay an d life-th reaten ing ar ter ial can n u la before in d u ct ion of an est h esia. Ph enylep h r in e
respirator y depression . is u sed d u r ing an d after in d u ct ion of an est h esia to p reven t even
t ran sien t hyp oten sion , an d hyp er ven t ilat ion an d hyp ot h er m ia
are avoided. Cen t ral ven ous cath eters provide som e guidan ce in
m ain tain ing euvolem ia or sligh t hyper volem ia.
■ Anesthesia Considerations for
Moyamoya and Extracranial-to -
Intracranial Bypass Surgeries ■ Conclusion
Pat ien t s w ith m oyam oya disease an d pat ien ts sch eduled for an An esth esia for n eurovascular su rger y involves com plex pat ien ts
ext racran ial-to-in t racran ial byp ass are som e of th e m ost com - and procedures and requires an ongoing dialogue bet w een exper-
plex cases for anesth esiologists to m anage. Most of these patients ienced surger y and an esthesia team s. The anesthesiologist’s goals
h ave in adequate cerebral blood flow an d preexist ing isch em ic are to m ain t ain adequate cerebral perfu sion th at is m atch ed to
cerebral in farct s. Th ere are n o m on itors to detect in adequate re- t h e p at ien t ’s CMRO2 an d to m in im ize in creases in ICP. Alt h ough
gion al cerebral perfusion in th e areas at risk during tem porar y clin ical evid en ce of it s efficacy is lackin g, t h e role of an est h esia
occlusion . To m in im ize t im es of in adequate flow, th e an esth esia n eu rop rotect ion , p ar t icu larly d u r in g t im es of tem p orar y isch -
goals are to m aintain baseline cerebral blood flow and to increase em ia, sh ou ld be con sidered. Fin ally, specific procedures an d th e
it du ring tem porar y cerebral blood vessel occlu sion . Ou r pract ice u se of n eu rophysiological m on itoring h ave im por t an t im plica-
is to m aintain blood pressure at or 10%above baseline blood pres- t ion s for th e m an agem en t of an esth esia.

References
1. Dagal A, Lam AM. Cerebral autoregu lat ion an d an esth esia. Curr Opin An - 16. Naidech AM, Jovan ovic B, War ten berg KE, et al. High er h em oglobin is as-
aesth esiol 2009;22:547–552 sociated w ith im proved outcom e after subarach n oid h em orrh age. Crit
2. An drew s RJ, Bringas JR, Alon zo G. Cerebrospin al fluid pH an d PCO2 rap - Care Med 2007;35:2383–2389
idly follow arterial blood pH and PCO2 w ith ch anges in ven t ilat ion . Neu- 17. Sm ith MJ, Le Rou x PD, Elliot t JP, Win n HR. Blood t ran sfusion an d in creased
rosurger y 1994;34:466–470, discussion 470 r isk for vasosp asm an d p oor ou tcom e after su barach n oid h em or rh age.
3. Din sm ore J. An aesth esia for elect ive n eurosurger y. Br J Anaesth 2007; J Neu rosurg 2004;101:1–7
99:68–74 18. McEw en J, Hut t un en KH. Tran sfu sion pract ice in n euroan esth esia. Curr
4. Sch ifillit i D, Grasso G, Con t i A, Fodale V. An aesth et ic-related n europrotec- Op in An aesth esiol 2009;22:566–571
t ion : in t raven ous or in h alat ion al agen t s? CNS Drugs 2010;24:893–907 19. Oddo M, Milby A, Ch en I, et al. Hem oglobin con cen t rat ion an d cerebral
5. Fukuda S, Warn er DS. Cerebral protect ion . Br J An aesth 2007;99:10–17 m etabolism in patients w ith an eur ysm al subarach noid hem orrhage. Stroke
6. Drum m on d JC, McKay LD, Cole DJ, Patel PM. Th e role of n it ric oxide syn - 2009;40:1275–1281
th ase in h ibit ion in th e adverse effect s of etom idate in th e set t ing of focal 20. Baugh m an VL. Brain p rotect ion d u r ing n eu rosu rger y. An est h esiol Clin
cerebral isch em ia in rat s. An esth Analg 2005;100:841–846 Nor th Am erica 2002;20:315–327, vi vi
7. Rasm u ssen M, Bu n dgaard H, Cold GE. Cran iotom y for su p raten tor ial 21. Head BP, Patel P. Anesthetics and brain protection. Curr Opin Anaesthesiol
brain t u m ors: risk factors for brain sw elling after op en ing th e du ra m ater. 2007;20:395–399
J Neu rosu rg 2004;101:621–626 22. Hin d m an BJ, Baym an EO, Pfisterer W K, Torn er JC, Tod d MM; IHAST Inves-
8. Gelb AW, Craen RA, Rao GS, et al. Does hyper ven t ilat ion im prove operat- t igators. No associat ion bet w een in t raoperat ive hypoth erm ia or supple-
ing con dit ion during supraten torial cran iotom y? A m u lt icen ter ran dom - m en t al protect ive dr ug an d n eurologic outcom es in pat ien t s un dergoing
ized crossover t rial. An esth An alg 2008;106:585–594 tem porar y clipping during cerebral aneu r ysm surger y: fin dings from th e
9. Low e GJ, Ferguson ND. Lung-protect ive ven t ilat ion in n eu rosurgical pa- In t raoperat ive Hypoth erm ia for An eur ysm Surger y Trial. An esth esiology
t ien t s. Cu rr Opin Crit Care 2006;12:3–7 2010;112:86–101
10. Rozet I, Ton t isirin N, Muangm an S, et al. Effect of equiosm olar solut ion s of 23. Grigore AM, Mu r ray CF, Ram akr ish n a H, Djaian i G. A core review of tem -
m an n itol versus hyper ton ic saline on in t raoperat ive brain relaxat ion an d p erat u re regim en s an d n eu rop rotect ion d u r ing card iop u lm on ar y by-
elect rolyte balan ce. An esth esiology 2007;107:697–704 p ass: d oes rew ar m ing rate m at ter? An est h An alg 2009;109:1741–1751
11. Wu CT, Ch en LC, Kuo CP, et al. A com parison of 3% hyper tonic salin e an d 24. Bern ard SA, Gray TW, Buist MD, et al. Treat m ent of com atose sur vivors of
m an n itol for brain relaxat ion during elect ive supraten torial brain t um or out-of-h ospit al cardiac arrest w ith in duced hypoth erm ia. N Engl J Med
su rger y. An esth An alg 2010;110:903–907 2002;346:557–563
12. Tom m asin o C. Flu id s an d t h e n eu rosu rgical p at ien t . An est h esiol Clin 25. Todd MM, Hin dm an BJ, Clarke W R, Torn er JC; In t raoperat ive Hypoth erm ia
North Am erica 2002;20:329–346, vi for An eu r ysm Su rger y Trial (IHAST) Invest igators. Mild in t raop erat ive hy-
13. Priebe HJ. An eur ysm al subarach n oid h aem orrh age an d th e an aesth et ist . poth erm ia during surger y for in t racran ial an eur ysm . N Engl J Med 2005;
Br J An aesth 2007;99:102–118 352:135–145
14. Mybu rgh J, Cooper DJ, Fin fer S, et al; SAFE St udy Invest igators; Au st ralian 26. Azzim on di G, Bassein L, Nonin o F, et al. Fever in acu te st roke w orsen s
an d New Zealan d In ten sive Care Societ y Clin ical Trials Group; Aust ralian progn osis. A prospect ive st udy. St roke 1995;26:2040–2043
Red Cross Blood Ser vice; George In st it ute for In tern at ion al Health . Salin e 27. Hajat C, Hajat S, Sharm a P. Effects of poststroke pyrexia on stroke outcom e:
or album in for flu id resuscit at ion in pat ien t s w ith t raum at ic brain inju r y. a m eta-an alysis of studies in patien ts. Stroke 2000;31:410–414
N Engl J Med 2007;357:874–884 28. Adam s HP Jr, del Zoppo G, Alber t s MJ, et al; Am erican Hear t Associat ion /
15. Hartog CS, Bauer M, Rein h art K. Th e efficacy an d safet y of colloid resu sci- Am erican St roke Associat ion St roke Cou n cil; Am erican Heart Associat ion /
t at ion in th e crit ically ill. An esth An alg 2011;112:156–164 Am erican St roke Associat ion Clin ical Cardiology Coun cil; Am erican Heart

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Associat ion /Am erican St roke Associat ion Cardiovascu lar Radiology an d 33. Tobias JD, Goble TJ, Bates G, An derson JT, Hoern sch em eyer DG. Effect s of
In ter ven t ion Coun cil; Ath erosclerot ic Periph eral Vascular Disease Work- dexm edetom idine on in t raoperat ive m otor an d som atosen sor y evoked
ing Group; Qualit y of Care Outcom es in Research In terdisciplin ar y Work- poten t ial m on itoring during spin al surger y in adolescen t s. Paediat r An -
ing Group. Guidelin es for th e early m an agem ent of adult s w ith isch em ic aesth 2008;18:1082–1088
st roke: a gu id elin e from th e Am erican Hear t Associat ion /Am erican St roke 34. Luost arinen T, Takala RS, Niem i TT, et al. Aden osin e-in duced cardiac ar-
Associat ion St roke Cou n cil, Clin ical Cardiology Cou n cil, Cardiovascu lar rest during in t raoperat ive cerebral an eur ysm rupt ure. World Neurosu rg
Radiology an d In ter ven t ion Coun cil, an d th e Atherosclerot ic Periph eral 2010;73:79–83, discussion e9
Vascular Disease an d Qualit y of Care Outcom es in Research In terdisciplin - 35. Hughey AB, Lesn iak MS, An sari SA, Roth S. W h at w ill an esth esiologist s be
ar y Working Grou p s: Th e Am erican Academ y of Neu rology affirm s th e an esth et izing? Tren ds in n eurosurgical procedure usage. Anesth Analg
valu e of th is gu idelin e as an ed u cat ion al tool for n eu rologist s. Circu lat ion 2010;110:1686–1697
2007;115:e478–e534 36. Varm a MK, Price K, Jayakrish nan V, Man ickam B, Kessell G. An aesth et ic
29. Baird TA, Parson s MW, Ph an T, et al. Persisten t post st roke hyperglycem ia con siderat ion s for in ter ven t ion al n euroradiology. Br J An aesth 2007;99:
is in depen den tly associated w ith in farct expan sion an d w orse clin ical 75–85
outcom e. St roke 2003;34:2208–2214 37. Lai YC, Man n in en PH. An esthesia for cerebral an eur ysm s: a com parison
30. Gray CS, Hildreth AJ, Sandercock PA, et al; GIST Trialist s Collaborat ion . bet w een in ter ven t ion al neu roradiology an d surger y. Can J An aesth 2001;
Glucose-pot assium -in sulin in fu sions in th e m an agem en t of post-st roke 48:391–395
hyperglycaem ia: th e UK Glucose In su lin in St roke Trial (GIST-UK). Lan cet 38. Sch m idt U, Bit t n er E, Pivi S, Marot a JJ. Hem odyn am ic m an agem en t an d
Neurol 2007;6:397–406 outcom e of pat ien t s t reated for cerebral vasospasm w ith in t raar terial n i-
31. Ban ou b M, Tet zlaff JE, Sch uber t A. Ph arm acologic and physiologic in flu - cardipin e an d/or m ilrin on e. An esth Analg 2010;110:895–902
en ces affect ing sen sor y evoked poten t ials: im plicat ion s for perioperat ive 39. Flexm an AM, Ryerson CJ, Talke PO. Hem odyn am ic st abilit y after in t ra-
m on itoring. An esth esiology 2003;99:716–737 arterial inject ion of verapam il for cerebral vasospasm . An esth An alg 2012;
32. Th ornton C, Lucas MA, New ton DE, Doré CJ, Jon es RM. Effect s of dex- 114:1292–1296
m edetom idin e on isofluran e requirem en t s in h ealthy volun teers. 2: Audi-
tor y and som atosensor y evoked responses. Br J Anaesth 1999;83:381–386

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11 Neuromonitoring
Christ ian Musahl, Claudia W eissbach, and Nikolai J. Hopf

can alter surgical st rategy. Th e tech n iques of th is categor y are


■ Indications elect roen cep h alograp hy (EEG), evoked p oten t ials (som atosen -
In t raop erat ive n eu rop hysiological m on itor ing (IONM) h as be- sor y evoked poten t ials [SSEPs), m otor evoked p oten t ials [MEPs],
com e an invalu able addit ion to n eu rosu rgical p rocedu res. Neu - auditor y evoked poten t ials [AEPs], an d visu al evoked poten t ials
rovascular su rgeon s rely h eavily on th e con t in u ous feedback [VEPs]), elect rom yography (EMG), D-w ave, t h e bu lbospongiosu s
provided by IONM. Resect ion of a cavern ou s m alform at ion of th e reflex, an d m on itoring of sp eech fu n ct ion during aw ake cran iot-
brain stem , tem porar y clipping of a paren t vessel during an eu - om ies. Tech n iques for localizing brain eloquen ce in clude in t ra-
r ysm su rger y, d ifferen t iat ion bet w een an ar terioven ou s m al- operat ive m apping, w h ich in clu des direct cor t ical st im ulat ion
for m at ion (AVM)-feed ing vessel an d a m otor cor tex su p p lying (DCS), ph ase reversal, an d n avigated t ran scran ial m agn et ic st im -
ar ter y, as w ell as su t u ring an an astom osis du ring ext racran ial- u lat ion (nTMS).
to-in t racran ial bypass surger y are all procedu res th at carr y th e Intraoperative neurophysiological m onitoring is used for prac-
risk of p erm an en t n eu rologic deficit for th e pat ien t .1 Th e m on i- tically all cerebral an d sp in al vascu lar p rocedu res in ou r n eu ro-
toring of sen sor y an d m otor fun ct ion , speech an d m em or y fun c- su rgical d ep ar t m en t . Dep en d ing on t h e locat ion an d n at u re of
t ion , as w ell as th e locat ing an d m on itoring of cran ial n er ves t h e lesion , m on itor in g w ill be m ore or less exten sive. Becau se
(CNs) h as becom e possible th rough applying th e respect ive tech - pat ien ts w ith vascu lar lesion s ten d to h ave m ore th an on e vascu -
n iqu es, th us im proving pat ien t outcom e.2–4 Th e prim ar y goal of lar problem (e.g., ad dit ion al sten osis, hyp er ten sion , angiop athy
IONM is to preven t st ru ct ural dam age to the brain an d provide etc.), th e ver y m in im um of IONM w ill be th e con t in u ous m on i-
fun ct ion al gu idan ce to th e su rgeon . toring of evoked som atosen sor y an d m otor poten t ials.
In t raoperat ive n europhysiological m on itoring m akes it pos-
sible to iden t ify th e in d ivid u al p at tern s of n eu ral fu n ct ion , th u s
facilitat ing iden t ificat ion of eloquen t areas in pat ien t s. For ex-
am ple, cran ial n er ve m otor n uclei or th eir fiber t racts can be lo- ■ Methods
cated at th e floor of t h e fou r th ven t ricle or w ith in th eir cou rse
th rough th e sku ll base an d arou n d vascu lar lesion s. Mon itoring
Anesthetic Considerations
of sen sor y, m otor, an d CN path w ays can preven t com plicat ion s In t raop erat ive n eu rop hysiological m on itor ing is h igh ly d ep en -
su ch as th e im p airm en t or loss of n eu ral fu n ct ion . Neu rologic d en t on an est h esia, an d it s opt im al u se d ep en d s on th e avail-
deficit s can be redu ced if th e evoked p oten t ials m irror th e cu r- abilit y of an exp er ien ced n eu roan est h esiologist . A su fficien t
ren t st ate of surger y (t im e equivalen ce), m ean ing th at ch anges in an algesic sedat ion w it h p recise con t rollabilit y com bin ed w it h a
n eu rom on itoring m u st correlate w ith surgical steps. Th e ch ange m argin al bu t predictable effect on n eu ron al act ivit y sh ould be
in poten t ials m u st be reversible if it s cau se can be elim in ated. u sed. Sh ort-act ing m uscle rela xan t s su ch as pan curon ium sh ould
Th is tech n ical accu racy h as on ly been m ade possible by th e ad- be u sed ; h ow ever, t h ey n eed n o lon ger be effect ive as soon as
vent of m odern com puter technology. Since then, procedures that t h e crit ical steps of th e su rger y are perform ed. Muscle relaxan ts
require an averaging of (evoked poten t ial) dat a an d a com parison sh ou ld be avoid ed in cases w h ere MEP or EMG are m on itored .
w ith a baselin e st udy h ave becom e possible. Today’s m on itoring Because in h alat ion al an esth et ics lead to a redu ct ion of am pli-
m ach in es are abou t five t im es faster th an th eir predecessors an d t u des an d a delay of laten cy in SSEP m on itoring, as w ell as a sig-
are capable of recording 16 differen t sign als at th e sam e t im e. n ifican t elevat ion of th e m otor th resh old above an in h alat ion
Th is m akes p ossible th e m on itoring of com plex procedures su ch con cen t rat ion of 0.5 of m in im u m alveolar con cen t rat ion (MAC),
as brain stem m on itoring. tot al in t raven ous an esth esia sh ou ld be applied. Opioids h ave a
Intraoperative neurophysiological m onitoring includes a large m in im al effect on MEPs but can result in am plit ude reduct ion if
variet y of m on itoring m eth ods an d th eir u se is path ology depen - given as a bolus. Ben zodiazepin es an d barbit u rates result in sup -
den t .5,6 Th ese in clu de tech n iqu es th at obt ain con t in uous in for- pression of MEPs.
m at ion about th e fun ct ion an d in tegrit y of certain brain region s Th erefore, th e ideal an esth et ic com bin at ion is th e com bin a-
or fiber tracts, and techniques for m apping for localizing eloquent t ion of p rop ofol an d an op ioid th at sh ou ld n ot be adm in istered as
areas of th e brain . Th e first group provides th e surgeon w ith con - a bolus. In h alat ion an esth et ics sh ou ld be avoided if possible, or
t in u ou s in t raoperat ive in form at ion abou t th e m on itored brain u sed at a MAC < 0.5.
fu n ct ion s, an d can be im m ed iately com pared to th e in it ial valu es Th e d ept h of an est h esia m ay be m on itored by bisp ect ral
at th e start of surger y. Th is provides real-t im e in form at ion th at in d ex (BIS) m on itor ing, a n on invasive, con t in u ou s m easu re-

150

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11 Neuromonitoring 151

m en t of t h e effect of an esth et ics on brain fu n ct ion . It h as been visable to low er t h e frequ en cy of st im u lat ion an d p rolon g t h e
rep or ted th at BIS m on itoring can sign ifican tly redu ce th e risk of sin gle st im u li. Th e in ten sit y of st im u lat ion can be as h igh as 50
an esth esia aw aren ess du ring su rger y.7 Th e sen sor is placed on m A. Tw o h u n dred an d fift y rep et it ion s p er averaging cycle are
th e pat ien t’s foreh ead an d p rovides valu es from 0 (equ ivalen t to su fficien t to acqu ire adequ ate p oten t ials w ith a good sign al-to-
EEG silen ce) to 100 (equ ivalen t to fu lly aw ake) derived from EEG n oise rat io.
dat a. A BIS valu e bet w een 40 an d 60 sh ould be th e goal d u ring an Th e st im u lat ion of p er ip h eral n er ves resu lt s in a sp read in g
operat ion . of act ion poten t ial along th e ascen ding path w ays of th e dorsal
colu m n an d elect r ical act ivat ion of t h e p r im ar y sen sor y cor tex
of th e con t ralateral postcen t ral gyrus w h ere it can be recorded
Monitoring th rough elect rodes in th e scalp.8,9
Electroencephalography Alterat ion s in body tem perat ure or blood pressure, ch anges in
th e t ype an d level of an esth et ics, an d p n eu m ocep h alu s can lead
Electroen cephalography provides inform ation about cortical and to ch anges in SSEPs, in dep en den t of surgical m an ipulat ion .
su bcor t ical fu n ct ion , bu t n ot deeper st r u ct u res su ch as sen so-
rim otor t ract s, CNs, or th e sp in al cord. EEG recordings presen t a
su m m at ion of excitator y an d in h ibitor y p oten t ials w ith an am - Motor Evoked Potentials
plit u de of 10 to 100 m V. Elect rodes are placed by conven t ion at Motor evoked p oten t ials can be record ed after d irect elect r ical
th e in tern at ion ally recogn ized “10-20” poin t s. Delt a w aves (u p or m agn et ic st im ulat ion of th e exposed m otor cor tex or by t ran -
to 4 Hz) sign ify “slow w ave sleep” or deep an esth esia, and m ay be scran ial st im u lat ion . Tran scran ial elect rical MEPs w ith a t rain
presen t after isch em ic inju r y to th e brain . Th eta w aves (4–7 Hz) st im u lat ion or m u lt i-pu lse sequ en ces h ave becom e st an dard for
are m ost com m on ly seen during gen eral an esth esia or after isch - n eu rovascu lar proced ures. Corkscrew elect rodes are placed over
em ic even t s, in toxicat ion , an d severe m et abolic im balan ce. Alph a C3 and C4 (international 10–20 EEG system ). An intensit y of stim -
w ave act ivit y (8–12 Hz) is seen m ost frequ en tly over th e occip i- ulat ion of 100 m A is sufficien t to receive adequate poten t ials an d
tal lobe in an aw ake pat ien t w ith closed eyes. Bet a w aves (12–30 stim ulation should not exceed 200 m A; especially w hen the m otor
Hz) sign ify m en t al act ivit y or con cen t rat ion , or can be provoked cor tex is exp osed, 10–20 m A is su fficien t .
w ith sm all doses of barbit u rates an d ben zodiazepin es. During Th e st im u lat ion lead s to act ivat ion of t h e pyram idal t ract
su rger y u n d er d eep an est h esia n eit h er alp h a n or bet a w ave ac- an d descen ding act ivit y along th e cor t icospin al t ract . Subderm al
t ivit y is iden t ified. n eedles are used to record m uscle MEPs. Ch anges in am plit ude
Cor t ical elect rical act ivit y u ses n early 50% of th e brain’s oxy- an d laten cy of respon se as w ell as m otor th resh old suggest st ru c-
gen dem an d w h ile th e rem ain der is used to m ain tain cellular t u ral dam age to t h e m otor system . Su it able m u scles for st im u -
in tegrit y. W h en oxygen su pp ly decreases, d u ring occlu sion of a lat ion are th e abductor pollicis brevis or forearm flexors for th e
m ajor vessel for exam p le, redu ced EEG act ivit y p rovides a w arn - u pper ext rem it ies, an d th e abdu ctor h allu cis brevis an d an terior
ing to th e surgeon of im p en ding inju r y. t ibial m uscle for th e low er ext rem it ies.
In clin ical pract ice t w o recording elect rodes per h em isph ere, In fluen cing factors th at m ay lead to ch anges in or loss of MEPs
on e for t h e an ter ior cerebral ar ter y (ACA) ter r itor y an d on e for in clude h alogen ated an esth et ics su ch as en fluran e, fluran e, an d
t h e m id d le cerebral ar ter y (MCA) ter r itor y, are com m on ly u sed isoflu ran e, an d m u scle rela xan t s. Ot h e r factor s in clu d e blood
for m on itor ing. p ressu re ch an ges an d com p ression of p er ip h eral n er ves in case
of p oor p at ien t p osit ion ing can fu r th er d ecrease reliabilit y of
m on itoring.
Evoked Potentials
Elect rical st im u lat ion of th e n er vous system result s in respon ses
Auditory Evoked Potentials
kn ow n as evoked poten t ials (EPs). EPs h ave specific sizes an d la-
ten cies, and these param eters carr y im portan t inform ation about Au d itor y evoked p oten t ials are gen erated by rep et it ive click
th e in tegrit y of th e tested path w ay. Advan ced com p utat ion al al- sou n d s of 95 d B ap p lied t h rough an ear p lug, w h ile d eafen ing
gorith m s th at allow for sum m at ion an d averaging of EPs w h ile t h e ot h er ear w it h a con t in u ou s n oise of 65 d B. Poten t ials are
elim in at ing backgrou n d n oise h ave facilitated th e m on itoring of recorded by an elect rode placed in fron t of th e t ragus. Clin ical
th e n at ive n er ve poten t ials. evalu at ion is based on th e am plit u de an d laten cy of th e evoked
poten t ials. Th ese p oten t ials h ave a ver y low am plit u de (< 1 µV)
an d a sh or t laten cy (< 6 m s). Given th e low am plit u de, am plifi-
Somatosensory Evoked Potentials
cat ion sh ou ld be m axim ized an d th e frequ en cy of st im u lat ion
Som atosen sor y evoked poten t ial provide an object ive fu n ct ion al sh ou ld be h igh e n ough to allow fast d ete ct ion of p at h ological
obser vat ion of th e som atosen sor y system . Th ese poten t ials are alte rat ion s w h ile p rese r vin g t h e abilit y for sin gle im p u lse
gen erated by th e st im u lat ion of periph eral n er ves in th e upper discrim in at ion .
an d low er ext rem it ies. In th e u p p er ext rem it y, th e m edian n er ve Th e evoked sign al t ravels from th e coch lea th rough th e co-
can be m on itored by in ser t ion of a bip olar st im u lat ion probe at ch lear n er ve an d coch lear n u cleu s, crosses to t h e con t ralateral
th e carpel t u n n el. In th e low er ext rem it y, th is can be ach ieved by lateral lem n iscu s, t h e in fer ior collicu lu s in t h e m id brain , an d
placing a p robe p osterior to th e m edial m alleolu s for th e t ibial t h e m ed ial gen icu late body to reach t h e p r im ar y au d itor y cor-
n er ve. In case of poor qualit y of th e acquired poten t ials, it is ad- tex. W it h in 1 secon d after st im u lat ion , ~ 20 evoked w aves are

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152 II Evaluation and Treatment Considerations for Neurovascular Disease

Epidural Motor Evoked Potentials (D-w ave)


Ep idu ral MEPs or D-w aves are evoked by t ran scran ial elect rical
st im u lat ion . Recordings are obt ain ed from th e sp in al cord by an
epidurally inserted strip electrode w hen using the single-stim ulus
tech n ique. Th e am plit ude of th e D-w ave is a relat ive m easure for
th e n u m ber of fast con du ct ing fibers in th e cor t icosp in al t ract .
In t raoperat ive reduct ion s of th e D-w ave am plit ude are gradual.
An irreversible injur y to th e spin al cord correlates w ith an am pli-
t u de redu ct ion of m ore th an 50%. W h en th e am p lit u d e of th e
D-w ave is com bin ed w ith m u scle MEPs, it h as a h igh predict ive
value for n eu rological ou tcom es. Pat ien ts w ith an in t raoperat ive
loss of m u scle MEPs bu t preser vat ion of th e D-w ave gen erally
have an im m ediate postoperative m otor deficit that gradually im -
proves. An additional reduction of 50%or even loss of the D-w ave
predicts a p erm an en t m otor d eficit .11 An esth et ics or m uscle re-
laxan t s h ardly in fluen ce th e record ing of th e D-w ave.

Electromyography of Cranial Nerves


W h en discu ssing EMG of CNs, on e h as to d ifferen t iate bet w een
(1) direct st im ulat ion of th e exposed m otor n er ve to iden t ify an d
m on itor n er ve fun ct ion , an d (2) free-ru n EMG for m on itoring
spon tan eou s CN act ivit y.
Mon itoring of CNs w as in it ially developed for su rger y of th e
cerebellopon t in e angle.12 Th e facial n er ve w as iden t ified th rough
sim ultaneous stim ulation of the ner ve an d obser ving the patien t’s
face. Delgado et al13 w ere th e first to report EMG poten t ials de-
rived from facial m uscles follow ing stim ulation of the intracranial
asp ect of t h e facial n er ve. Sin ce Møller an d Jan n et t a’s 12 p u blica-
t ion in 1985, m on o - or bip olar st im u lat ion of CNs an d t h e re-
Fig. 11.1 Auditory evoked potential recorded during surgical procedure. cord ing of p oten t ials from th e corresp on ding m u scles by n eedle
Baseline m easurem ent s are noted at the bot tom and continuous intra elect rod es h as becom e a stan dard procedu re for all m otor
operative measurem ents on top. Waves I, III, and V are marked. (Courtesy CNs.14,15 In addit ion , direct st im ulat ion of exposed cen t ral n eural
of Nikolai Hopf.)
st r u ct u res, id en t ificat ion an d d iscr im in at ion of CNs, n u clei, or
t ract s is p ossible.16,17
A bipolar st im ulat ion probe is u sed w ith 0.05 to 2 m A for
gen erated, th ough on ly w aves I th rough V are of clin ical rele- st im u lat ing CN n u clei. Th e sign al regist rat ion is p erform ed by
van ce (Fig. 11.1). Th ese five w aves can be correlated to an atom ic paired needle electrodes w ithin the corresponding m uscle. Ner ve
lan dm arks w ith in th e au ditor y path w ay. Wave I h as its origin in fu n ct ion can be con t rolled by sequ en t ial st im u lat ion of th e n er ve
th e dist al coch lear n er ve, w ave II in th e ju n ct ion bet w een th e in different locations (proxim al and distal) throughout the proce-
n er ve and coch lear n ucleus, w ave III from th e caudal par t of th e dure. Th e laten cy of the poten tial after distal stim ulat ion sh ould
pon s, w ave IV from th e m edial lem n iscu s, an d w ave V project s to be low er th an after proxim al st im ulat ion in an in t act n er ve. In
th e in ferior collicu lu s. case on ly dist al st im u lat ion resu lt s in a p oten t ial, a discon t in u a-
Factors th at can in flu en ce th e poten t ials are a sudden drop of t ion w ith in th e n er ve m u st be p resen t an d a postop erat ive defi-
pat ien t tem perat u re or blood p ressu re, lou d n oises w ith in th e cit is likely.
operat ing room , ret ractors, or alterat ion in tem perat ure w ith in Cerebrosp in al flu id (CSF) can alter t h e st im u lu s by sh or t-
th e surgical field. cu t t ing th e cu r ren t . If p roxim al an d dist al laten cies are iden t i-
cal, t ran sm ission th rough th e CSF an d n ot th e n er ve sh ou ld be
su sp ected, an d t h e m easu rem en t sh ou ld be rep eated in a dr y
Visual Evoked Potentials
set t ing.
Visu al evoked p oten t ials can be m on itored for all p ath ologies In addition to direct stim ulation, the recording of free-running
arou n d t h e visu al system . Th e in t rodu ct ion of p ow er fu l ligh t - EMG for th e m on itoring of spon t an eou s CN act ivit y is possible
em it t in g d iod es (LEDs) h as m ad e a st able st im u lat ion of t h e (Fig. 11.2).14,16 In appropriate m an ipu lat ion or inju r y (e.g., th e
visu al system possible.10 Curren tly, an exact an atom ic correla- st retch ing of a CN by ret ract ion ) can be recogn ized . Feedback is
t ion of ch anges in am plit ude or laten cy is n ot p ossible. Given th at provided in real t im e an d can be u sed to opt im ize th e safet y of
am plit ude an d laten cy are in fluen ced by an esth esia, VEP m on i- th e p rocedu re. Tw o t ypes of EMG p oten t ials are p ossible. Con t act
toring is n ot yet con sidered a stan dard procedure during n euro- act ivit y describes an elect rical act ivit y, w h ich t akes place sim ul-
vascu lar procedu res. tan eously to surgical m an ipulat ion (con t act) an d ceases directly

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11 Neuromonitoring 153
Fig. 11.2 The standard needle positions for electromyography
(EMG) monitoring of cranial nerves (CNs). The electrode for m oni
toring CN X is em bedded within the respiratory tube. (Courtesy of
Nikolai Hopf.)

after m an ipulat ion is stopped. Path ological act ivit y or path ologi-
cal spon t an eou s act ivit y exceeds su rgical m an ip u lat ion an d, in
■ Mapping
con t rast to con tact act ivit y, in dicates im p airm en t of th e n eu ral Intraoperative Mapping
st r u ct u re an d p ostoperat ive deficit . Long-last ing act ivit ies w ith
h igh frequen cies an d am plit u des, w h ich in dicate a loss of n er ve Direct Cortical Stimulation
fibers, are predict ive of postoperat ive deficits, w h ile sh or t an d
syn ch ron al act ivit y in m u lt ip le ch an n els is m ostly du e to Lesion s aroun d or directly w ith in eloquen t areas m igh t alter n or-
ar t ifacts. m al an atom y to such an exten t th at it becom es difficult for th e
surgeon to iden t ify th ese areas correctly.19 Fun ct ion al m apping
w ith in t raoperat ive direct cor t ical st im ulat ion as it w as pub -
The Bulbospongiosus Reflex
lish ed by Foerster, Pen field, an d Jasper in 1954 rem ain s th e “gold
Th e bu lbosp ongiosu s reflex (BSR), p reviou sly called th e bu lbo- st an dard” in th ese cases. After cor t ical exp osu re, sh or t t rain s of
cavern osu s reflex, is a polysyn apt ic reflex th at is u sed for m on i- five st im u li w ith a pulse w idth of 0.5 m s an d an in terst im u lu s
toring an al sph in cter fun ct ion . St im u lat ion of th e dorsal pen ile/ in ter val of 4 m s are applied. St im ulat ion in ten sit y is in creased in
clitoral n er ve is ach ieved th rough a ring elect rode arou n d th e steps of 1 m A w ith an u pp er in ten sit y lim it of 25 m A u n t il an
pen is or t w o su rface elect rodes over th e clitoris an d labiu m . A EMG resp on se is recorded (Fig. 11.3). Motor p oten t ials are re-
sh or t t rain of five st im u lat ion s is effect ive for opt im al st im u la- corded from lim b m u scles th rough n eedle elect rodes, w h ile th e
t ion .18 Th e recording of p oten t ials is obt ain ed from th e extern al pat ien t is in st ru cted to p erform tasks. Ever y st im u lated area is
an al sph in cter m uscle w ith t w o n eedle elect rodes. Preser vat ion m arked w ith a n um ber creat ing an in dividual m ap of m otor
of th e BSR during surger y in dicates in t act postoperat ive sph in c- fu n ct ion for th e p at ien t .20 In tegrit y of areas adjacen t to th e le-
ter cont rol, w h ile an in t raoperat ive loss of th e BSR in dicates an at sion , as w ell as su bcor t ical fiber t ract s, can be ch ecked th rough -
least t ran sien t loss of sp h in cter con t rol. Th e sam e an esth esia out th e procedu re. Good neurological outcom es correlate w ith
regim en recom m en ded for rou t in e MEPs sh ou ld be used w h en in tact poten t ials. Ch anges in an esth esia an d th e u se of m u scle
m on itoring BSR. relaxan ts m ay lim it th e u t ilit y of direct cor t ical st im u lat ion .

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154 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 11.3 Intraoperative direct cortical stim ulation. Top:


intraoperative im age of direct cortical stimulation (DCS)
after localizing the m otor cortex by neuronavigation. Bot-
tom: DCS responses from upper extrem it y with large re
sponse from biceps and sm all hand m uscles. (Courtesy of
Nikolai Hopf.)

Phase Reversal Speech Monitoring


Ph ase reversal is a m eth od of locat ing th e cen t ral su lcu s th rough Th e m on itoring of sp eech fu n ct ion for vascu lar lesion s arou n d
cor t ical recording of SSEPs of t h e m edian or t ibial n er ve.21 Th e Broca’s and Wernicke’s areas requires the cooperation of an aw ake
polarit y of th e recorded p oten t ials from th e sen sor y an d th e pat ien t . Th e m odern regim en of p rop ofol an d rem ifen t an il en -
m otor gyri are reversed (p h ase reversal), an d th is reversal is th e ables th e an esth esiologist to closely con t rol a pat ien t’s level of
basis for th is m eth od of m on itoring. W h ile st im u lat ing th e t ibial an algesia an d sedat ion . Th is com bin at ion en sures pat ien t com -
or m edian n er ve, th e exposed cortex is m apped by placing st rip for t , w h ile allow ing rapid ret urn to con sciousn ess in t raopera-
elect rodes for recording or th ogon ally across w h at th e su rgeon t ively for aw ake cor t ical m app ing an d sp eech fu n ct ion con t rol.
assu m es is th e cen t ral sulcu s. Th e st rip elect rodes sh ould con - An experien ced su rgical team th at in clu des a speech th erapist is
tain four or m ore in dividually recording elect rodes. Som atosen - crit ical for th e effect ive im p lem en tat ion of th is m odalit y.
sor y poten t ials recorded from th e cor tex are h igh am plit u de an d In t raoperat ively, p at ien t s are posit ion ed com for t ably on th e
in ter p ret able resp on ses are read ily obt ain ed by d irect obser va- back w ith th e h ead t urn ed sligh tly to th e righ t an d fixed in th e
t ion of p oten t ials or after m in im al averagin g. Th is tech n iqu e Mayfield clam p . Follow ing cran iotom y an d th e op en ing of th e
com m on ly requ ires less th an 10 records. Recording from an elec- du ra, th e p at ien t is aw aken ed . Th e pat ien t is asked to n am e ou t
t rode on th e sen sor y cor tex leads to a p rom in en t n egat ive peak lou d th e objects presen ted by th e speech th erap ist on sp ecific
w ith a laten cy of ~ 20 m s regarding th e m edian n er ve, an d a posi- cards or a com pu ter screen . Sim ultan eously, th e surgeon applies
t ive peak after 40 m s for th e t ibial n er ve. Recording from an elec- a 4-secon d bipolar st im ulat ion of 5 to 20 m A to th e cor t ical
t rode on th e m otor cor tex leads to a p osit ive p eak (Fig. 11.4). st r u ct u res. As a resu lt of th e st im u lat ion , ep ilept ic seizu res m ay
Th u s, th e cen t ral su lcu s is located bet w een th e posit ive an d n eg- occur; th us, con t in uous EEG m on itoring during th e procedure is
at ive p eaks. In flu en cing factors are th e sam e as for regu lar SSEP required. St im u lat ion of Broca’s or Wern icke’s area result s in
m on itoring. t ran sien t aph asia. Poin ts of st im u lat ion are m arked by n u m bers

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11 Neuromonitoring 155

n eu ron avigat ion , com bin ed w ith a n avigated m agn et ic coil, an d


a com pu ter in terface for calcu lat ing th e dist ribut ion of th e elec-
t rical field, dep en ding on in dividu al an atom y an d coil p osit ion . A
previously obtained m agnetizat ion -prepared rapid gradient-echo
(MP-RAGE) sequ en ce is n ecessar y for accu rate localizat ion . Th e
pat ien t is registered in th e nTMS n eu ron avigat ion system u sing
th e in tegrated p rotocol of su rface an d lan dm ark regist rat ion .
TMS applies a m agn et ically in duced cu rren t in side a t issue, th us
elicit ing a d irect elect r ical st im u lat ion as u sed in t h e in t raop -
erat ive DCS. EMG is record ed from t h e lim b m u scles. Posit ive
respon ses reflect ing th e m otor cor tex are in tegrated via digit al
im aging an d com m un icat ion s in m edicin e (DICOM) im por t in
th e in t raop erat ive n eu ron avigat ion soft w are iPlan 2.0 (Brain lab,
Feld kirch en , Ger m any), fu sed to t h e MP-RAGE im ages an d ex-
por ted to th e operat ing room (Fig. 11.5).
nTMS requ ires a m in im u m level of com p lian ce an d can be
u sed in ap h asic p at ien t s an d t h ose su ffer in g from d em en t ia or
severe fron t al lobe syn drom e w h o m ay n ot be able to p erform
a specific fMRI m otor paradigm . nTMS is par t icularly useful for
AVMs w h ere fMRI often is n ot feasible, an d in n on -com plian t
sm all ch ild ren w h ere it m ay be th e on ly opt ion for p reop erat ive
fun ct ion al test ing.

■ Clinical Implications
Supratentorial Aneurysms
• Vascular lesions
Fig. 11.4 Cortical recording of som atosensory evoked potentials for lo • Aneurysms of the internal carotid artery (ICA), anterior
calization of the central sulcus. Phase reversal can be observed bet ween
electrodes t wo and three. (Courtesy of Nikolai Hopf.)
cerebral artery (ACA), m iddle cerebral artery (MCA),
posterior com m unicating artery (PCoA), anterior com m u
nicating artery (ACoA)
• Structures at risk
creat ing an in dividual cor t ical m ap w ith respect to speech fun c- • Speech area: production and comprehension
t ion for th e p at ien t .20 After m ap ping, resect ion of th e vascu lar • Motor and sensory cortex
lesion can eith er be com pleted w ith gen eral an esth esia if elo- • Recommended monitoring
qu en t areas p rove to be a safe dist an ce from th e lesion , or in an • MEP, SSEP
aw ake pat ien t perform ing repet it ive speech m on itoring w h en • BIS
lesion s involve crit ical st r u ct u res. • Optional monitoring
• Awake craniotomy
• EEG
Preoperative Mapping
Navigated Transcranial Magnetic Stimulation
Illustrative Case
Today, preop erat ive n on invasive localizat ion of brain fu n ct ion s is
perform ed by fu n ct ion al m agn et ic reson an ce im aging (fMRI). To A 49-year-old wom an w ith a h istory of aneurysm al subarachnoid
detect th e m otor cor tex, th e p at ien t is su bjected to a stan dard h em orrh age (SAH) an d m ult iple cerebral an eur ysm s presen ted
m otor paradigm . Because th e resolut ion is h igh ly depen den t on for evalu at ion . Th e pat ien t w as n eurologically in tact despite th e
th e p at ien t’s m otor t ask p erform an ce, th e m eth od h as lim it a- h istor y of h em or rh age. Her m u lt ip le an eu r ysm s w ere t reated
t ion s in n on com p lian t or p aret ic p at ien ts.22 Addit ion ally, AVMs u sing m icrosu rgical an d en d ovascu lar tech n iqu es. Follow -u p
t radit ion ally p ose a p roblem for fMRI becau se of u n u sual h em o- cath eter angiograp hy revealed recu rren ce of a previou sly t reated
dyn am ics.23 Navigated t ran scran ial m agn et ic st im u lat ion (nTMS) left-sided MCA an eu r ysm .
is a n ovel altern at ive for preop erat ive fu n ct ion al m ap ping th at Su rgical clipp ing w as p lan n ed via a left su p raorbit al app roach
detect s eloqu en t cor t ical areas directly, com p arable to in t raop - through an eyebrow incision. Continuous SSEP and MEP m onitoring
erat ive DCS.24 w as ap plied. In t raop erat ively m u lt iple coil fragm en ts w ere fou n d
Th e NBS System 4 (Nexst im , Helsin ki, Fin lan d) is th e first to be outside of th e an eu r ysm in th e su barach n oid space. Th is
com m ercially available system for nTMS. Th is system con sist s of led to perforat ion of th e in ferior bran ch of th e MCA du ring dis-
an opt ical t racking system as a base for a n on invasive fram eless sect ion . Tem p orar y clipp ing of th e M1 segm en t w as n ecessar y to
(text cont inues on page 158)

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156 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

Fig. 11.5a–g Anteroposterior (AP) (a) and lateral (b) pre-


operative catheter angiography showing an arteriovenous
malformation (AVM) in the central region. (c) Preoperative
localization of the m otor cortex via navigated transcranial
c magnetic stim ulation (nTMS).

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Fig. 11.5a–g (continued ) Dots within magnetic resonance
imaging m ark spots of m otor responses after stimulation.
Intraoperative screenshot of direct cortical stimulation (d),
and it s m otor responses (e ), used sim ultaneously with
neuronavigation showing good correlation with nTMS.
Postoperative AP (f) and lateral (g) angiography confirm s
com plete resection of the lesion. (Courtesy of Nikolai
Hopf.)

f g

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158 II Evaluation and Treatment Considerations for Neurovascular Disease

close th e perforated vessel w all. SSEP am p lit u de decreased after Ret rospect ive an alysis of nTMS an d DCS dat a sh ow ed excellen t
5 m in u tes of vessel occlu sion , w h ereas MEPs rem ain ed st able correlat ion .
(Fig. 11.6). Con sequ en tly, th e M1-segm en t w as reopen ed before
t h e clip p in g of t h e an e u r ysm . Th e SSEPs ret u r n ed to n or m al
am plit ude im m ediately. Clipp ing th e an eu r ysm itself dem an ded Vascular Lesions of Broca’s and
repeated tem porary M1 occlusion. Therefore, the patient was pre- Wernicke’s Areas
oxygen ated p rior to clipp ing. Clip p ing th e an eu r ysm dem an ded
8 m in u tes of tem porar y M1 occlusion . At th e t im e of tem porar y • Vascular lesions
clipp ing SSEP an d MEP am p lit u d es st ar ted to decrease. Reop en - • Aneurysm: left MCA, left ICA
ing of th e M1-segm en t resulted in th e im m ediate recover y of • AVM: left temporal, left insular, left frontal
SSEP an d MEP am p lit u des. • Cavernous malformation: speech area
Postoperatively no new n eurologic deficit w as apparent. Cath - • Structures at risk
eter angiography con firm ed th e com plete occlu sion of th e MCA • Speech area: production and comprehension
an eur ysm . A com puted tom ography (CT) scan before disch arge • Motor cortex: left side
sh ow ed no isch em ic ch anges. • Sensory cortex: left side
• Recommended monitoring
• MEP, SSEP
Rolandic Vascular Lesions • BIS
• Optional monitoring
• Vascular lesions • Awake craniotomy
• Aneurysm: MCA, ICA • DCS: mapping of speech area
• AVM: central region • EEG: recognition of epileptic activit y
• Cavernous malformation: central region
• Structures at risk
• Motor and sensory cortex Illustrative Case
• Recommended monitoring
• MEP, SSEP A 43-year-old w om an presen ted w ith acu te on set of bilateral
• DCS, BIS t in n it us. MRI w as suspiciou s for an AVM. In it ial cath eter angiog-
• Optional monitoring raphy revealed a fron totem poral Sp et zler-Mart in grade IV AVM
• nTMS: preoperative mapping adjacen t to Broca’s area. Mult iple en dovascular par t ial em boliza-
t ion s led to th e redu ct ion of AVM size, bu t th e act ive residu al w as
close to Broca’s area. Endovascular test occlusion of the proxim al
feeding vessel (M2 segm en t) resulted in com plete speech arrest .
Illustrative Case
Therefore, an aw ake craniotom y for resection of the residual AVM
A 63-year-old m an presen ted w ith th e acute on set of a m assive w as in dicated.
headache. A CT scan revealed a sm all at ypical subarach noid h em - Con t in u ou s SSEP an d MEP m on itoring w as app lied as w ell as
orrh age w ith in th e cen t ral su lcu s. Cath eter angiography sh ow ed in t raop erat ive sp eech test ing. EEG w as recorded to detect pos-
a Sp et zler-Mar t in grade II AVM w ith in th e p recen t ral su lcu s. At- sible in t raop erat ive seizu res. Cran iotom y w as p erform ed w ith
tem pted en dovascu lar em bolizat ion w as u n su ccessfu l, so op era- th e pat ien t u n der gen eral an esth esia. After th e op en ing of th e
t ive resect ion of th e AVM w as in dicated. du ra, sedat ion w as term in ated an d Broca’s area w as id en t ified by
Preoperat ive localizat ion of th e m otor cor tex by fMRI w as n ot direct cor t ical st im u lat ion . Du ring resect ion of th e AVM, crit ical
con clu sive d u e to ar t ifact s by t h e AVM. nTMS w as p erform ed an d vessels w ere tem porarily occluded un der repet it ive speech test-
t h e m otor cor tex (h an d kn ob) w as id en t ified d irect ly p oster ior ing (Fig. 11.7). In case of in tact fun ct ion , th e resect ion w as re-
to th e sulcal AVM. Neu ron avigat ion w as u sed for th e plan n ing of su m ed. W h en test occlu sion led to speech arrest , th e vessel w as
a m in im ally invasive approach . Con t in uou s SSEP an d MEP m on i- reopen ed an d th e resect ion w as stopp ed .
toring w as used. After open ing of th e dura, th e m otor cor tex w as Th e p at ien t tolerated su rger y w ell. All in t raop erat ive deficit s
located by DCS (Fig. 11.5). Com p lete resect ion of th e AVM w as w ere tem porar y an d resolved com pletely during surger y after
in ten ded. SSEP an d MEP m on itoring stayed st able th rough out th e reop en ing of th e resp ect ive vessel. No n ew n eu rologic d eficit
th e procedu re. occurred postoperat ively. As expected, postoperat ive angiogra-
Postoperat ively, n o n ew n eurologic deficit s w ere n oted. Cath - phy sh ow ed a sm all residu al of th e AVM, an d th u s stereotact ic
eter angiography con firm ed th e com plete resect ion of th e AVM. radiosu rger y w as in it iated .

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11 Neuromonitoring 159
Fig. 11.6a–d (a) Intraoperative som atosensory evoked potential (SSEP) m onitoring with baseline at the
bot tom . The highlighted section represents temporary clipping of the M1 segm ent with a decrease in
SSEP am plitudes. After reopening of the artery, SSEPs return to norm al. (b) Preoperative anteroposterior
(AP) angiography of previously coiled aneurysm . (c) Intraoperative view showing coils within the arach
noid space and t wisting around one M2 branch, leading to perforation. (d) Postoperative AP angiography
with complete occlusion of the aneurysm . (Courtesy of Nikolai Hopf.)

c d

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160 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

Fig . 11.7a– d (a) Preoperative anteroposterior (AP)


angiography of the arteriovenous m alform ation (AVM).
(b) Postoperative AP angiography dem onstrates a sm all
rem nant of the AVM. (c) Intraoperative screenshot of
neuronavigation system after m apping of Broca’s area via
c speech testing.

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11 Neuromonitoring 161
Fig. 11.7a–d (continued) (d) Intraoperative pic
ture of fully awake patient performing speech
testing with speech therapist presenting objects
on cards. (Courtesy of Nikolai Hopf.)

Vascular Lesions of the Cerebellopontine Angle an d MEP m on itoring as w ell as EMG of CNs V to XI w as applied.
Total resect ion of th e AVM w as ach ieved w ith ou t altering th e
• Vascular lesions m on itored st ru ct ures.
• Aneurysm: posterior circulation Postoperat ively th e pat ien t sh ow ed n ew cerebellar sym ptom s
• AVM: cerebellar due to resection of a large part of th e right cerebellar h em isph ere.
• Cavernous malformation No CN dist u rban ce w as n oted. Cat h eter angiograp hy verified a
• Structures at risk com plete resect ion of th e AVM (Fig. 11.8). MRI sh ow ed n o isch -
• Cranial nerves em ic ch anges.
• Brainstem
• Cerebellum
• Recommended monitoring Vascular Lesions of the Brainstem
• EMG of CN III–XI
• Vascular lesions
• MEP, SSEP
• Cavernous malformation
• BIS
• AVM
• Aneurysms: vertebral artery (VA), basilar artery (BA)
• Structures at risk
Illustrative Case • Brainstem: motor and sensory tracts
• Cranial nerve nuclei
A 16-year-old girl in it ially presen ted w ith a cerebellar h em or-
• Recommended monitoring
rh age su sp iciou s for an AVM. Cat h eter an giograp hy revealed a
• MEP, SSEP
r igh t -sided in fraten torial Spet zler-Mar t in grade IV AVM w ith
• EMG of CN III–XI
feeders from th e righ t posterior in ferior cerebellar arter y (PICA)
• BIS
an d an terior in ferior cerebellar ar ter y (AICA). An MRI sh ow ed ex-
ten sion of th e AVM from th e righ t cerebellopon t in e angle to th e
fou rth ven t ricle an d th e sigm oid sin us. Mult iple en dovascular
Illustrative Case
em bolizat ion s led to sign ifican t size redu ct ion of th e act ive part
of th e AVM. Follow ing th e last en dovascular t reat m en t , th e pa- A 24-year-old m an presen ted w ith acute on set of a sligh t left-
t ien t develop ed a left-sided sen sor y loss as w ell as a loss of h ear- sided hem iparesis and elevated reflexes of the left upper and lower
ing on th e righ t sid e. ext rem it y. In it ial MRI revealed a righ t-sided pon t in e cavern ou s
Surgical resection of th e AVM w as plann ed th rough a right ret- m alform at ion accom pan ied by an acu te h em orrh age of ~ 18 m m
rosigm oid approach aided by n euron avigat ion . Con t in uous SSEP in diam eter (Fig. 11.9).
(text cont inues on page 164)

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162 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

c d

Fig. 11.8a–d Preoperative T2 weighted magnetic resonance im age (MRI) to cranial nerves. Postoperative T2 weighted MRI (c) and lateral angiogram
(a) and lateral angiogram (b) of an arteriovenous m alform ation of the (d) dem onstrate no evidence of residual. (Courtesy of Nikolai Hopf.)
cerebellopontine angle. Complete resection was achieved without dam age

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11 Neuromonitoring 163

a b

c d

Fig. 11.9a–f Preoperative T2 weighted axial (a) and T1 weighted sagit tal malform ation. (c,d) Intraoperative endoscopic views after resection of the
(b) magnetic resonance im ages (MRIs) (a) and lateral angiogram (b) of an lesion. (continued on page 164)
arteriovenous m alform ation of the cer of a right sided pontine cavernous

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164 II Evaluation and Treatment Considerations for Neurovascular Disease

e f

Fig. 11.9a–f (continued ) Postoperative T2 weighted axial (e) and T1 weighted sagit tal (f) MRIs confirm complete resection with slight hem orrhage in
side the resection cavit y. (Courtesy of Nikolai Hopf.)

Su rgical resect ion w as p lan n ed u sing a righ t-sided ret rosig- Illustrative Case
m oid ap p roach . Con t in u ou s SSEP an d MEP m on itor ing as w ell
as EMG of CNs III to XII w as ap p lied . Neu ron avigat ion w as u sed A 51-year-old w om an presen ted w ith sud den on set of back pain
to d eter m in e t h e best en t r y p oin t for resect ion . Du r in g blu n t accom pan ied by h eadach e, n ausea, an d vom it ing. Bladder fun c-
resect ion, SSEP an d MEP am plit udes decreased by n early 50%, t ion w as d ist u rbed an d an in creasing sen sor y loss st ar t ing in th e
w h ereas CN m on itoring rem ain ed stable. Com plete resect ion of p er ian al region w as d escr ibed . Sp in al MRI revealed a m assive
th e cavern ous m alform at ion w as ach ieved. sp on t an eou s sp in al su barach n oid h em orrh age. Sp in al cat h eter
Directly after surger y th e pat ien t w as h em iplegic on th e left angiography detected a th oracic (T7) in t radural an eur ysm as th e
side an d su ffered from dou ble vision . Th e dou ble vision van ish ed cau se for th e h em orrh age.
w ith in days, an d th e h em ip aresis recovered steadily. With in 5 Su rger y w as in d icated for decom p ression of th e sp in al cord as
days t h e p at ien t w as able to w alk w it h ou t assist an ce, bu t t h e w ell as occlusion of th e an eur ysm . Con t in u ous SSEP, MEP, an d
p aresis of t h e left h an d rem ain ed m ore p rom in en t . Postop era- D-w ave m on itoring w as ap p lied. A left-sided h em ilam in ectom y
t ive MRI con firm ed th e com p lete resect ion of th e vascu lar lesion on T7 level w as perform ed. After open ing of th e dura, a th ick
w ith out sign s of isch em ic lesion s. m em bran e of coagulated blood w as resected before iden t ifying
th e an eu r ysm adjacen t to th e dorsal aspect of th e sp in al cord
Spinal Vascular Lesions (Fig. 11.10). Test occlusion of the parent vessel did not lead to any
ch anges in evoked sen sor y or m otor poten t ials. Th erefore, th e
• Vascular lesions an eur ysm w as t rapped an d resected com pletely.
• Aneurysm: intradural No n ew n eurologic deficit occurred postoperat ively. Bladder
• AVF: spine fu n ct ion as w ell as sen sor y deficit resolved com p letely w ith in a
• Cavernous malformation: spinal cord few days. Spin al angiography sh ow ed th e com plete disappear-
• Structures at risk an ce of th e an eu r ysm .
• Spinal cord: motor and sensory tracts
• Bladder/bowl function
• Recommended monitoring
• MEP, SSEP ■ Conclusion
• D-wave
• Optional monitoring In t raoperat ive n europhysiological m on itoring is a valuable addi-
• Bulbospongiosus reflex t ion to th e n eu rosu rgical arm am en tariu m an d greatly in creases
th e safet y of n eu rovascular procedures.

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11 Neuromonitoring 165

a b

Fig. 11.10a–c (a) Preoperative sagit tal T2 weighted m ag


netic resonance image showing acute intradural hem or
rhage of the thoracic spine. (b) Anteroposterior spinal angi
ography dem onstrates a thoracic intradural aneurysm at the
level of T7. (c) Intraoperative picture of the partially throm
bosed aneurysm . (Courtesy of Nikolai Hopf.) c

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166 II Evaluation and Treatment Considerations for Neurovascular Disease

References
1. Krayen bü h l N, Sarn th ein J, Oin as M, Erdem E, Krish t AF. MRI-validat ion of 14. Eisn er W, Sch m id UD, Reu len HJ, et al. Th e m ap p ing an d con t in u ou s
SEP m on itoring for ischem ic even t s during m icrosurgical clipping of in - m on itoring of th e in t rin sic m otor n uclei during brain stem surger y. Neu-
t racran ial an eur ysm s. Clin Neu rophysiol 2011;122:1878–1882 rosurger y 1995;37:255–265
2. Sala F, Bricolo A, Faccioli F, Lan teri P, Gerosa M. Surger y for in t ram edullar y 15. Rom stöck J, Strauss C, Fahlbusch R. Continuous electrom yography m onitor-
spin al cord t u m ors: th e role of in t raop erat ive (n eu rop hysiological) m on i- ing of m otor cranial nerves during cerebellopontine angle surger y. J Neuro-
toring. Eu r Spin e J 2007;16(Su p pl 2):S130–S139 surg 2000;93:586–593
3. Sala F, Lan teri P. Brain surger y in m otor areas: th e invaluable assist ance of 16. St rau ss C, Rom stöck J, Nim sky C, Fah lbusch R. In t raoperat ive iden t ifica-
in t raoperat ive n europhysiological m on itoring. J Neurosurg Sci 2003;47: t ion of m otor areas of th e rh om boid fossa using direct st im ulat ion . J Neu-
79–88 rosurg 1993;79:393–399
4. Sala F, Krzan MJ, Delet is V. In t raoperat ive neurophysiological m on itoring 17. Frit schi JA, Reu len HJ, Spet zler RF, Zabram ski JM. Cavern ous m alform a-
in pediat ric n eurosurger y: w hy, w hen , h ow ? Ch ilds Ner v Syst 2002;18: t ion s of t h e brain stem . A review of 139 cases. Act a Neu roch ir (W ien )
264–287 1994;130:35–46
5. Nuw er MR. In t raoperat ive m on itoring of th e spin al cord. Clin Neuro- 18. Delet is V, Vodusek DB. In t raoperat ive recording of th e bulbocavern osus
physiol 2008;119:247 reflex. Neurosurger y 1997;40:88–92, discussion 92–93
6. Møller AR. Int raoperat ive Neurophysiological Mon itoring, 2n d ed. Totow a, 19. Ebeling U, Reulen HJ. Space-occu pying lesion s of th e sen sori-m otor re-
NJ: Hu m an a Press, 2006 gion . Adv Tech St an d Neurosurg 1995;22:137–181
7. Myles PS, Leslie K, McNeil J, Forbes A, Ch an MT. Bispect ral in dex m on itor- 20. Ojem an n G, Ojem an n J, Let t ich E, Berger M. Cort ical language localizat ion
ing to preven t aw aren ess during an aesth esia: th e B-Aw are ran dom ised in left , dom in an t h em isph ere. An elect rical st im ulat ion m apping invest i-
con t rolled t rial. Lancet 2004;363:1757–1763 gat ion in 117 p at ien t s. J Neu rosu rg 1989;71:316–326
8. Grun dy BL. Monitoring of sen sor y evoked poten t ials during n eu rosurgical 21. Cedzich C, Tan iguch i M, Sch äfer S, Sch ram m J. Som atosen sor y evoked po-
operat ion s: m eth ods an d applicat ion s. Neu rosurger y 1982;11:556–575 ten t ial ph ase reversal and direct m otor cor tex st im ulat ion during surger y
9. Grun dy BL, Nelson PB, Doyle E, Procopio PT. In t raoperat ive loss of som ato- in an d aroun d the central region . Neurosurger y 1996;38:962–970
sensor y-evoked potent ials predict s loss of spin al cord fun ct ion . An esth e- 22. St ippich C, Kress B, Och m ann H, Tron n ier V, Sar tor K. [Preoperat ive fun c-
siology 1982;57:321–322 t ion al m agn et ic reson an ce tom ography (FMRI) in pat ien t s w ith rolan dic
10. Kodam a K, Goto T, Sato A, Sakai K, Tan aka Y, Hongo K. St an dard an d lim it a- brain t um ors: in dicat ion , invest igat ion st rategy, p ossibilit ies an d lim ita-
t ion of in t raoperat ive m on itoring of th e visual evoked poten t ial. Act a t ion s of clin ical applicat ion ]. Rofo 2003;175:1042–1050
Neu roch ir (Wien ) 2010;152:643–648 23. Juenger H, Ressel V, Brau n C, et al. Misleading fu nct ion al m agn et ic reso-
11. Delet is V, Sala F. In t raop erat ive n eu rop hysiological m on itor in g of t h e nan ce im aging m apping of the cortical han d representation in a 4-year-old
sp in al cord during spin al cord an d spin e surger y: a review focus on th e boy w ith an arterioven ous m alform at ion of the cen t ral region . J Neuro-
cor t icospin al t ract s. Clin Neurophysiol 2008;119:248–264 surg Pediat r 2009;4:333–338
12. Møller AR, Jan n et t a PJ. Mon itoring of facial n er ve fun ct ion during rem oval 24. Pich t T, Sch m idt S, Bran dt S, et al. Preoperat ive fun ct ion al m apping for
of acoust ic t um or. Am J Otol 1985;Su ppl:27–29 rolan dic brain t u m or surger y: com parison of n avigated t ran scran ial m ag-
13. Delgad o TE, Bu ch eit WA, Rosen h olt z HR, Ch rissian S. In t raop erat ive n et ic st im ulat ion to direct cor t ical st im ulat ion . Neurosurger y 2011;69:
m on itoring of facila m u scle evoked resp on ses obt ain ed by in t racran ial 581–588, discussion 588
st im u lat ion of th e facila n er ve: a m ore accurate tech n ique for facila n er ve
dissect ion . Neurosu rger y 1979;4:418–421

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12 Cerebral Protection
Douglas J. Cook , Jacob Fairhall, Crist ian Valdes, and Michael Tym iansk i

Cerebrovascu lar p roced u res h ave t h e p oten t ial to cau se brain over, w ith in th e isch em ic pen um bra cells m ay go on to die in a
injur y th rough isch em ia in duced by tem porar y or perm an en t delayed fash ion follow ing reperfu sion .4–6
vessel occlusion or by brain ret ract ion . For exam ple, repair of At th e cellular level n um erous m olecular cascades leading to
com p lex brain an eu r ysm s, carot id revascu larizat ion , an d cere- cell death are t riggered in th e set t ing of isch em ia (Fig. 12.1). Cell
bral bypass procedures require tem porar y vessel occlusion an d death occu rs th rough n ecrot ic cell death (im m ediate cell death
periods of cerebral isch em ia. Perm an en t vessel occlu sion m ay related to st ru ct ural dam age to th e cell or act ivat ion of lyso-
occur as a n ecessar y par t of n eurovascular procedures such as in som es) or th rough apoptot ic cell death (a m ore delayed, bu t p re-
h u n ter ian ligat ion or in t h e obliterat ion of ar ter ioven ou s m al- determ in ed cell death p rocess resu lt ing from fatal dam age to cell
for m at ion s an d fist ulas. Perm an en t vessel occlusion or sten osis com pon en ts an d in duct ion of apoptot ic path w ays). In it ially, in
m ay also occur as an iat rogen ic com plicat ion of n eu rosurgical t h e absen ce of oxygen an d glu cose, aerobic resp irat ion is im -
procedures. Hypotension , excessive blood loss, hem odilution , hy- p aired an d cellu lar stores of glu cose an d glycogen are rap id ly
poglycem ia, an d hyp oxia du ring su rger y m ay p rovoke isch em ic d ep leted . W it h in m in u tes of isch em ia on set , oxidat ive p h os-
injur y, p ar t icularly in th e case of flow -lim it ing disease states, p h or ylat ion ceases an d cellu lar con cen t rat ion s of h igh -en ergy
in clu ding m oyam oya disease an d ath erosclerot ic sten osis or oc- ph osph ates drop precipitou sly. At th is p oin t an aerobic glycolysis
clu sion . Based on a con t in u ou sly im p roving u n derst an ding of th e is in it iated an d lact ic acid con cen t rat ion s in crease, lead in g to
path ophysiology un derlying ischem ic brain injury and a desire to t issu e acidosis. En ergy-depen den t h om eostat ic m ech an ism s in
avoid perm an en t n eu rologic injur y related to cerebral isch em ia, n euron s an d glia fail in th e absen ce of h igh -en ergy ph osph ates.
several st rategies to p rotect th e brain from isch em ic cell death In par ticular, Na +-K+–aden osine triphosph atase (ATPase) fails, re-
h ave been explored an d em p loyed in n eu rovascu lar su rger y. sulting in elevated int racellular Na + con cen t rat ion s an d cell sw ell-
ing, m an ifest at th e t issu e level as cytotoxic edem a. Sust ain ed
h om eostat ic failure result s in n ecrot ic cell death ; h ow ever, early
cell sw elling m ay be reversible if en ergy stores are restored.
■ Pathophysiology of Cerebral Ischemia Syn apt ic reu pt ake of t h e excit ator y n eu rot ran sm it ter glu -
t am ate is im p aired in en ergy failu re, resu lt ing in act ivat ion of
and the Concept of Neuroprotection N-m et hyl-D-asp ar t ate (NMDA), α -am in o -3-hyd roxy-5-m et hyl-
Cerebral isch em ia is defin ed as a decrease in cerebral blood flow 4-isoxazoleproprion ic acid (AMPA) an d oth er m et abot ropic glu -
below the m etabolic requirem ents for norm al physiological func- tam ate receptors w ith result an t in flu x of calciu m . Elevated in t ra-
tion in a given region of th e brain . In region s w ith blood flow less cellular calcium results in degradat ion of st ruct u ral in t racellular
th an 8 m L/100 g t issu e/m in u te, t issu e rap idly u n dergoes n ecrot ic protein s an d ext racellu lar m at rix protein s, resu lt ing in cellu lar
cell death .1 In th e case of cerebral ar terial occlu sion , th is “core” dam age, loss of cell– cell adh esion , an d cell death . Calciu m in flu x
region is gen erally su rrou n ded by th e “isch em ic pen u m bra,” a resu lt s in direct act ivat ion of th e ph osp h olipases, w ith result an t
zon e of t issue th at suffers from crit ically low blood flow bet w een hydrolysis of ph osph olipids in cell an d m itoch on drial m em bran es
8 an d 20 m L/100 g t issu e/m in u te.2 In region s w it h d ecreased in to free fat t y acids th at are m et abolized to produce leukot rien es
flow there is an initial autoregulator y response that im proves tis- an d prostaglan din s th at in du ce inflam m ator y cascades an d in -
su e p erfu sion an d oxygen at ion .3 In respon se to decreased perfu - crease cell perm eabilit y. Ph osph olipase hydrolyzes cardiolipin
sion pressu re, brain ar terioles dilate an d in crease cerebral blood w ith in m itoch on drial m em bran es an d im pairs th e elect ron t ran s-
volum e, in creasing th e am oun t of blood perfusing th e oligem ic port ch ain resu lt ing in free radical product ion . Dam age to m ito-
region . Th e degree to w h ich th e brain is able to augm en t blood ch on drial m em bran es also resu lt s in dest r u ct ion of m itoch on -
volum e in th is m an n er is term ed th e h em odyn am ic reser ve. At dria an d direct release of p roap optot ic factors cytoch rom e c an d
th e cellu lar level th ere is an elevat ion in oxygen ext ract ion from apoptosis-in ducing factor, prom ot ing cell death th rough act iva-
th e blood in th e set t ing of oligem ia. Th e degree to w h ich oxygen t ion of apoptot ic p ath w ays in clu ding act ivat ion of caspase-3.
ext ract ion can be elevated to overcom e isch em ia is term ed th e Oxidat ive st ress plays a m ajor role in cell death in du ced fol-
perfusion reserve. With contin ued im pairm ent of perfusion these low ing isch em ia. Act ivat ion of NMDA receptors result s in direct
autoregu lator y m ech an ism s becom e exh austed an d even t ually in du ct ion of n it ric oxide syn th ase (NOS).7,8 NOS act ivat ion re-
fail, leading to overall cellu lar failure. On a m acro scale th e isch - su lt s in t h e p rodu ct ion of t h e radical species n it ric oxid e (NO)
em ic pen um bra becom es electrically silent sh ortly after the onset from t h e conversion of argin in e to cit r u llin e.9 Ad d it ion ally, NOS
of isch em ia. If perfusion is restored to th e isch em ic pen um bra, act ivat ion in th e absen ce of argin in e resu lt s in su p eroxid e p ro-
then norm al elect rophysiological function resum es, w hereas w ith d u ct ion , an oth er sou rce of react ive oxygen species.9 NO react s
con t in u ed isch em ia t h e p en u m bra area goes on to die.1,2 More- w it h su p eroxid e to p rod u ce p eroxyn it r ite, a react ive n it rogen

167

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168 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 12.1 Following the onset of ischem ia in the brain cell, death ensues structure, whereas apoptotic mechanisms are triggered by an accumulation
via immediate necrotic and delayed apoptotic mechanisms. Necrotic mecha- of insults to the cell such as the accum ulation of reactive oxygen species,
nism s of cell death result from m ajor disruption of cell hom eostasis or DNA damage, and structural protein damage. ATP, adenosine triphosphate.

sp ecies th at cau ses d irect cellu lar an d m itoch on d r ial dam age. verit y of th e cellular en ergy deprivat ion . Based on th is prem ise,
As p reviou sly described, cardiolip in hydrolysis in m itoch on drial protect ive st rategies for an t icip ated isch em ia in n eu rovascu lar
m em branes by ph osph olipase-A2 results in free radical species su rger y can be grou p ed in to th ree areas: th ose aim ed at redu c-
accum ulation, an additional source of superoxide.10 The en d result ing m etabolic dem an d, th ose aim ed at im proving collateral flow,
of oxidat ive species accum ulat ion is dam age to cell m em bran es an d th ose aim ed at in creasing th e cellu lar toleran ce/reducing
an d m itoch on drial m em bran es, an d injur y to DNA, culm in at ing secon dar y dam age related to isch em ia.
in th e act ivat ion of ap optot ic p ath w ays.
Cell dam age an d death in th e set t ing of cerebral isch em ia re-
su lt from several m ech an ism s. Treat m en t s d esign ed to t arget
th ese in divid u al or m u lt ip le m ech an ism s of cell death h ave been
evalu ated in both an im al m odels an d h u m an clin ical t rials of
■ Cerebral Protection for Neurovascular
acute isch em ic st roke. Th erapies in ten ded to protect th e brain Surgery
from isch em ic cell death or to reverse th e deleteriou s effect s of
Decreasing Energetic Demands
isch em ia can be collect ively grou p ed in to a class of t reat m en ts
term ed n europrotectan t s. Th e con cept of n europrotect ion arose Isch em ia results in cellular en ergy failure, leading to cellu lar
from t h e or igin al obser vat ion of t h e isch em ic pen u m bra an d dam age an d death . En ergy failu re is a resu lt of dim in ish ed raw
t h e p oten t ial to restore n eu rologic fu n ct ion by im proving blood m aterials for aerobic an d an aerobic respirat ion , resu lt ing in a fi-
flow. Th e con cept of n eu roprotect ion also in cludes th e poten t ial nite supply of high -en ergy ph osph ates during ischem ia. Decreas-
to preven t delayed cell death by reversing or op posing apoptosis ing th e rate of con sum pt ion of in t racellular stores of h igh -en ergy
in th e isch em ic pen u m bra. In su m m ar y, cell fate follow ing isch - ph osp h ates, oxygen , glu cose, an d glycogen p rovides m ore t im e
em ia, su r vival or death , can be sim p lified as a scen ario of sup ply bet w een isch em ia on set an d en ergy failure.11 In t u rn , hyp oth er-
an d dem an d. If th ere is a sufficien t supply of oxygen an d glucose m ia h as been sh ow n to d ecrease m et abolism , decrease free radi-
or in t racellular en ergy stores to m eet th e m in im um m et abolic cal sp ecies produ ct ion , in h ibit th e release of cytoch rom e c, an d
requirem en t s of a cell du ring isch em ia, th en cells su r vive. If m in - decrease ap optosis follow ing cerebral isch em ia.11–13 Hypoth er-
im al m et abolic dem an ds can n ot be m et , th en cell death en sues m ia w as first ap plied to an eu r ysm su rger y in th e 1950s by Bot-
th rough apoptot ic or n ecrot ic m ech an ism s dep en ding on th e se- terell et al.14,15 at t h e Un iversit y of Toron to (Fig. 12.2). Sin ce th at

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12 Cerebral Protection 169
Fig. 12.2 Intraoperative hypotherm ia for re-
pair of complex intracerebral aneurysm s was
first employed at the Universit y of Toronto by
William Lougheed and E. Harry Bot terell. This
photograph depict s an early case of intraoper-
ative hypotherm ia for aneurysm repair induced
by placing the anesthetized patient in a tub
of ice and alcohol. (Photo courtesy of William
Lougheed, MD Departm ent of Neurosurgery,
Universit y of Toronto.)

t im e, hyp oth erm ia h as becom e m ore com m on an d h as been ap - provem en ts.26,27 Hu m an st u dies h ave dem on st rated a redu ct ion
plied as m ild in du ced hyp oth erm ia d u ring tem p orar y vascu lar in m etabolic dem an d du ring in t raoperat ive burst suppression .28
occlusion an d as profoun d hypoth erm ia for longer periods of Th e u se of bu rst su p p ression h as n ot been specifically add ressed
isch em ia or in conju n ct ion w ith card iac stan dst ill.16,17 Th e In t ra- for use in t ran sien t occlusion du ring n eurovascu lar procedures;
operat ive Hypoth erm ia for An eur ysm Surger y Trial (IHAST) com - h ow ever, th e con cept is w idely adopted an d can be safely un der-
pared m ild in duced hypoth erm ia (target tem perat ure of 33°C) taken . Th e agen t s discussed h ave a ten den cy to decrease blood
du ring an eu r ysm su rger y to n orm oth erm ia in 1001 p at ien t s.18 p ressu re an d m u st be u t ilized in conju n ct ion w it h ot h er tech -
Th ere w as n o differen ce bet w een th e t reat m en t grou ps in term s n iqu es to m ain t ain blood p ressu re or even elevate p ressu res
of fu n ct ion al ou tcom e score. In secon dar y ou tcom e an alysis, d u r ing periods of isch em ia.
bacterem ia w as m ore often obser ved in th e hypoth erm ia group Hypoth erm ia an d burst suppression h ave been frequen tly
(5%) th an in th e con t rol group (3%). Alth ough th is t rial did n ot com bin ed as a n eu rop rotect ive st rategy for t ran sien t brain isch -
dem on st rate im p roved ou tcom es w ith m ild hyp oth erm ia, it did em ia.29,30 Th is tech n ique h as a soun d physiological basis, an d a
dem on st rate th at m ild hyp oth erm ia in an eu r ysm su rger y is rela- ret rosp ect ive review of t h ese procedu res h as dem on st rated th e
t ively safe w it h lit t le d ow n sid e. In t raop erat ive coolin g m ay be safet y of com bin ing th e t w o; th erefore, com bin ed hyp oth erm ia
ach ieved w ith a cooling blan ket or in t ravascu lar cooling device, an d burst suppression con t in u es to be used as a n europrotect ive
or by ext racorporeal cooling.19,20 Th e ch oice of cooling m eth od adjun ct to decrease cellu lar m etabolic dem an d in t raoperat ively.
dep en ds on th e depth of hyp oth erm ia desired an d th e size of th e Th is pract ice h as n ot been direct ly tested in a clin ical t rial bu t
pat ien t . appears to be relat ively safe an d con form s w ith in t u it ive physi-
Sim ilar to the argum en t supporting hypotherm ia in aneur ysm ological prin ciples based on data derived from an im al st udies.
surger y, avoidan ce of fever in th e peri-isch em ic p eriod can im -
prove outcom e. In anim al m odels of ischem ic stroke, hypertherm ia
is associated w ith w orse fu n ct ional an d h istological ou tcom es.21
Improving Blood Supply
Fever h as been associated w ith w orse ou tcom e follow ing cere- Collateral circu lat ion in th e brain provides altern ate path w ays
bral isch em ia.22,23 for blood flow to a given region of brain . Th ere is variat ion be-
Ph arm acological m ean s of redu cing n eu ron al act ivit y du ring t w een in dividu als in th e an atom y an d exten t of collateral flow,
su rger y decreases m etabolic dem an d an d can be u sed for cere- an d th is can be est im ated preoperat ively to h elp st rategize ap -
bral protect ion . An esth et ic agen ts th at ach ieve th is in clude bar- proach es to tem p orar y or perm an en t occlu sion in n eu rosu rgical
biturates, benzodiazepines, propofol, etom idate, and inhalational procedu res. Th e circle of Willis is an exam p le of brain collateral
agents.24,25 Intraoperative electroencephalogram (EEG) is utilized flow.31 Collateral flow bet w een righ t an d left h em isph eres is p ro-
to t it rate these agen ts to ach ieve EEG isoelect ricit y (or, at m in i- vided by th e an terior com m un icat ing ar ter y, an d collateral flow
m u m , EEG bu rst su pp ression ). An im al st u dies of bu rst su p pres- from posterior to an terior circu lat ion is p rovided by t h e p aired
sion during brain ischem ia have dem onstrated reduced m etabolic posterior com m u n icat ing ar teries. In proced u res requ iring tem -
dem an d, reduced free radical accum ulat ion, im proved m em brane porar y vessel occlusion like carotid endarterectom y, the presen ce
st abilit y, d ecreased cell an d t issu e d eat h , an d fu n ct ion al im - an d size of p osterior com m u n icat ing ar ter ies an d t h e an terior

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170 II Evaluation and Treatment Considerations for Neurovascular Disease

com m u n icat ing ar ter y can p redict th e n eed for sh u n t ing du ring bellar cor tex; h ow ever, vessels su pplying subcor t ical st ruct ures
carot id occlu sion .32 In p roxim al vessel occlu sion of th e in tern al gen erally do n ot h ave robust collateral supply an d in t urn do n ot
carot id ar ter y for gian t an terior circu lat ion an eu r ysm s or ver te- tolerate tem p orar y or p erm an en t occlusion .
bral ar ter y(ies) for posterior circu lat ion gian t an eur ysm s, a pat- Based on th e aforem en t ion ed collateral an atom y, on e can pre-
en t circle of Willis is requ ired to proceed safely; th ese collateral d ict w h et h er occlu sion w ill be tolerated an d w h et h er adju n ct s
path w ays are tested u sing a tem p orar y balloon occlu sion test are requ ired to im p rove collateral flow d u r ing a n eu rovascu lar
preop erat ively.33 Collateral supply in th e m ore distal in t racran ial procedu re. For in stan ce, collateral flow in th e distal vascu lat u re
circu lat ion d ep en d s on overlap of vascu lar ter ritories an d th e perm it s lesion s in th e dist al cerebral vessels to be occlu ded or
p resen ce of leptom en ingeal collaterals. For in st an ce, occlu sion resected w ith m in im al isch em ic risk. More proxim al occlusion in
in th e proxim al m iddle cerebral ar ter y (MCA) dist ribut ion in th e th e cerebral vessels requ ires u se of p rotect ive m easu res or in ter-
M1 or M2 segm en t s is n ot gen erally tolerated for exten ded p eri- m it ten t reperfu sion . How ever, th e th eoret ical p rotect ive versu s
ods as th ere is insufficien t overlap from adjacen t an terior cere- h arm ful effect s of in term it ten t reperfusion are debated.34,35
bral ar ter y (ACA) supply an d often in sufficien t leptom en ingeal On e direct m ean s of providing collateral flow for prolonged
su pply to overcom e isch em ia in du ced in th e MCA territor y. How - tem porar y occlusion in th e proxim al cerebral vasculat ure is th e
ever, occlu ding m ore d ist ally in to t h e M3 an d M4 d ist r ibu t ion s u se of protect ive bypass (Fig. 12.3).36,37 Th is tech n ique h as m ost
of th e MCA is generally tolerated becau se th ere is overlap of vas- often been applied in th e MCA dist ribution for repair of com plex
cular su pply w ith adjacen t dist al MCA territories. Th is prin ciple proxim al MCA an eu r ysm s w h ere a tem p orar y byp ass irrigates
applies to th e in t racran ial vessels su pplying cerebral an d cere- th e dist al MCA territor y du ring p roxim al tem porar y occlu sion

a b

d f

Fig. 12.3a–f Case illustration of protective bypass utilized


in the repair of a giant cavernous carotid artery aneurysm .
(a–c) The aneurysm was discovered after the patient pre-
sented with ophthalm oplegia. The aneurysm was deem ed
e ineligible for endovascular treatm ent or direct open m icro-
surgical clipping. Therefore, the patient underwent an external
carotid to m iddle cerebral artery bypass to facilitate trapping
of the aneurysm . (d) Internal carotid bifurcation dem onstrat-
ing the m iddle cerebral artery, anterior cerebral artery, and
distal aneurysm al dilatation of the carotid artery. (e) Anasto-
m osis of the distal saphenous vein graft into the M1 segm ent
using the excim er laser-assisted nonocclusive anastom osis
technique. The aneurysm was ultim ately trapped with the
m iddle cerebral and anterior cerebral arteries supplied by the
external carotid saphenous vein graft. (f) Computed tom og-
raphy angiogram of the final result.

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12 Cerebral Protection 171

an d an eu r ysm repair. Th e flow requirem en t s of th e distal vascu- resu lt s in an in crease in free radical produ ct ion over con t rols an d
lar territor y can be est im ated by m easu ring p reoperat ive flow in w orsen ed ou tcom e in roden t m odels of focal cerebral isch em ia.50
th e p roxim al vessel w ith n on invasive tech n iqu es su ch as n on in - After sh or t t ran sien t isch em ia, n eu ron al fu n ct ion is m ore se-
vasive optim al vessel analysis m agnetic resonance im aging (NOVA verely im paired and takes longer to recover in hyperglycem ic rats.51
MRI).38 Th is flow sets a target to m atch in t raoperat ively using Th is effect w as at t ribu ted to local t issu e acidosis as opp osed to
eith er a su perficial tem poral ar ter y graft for low flow s or long im pairm en t of ion ic ch an n els. Clin ically, elevated serum glucose
vein graft for h igh flow s. In t raop erat ive flow s can be m easu red on ad m ission for acu te isch em ic st roke cou n teract s t h e ben efi-
using the cu t-flow in dex to d eterm in e w h eth er a graft w ill be cial effect s of t h rom bolysis an d is associated w it h d ecreased
su fficien t to replace flow du ring tem porar y occlu sion .39 Prior to salvage of p en u m bral t issu e, larger lesion volu m e, an d w orse
tem porar y clipping, th e bypass is sew n in to place an d flow to th e outcom e.52,53 Maintenance of perioperative norm oglycem ia prior
distal vasculat ure is confirm ed at the tim e of tem porary occlusion . to tem porar y isch em ia likely im proves cellular toleran ce to isch -
Th e an eu r ysm is th en recon st ru cted u n der tem p orar y occlu sion em ic dam age, alth ough th is h as n ot been sp ecifically addressed
w ith p rotect ion . Th e byp ass is gen erally occlu ded on ce proxim al in th e clin ical literat ure.
flow is reestablish ed. In cases w h ere com plex an eur ysm s can n ot Several p h ar m acological agen t s to red u ce secon dar y inju r y
be recon st r u cted, th e byp ass can be left in place if th e an eu r ysm follow ing ischem ia h ave been evaluated in h um an clin ical t rials
requ ires t rapping. of acute isch em ic st roke. Neurotoxicit y in duced by act ivat ion of
In duced hyper ten sion is an oth er m ean s of in ducing collateral NMDA receptors h as been th e m ost frequ en tly t argeted m ech a-
su p ply du ring n eu rovascu lar p rocedu res. Mild elevat ion of m ean nism of secondary injury targeted.54 NMDA antagonists have been
ar terial pressure h as been dem on st rated to im prove brain oxy- develop ed to p reven t n eu rotoxicit y in du ced by cellu lar calciu m
gen at ion an d blood flow in an im al m odels.38,40 Th is effect is m ost in flu x an d NOS act ivat ion by t h e receptor. Th ese agen t s h ave
likely related to an in crease in leptom en ingeal an d pial collateral in clu ded dr ugs like selfotel, apt igan el, elip rodil, licost in el, gaves-
flow .41 In d u ced hyp er ten sion h as been invest igated as a t reat - t in el, an d ketam in e, am ong oth ers, an d h ave u n iversally failed
m en t for acute isch em ic st roke in an im als an d h u m an s. An im al clin ical t r ials of acu te isch em ic st roke.55 Th ese agen t s h ave n ot
studies have produced prom ising results 40 ; h ow ever, th ere is on ly been sp ecifically assessed for efficacy in tem p orar y isch em ia
an ecdotal eviden ce th at hyper ten sion m ay im prove st roke ou t- associated w ith n eurovascular surger y an d are n ot u t ilized in
com e in h u m an s, as n o large-scale h u m an t rial of in d u ced hyp er- practice due to hypotension, psychom im etic effects, and other del-
ten sion h as been perform ed.42 As an adjun ct to n eurovascu lar eterious side effect s of th is drug class. To overcom e th ese issues
procedu res involving tem p orar y clip p ing of dist al vessels, th ere w ith NMDA an tagon ists, dow n st ream t arget s in th e glutam ate
is obser vat ion al an d an ecdot al eviden ce of im proved collateral n eu rotoxicit y cascade h ave been t argeted. Postsyn apt ic den sit y
flow w ith induced hypertension. This evidence includes im prove- protein 95 (PSD-95) is a m em bran e bou n d p rotein th at cou p les
m en t s in blood flow, evoked poten t ials, an d elect roen ceph alo- th e act ivat ion of NMDA to NOS an d in it iates th e n eu rotoxic ef-
gram after induction of hypertension and elevated retrograde flow fect s of NOS act ivat ion in glu t am ate-in du ced n eu rotoxicit y.7 A
from sm all collateral vessels in th e d ist al MCA dist ribu t ion du r- sp ecific in h ibitor of PSD-95, Tat -NR2B9c, h as been d evelop ed
ing tem porar y occlu sion an d arteriotom y of M4 bran ch es du ring th at p reven t s NOS act ivat ion by NMDA an d im p roves n eu rologic
byp ass p rocedures.43 outcom e in m u lt iple roden t an d n on h um an prim ate m odels of
Sym ptom at ic vasospasm follow ing su barach n oid h em orrh age st roke.56,57 Th is th erapy is being evalu ated in a clin ical t rial of
is often at t ribu ted to im p aired flow th rough severely sten osed drug efficacy in p reven t ing st rokes follow ing en dovascu lar re-
in t racran ial vessels.44 To overcom e im p aired flow an d im p rove pair of brain an eu r ysm s.58 Th is t rial represen ts th e first use of a
d ist al p er fu sion t h rough bot h d irect an d collateral p at h w ays, n eu roprotectan t for th e preven t ion of n eurovascular procedure–
in t ra-arterial calciu m ch an n el blocker in fusion s an d angiop last y related stroke. The use of a neuroprotectant in neurovascular pro-
h ave been em ployed to open proxim al vessels. Th ese tech n iques cedu res is an appealing opt ion an d sh ou ld be fu rth er evalu ated
h ave p roven effect ive in im p roving bot h t h e clin ical exam an d w ith oth er prom ising agents in th e fu t u re.
blood flow on perfu sion im aging.45,46 Magn esiu m h as a n eu rop rotect ive effect in an im al m odels of
Im p roving blood rh eology an d oxygen -car r ying cap acit y en - acute isch em ic st roke.59 Magn esiu m in h ibit s glu t am ate excito-
su res opt im al su p p ly to t h e brain d u r ing t im es of isch em ia. Th e toxicit y by en ter in g an d blocking t h e p ore of t h e NMDA recep -
h em atocrit sh ould be m ain t ain ed in th e n orm al range as an em ia tor ch an n el.60,61 In fu sion of m agn esiu m su lfate follow in g acu te
an d elevated h em atocrit are both associated w ith poor ou tcom e isch em ic st roke did n ot ach ieve clin ical efficacy in early clin ical
in acu te isch em ic st roke.47,48 To m axim ize oxygen deliver y, hy- t rials 62 ; h ow ever, th e early adm in ist rat ion of m agn esium in th e
poxia m ust be avoided. Sim ilarly, hypoglycem ia m ust be avoided p reh osp it al set t ing is bein g evalu ated for st roke.63 In t raop era-
in acu te isch em ic st roke as it is associated w ith poor n eu rologic t ive m agn esiu m su lfate in fu sion for tem p orar y occlusion du ring
outcom e; h ow ever, th is m ust be balan ced again st th e n eed to an eu r ysm su rger y h as been st u died in a prelim in ar y fash ion .64
avoid hyperglycem ia.49 Magn esiu m in fu sion im p roved brain oxygen at ion d u r in g t h e
p eriod of isch em ia an d in creased th e rate of brain oxygen at ion
recover y follow ing rep erfu sion . Fur th er st udies are required to
Improving Cellular Tolerance to Ischemia validate th is th erapy for n europrotect ion du ring n eurovascular
Meth ods to im prove th e toleran ce of isch em ic cells to th e m any procedu res.
n eu rotoxic cascades in it iated after isch em ia h ave been evaluated Oth er m ech an ism s of n eurotoxicit y follow ing isch em ia h ave
in n u m erous an im al m odels an d h um an clin ical t rials. For in - been targeted ph arm acologically in acute isch em ic st roke w ith -
st an ce, elevated seru m glu cose at th e t im e of cerebral isch em ia ou t clin ical efficacy.65 Th ese m ech an ism s m ay be of in terest in

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172 II Evaluation and Treatment Considerations for Neurovascular Disease

cerebral protect ion for n eurovascular procedures but h ave n ot ■ Conclusion


been specifically proposed for this indication. These therapies are
too n um erous for review in th is ch apter, but th ey can be briefly Cerebral protect ion for n eu rovascu lar proced u res in clu des in ter-
sum m arized. In addition to NMDA an tagonists, AMPA and m eta- ven t ion s th at poten t ially span th e en t ire perioperat ive period.
bot ropic glu tam ate receptor an tagon ism h as been proposed to For in stan ce, diabet ic pat ien ts m u st be closely m on itored in th e
lim it excitotoxicit y follow ing isch em ia. Calciu m ch an n el block- preop erat ive clin ic an d m ay requ ire addit ion al in ter ven t ion to
ers an d calciu m ch elators h ave been p rop osed to redu ce ext ra- correct hyp erglycem ia in th e p eriop erat ive period. Su rgeon s an d
cellular calciu m con cen t rat ion an d to redu ce calcium in flu x an d an est h esiologist s m ay ch oose to st ar t p at ien t s on st at in agen t s
excitotoxicit y. An t ioxidan t agen t s an d radical t rap ping agen ts in th e p reop erat ive p er iod , esp ecially p at ien t s w it h dyslip id -
in ten ded to n eut ralize accu m ulat ing free radicals h ave been pro- em ia. In t raoperat ive cerebral p rotect ion can be t ailored to su it
posed to p reven t secon dar y dam age related to react ive oxygen in dividu al cases or be delivered as a p rotocol con sisten tly in all
species after stroke. Anti-inflam m ator y drugs have been proposed n eu rovascu lar cases. It is difficu lt to gen eralize a protocol for ce-
to reduce secon dar y injur y related to in flam m at ion follow ing rebral protection, as individual preferences and experiences shape
st roke. St at in s h ave been sh ow n to h ave an t i-in flam m ator y an d w h at is don e in a given in st it ut ion . Th e protocol for cerebral pro-
n eu roprotect ive effects, an d pat ien t s pret reated on st at in s prior tect ion for n eurovascu lar procedures m ay in clude in du ced hypo-
to an isch em ic st roke h ave been sh ow n to h ave im proved out- th erm ia, bu rst su pp ression , in du ced hyp er ten sion , an d opt im al
com es, suggesting that statin pretreatm ent m ay be of benefit prior blood sugar control. There are lim ited clinical data to support any
to neurovascular procedures. Finally, γ-am in obut yric acid an d se- on e in ter ven t ion m ore th an an oth er. In gen eral, th ese in ter ven -
roton in agon ist s h ave been p rop osed to red uce n euron al m etab - tion s are safe, w ell tolerated, an d m ay be applied in com bination.
olism an d prolong n euron al toleran ce to isch em ia. Ph ar m acological cerebral p rotect an t s for n eu rovascu lar p ro -
In subarach n oid h em orrh age-related vasospasm , th e L-t ype ced u res are being invest igated . Any op p or t u n it y to im p rove
calciu m ch an n el blocker n im od ipin e h as been u sed as a cerebral p at ien t ou tcom e is of great im port an ce; h ow ever, t h e discover y
protectan t to p reven t delayed n eu rologic deficit s.66,67 Th e m ech - of a n eu roprotect an t th at cou ld be delivered before or du ring
an ism of act ion of n im odipin e is n ot specifically kn ow n but m ay n eu rovascular procedu res w ould revolut ion ize specific open an d
be related to vascular dilat ion , in t rin sic n europrotect ive effect s en d ovascu lar procedu res w h ere th e risk of p rolonged tem porar y
related to calciu m ch an n el an t agon ism , or im p rovem en t of blood occlusion h as been too risky to at tem pt .
rh eology.44,68

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spect ive an d th erapeu t ic im plicat ion s. Cerebrovasc Dis 2001;11(Su ppl 1): m an nitol for brain relaxat ion du ring elect ive supraten torial brain t um or
2–8 surger y. An esth An alg 2010;110:903–907
2. Ast r up J, Siesjö BK, Sym on L. Th resh olds in cerebral ischem ia—th e isch - 13. Tom m asin o C. Fluids an d th e n eurosurgical pat ient . An esth esiol Clin
em ic pen um bra. St roke 1981;12:723–725 North Am erica 2002;20:329–346, vi vi
3. Lee DH, Kang DW, Ah n JS, Ch oi CG, Kim SJ, Suh DC. Im aging of th e isch - 14. Bot terell EH, Lough eed W M, Scot t JW, Van dew ater SL. Hypoth erm ia, an d
em ic pen u m bra in acute st roke. Korean J Radiol 2005;6:64–74 in terru pt ion of carot id, or carot id an d ver tebral circulat ion , in th e surgical
4. Ito U, Spat z M, Walker JT Jr, Klat zo I. Experim en tal cerebral isch em ia in m anagem ent of intracranial aneurysm s. J Neurosurg 1956;13:1–42
m ongolian gerbils. I. Light m icroscopic obser vat ion s. Act a Neuropathol 15. Bot terell EH, Lough eed W M, Morley TP, Van dew ater SL. Hyp oth erm ia in
1975;32:209–223 th e surgical t reat m en t of r upt u red in t racran ial an eur ysm s. J Neu rosurg
5. Pu lsin elli WA, Brierley JB, Plu m F. Tem p oral p rofile of n eu ron al dam age 1958;15:4–18
in a m od el of t ran sien t forebrain isch em ia. An n Neu rol 1982;11:491– 16. Bell TE, Kongable GL, Stein berg GK. Mild hypoth erm ia: an altern at ive to
498 deep hyp oth erm ia for ach ieving n eu roprotect ion . J Card iovasc Nu rs 1998;
6. Kirin o T. Delayed n euron al death in th e gerbil h ippocam pus follow ing 13:34–44
isch em ia. Brain Res 1982;239:57–69 17. Sp et zler RF, Had ley MN, Rigam on t i D, et al. An eu r ysm s of th e basilar ar-
7. Sat tler R, Xiong Z, Lu W Y, Hafn er M, MacDon ald JF, Tym ian ski M. Specific ter y treated w ith circulator y arrest , hypotherm ia, and barbiturate cerebral
coupling of NMDA receptor act ivat ion to n it ric oxide n eurotoxicit y by protect ion . J Neu rosu rg 1988;68:868–879
PSD-95 protein . Scien ce 1999;284:1845–1848 18. Todd MM, Hin dm an BJ, Clarke W R, Torn er JC; In t raoperat ive Hyp oth erm ia
8. Sat tler R, Xiong Z, Lu W Y, MacDon ald JF, Tym ian ski M. Dist in ct roles of for An eur ysm Surger y Trial (IHAST) Invest igators. Mild in t raoperat ive hy-
syn apt ic and ext rasyn apt ic NMDA receptors in excitotoxicit y. J Neurosci poth erm ia du ring su rger y for in t racran ial an eu r ysm . N Engl J Med 2005;
2000;20:22–33 352:135–145
9. Porasuph at an a S, Tsai P, Rosen GM. Th e gen erat ion of free radicals by n i- 19. Stein berg GK, Ogilvy CS, Sh u er LM, et al. Com p arison of en dovascu lar an d
t ric oxide syn th ase. Com p Biochem Physiol C Toxicol Ph arm acol 2003;134: su rface cooling du ring un ru pt u red cerebral an eur ysm repair. Neurosur-
281–289 ger y 2004;55:307–314, discussion 314–315
10. Adibh atla RM, Hatch er JF, Dem psey RJ. Ph osph olipase A2, hydroxyl radi- 20. Tsu ei BJ, Kearn ey PA. Hyp oth erm ia in th e t rau m a p at ien t . Inju r y 2004;35:
cals, an d lipid peroxidat ion in t ran sien t cerebral ischem ia. An t ioxid Redox 7–15
Sign al 2003;5:647–654 21. Kim Y, Bu sto R, Diet rich W D, Kraydieh S, Gin sberg MD. Delayed p ost isch -
11. Rozet I, Ton t isirin N, Muangm an S, et al. Effect of equiosm olar solut ion s of em ic hyperth erm ia in aw ake rat s w orsen s th e h istopathological outcom e
m an nitol versus hyper ton ic salin e on in t raoperat ive brain relaxat ion and of t ran sien t focal cerebral ischem ia. St roke 1996;27:2274–2280, discus-
elect rolyte balan ce. An esth esiology 2007;107:697–704 sion 2281

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22. Azzim on di G, Bassein L, Non in o F, et al. Fever in acute st roke w orsen s m easured by laser Doppler im aging. Neurosurger y 1998;42:617–624,
progn osis. A prospect ive st udy. St roke 1995;26:2040–2043 discu ssion 624–625
23. War ten berg KE, Sch m idt JM, Claassen J, et al. Im pact of m edical com plica- 44. Weyer GW, Nolan CP, Macdon ald RL. Eviden ce-based cerebral vasospasm
t ion s on outcom e after subarach n oid h em orrh age. Crit Care Med 2006; m an agem en t . Neurosurg Focus 2006;21:E8
34:617–623, quiz 624 45. Kassell NF, Helm G, Sim m on s N, Ph illips CD, Cail WS. Treat m en t of cere-
24. Baugh m an VL. Brain protect ion during n eurosurger y. An esth esiol Clin bral vasospasm w ith in t ra-ar terial papaverin e. J Neurosu rg 1992;77:848–
North Am erica 2002;20:315–327, vi vi 852
25. Hoff JT, Pit t s LH, Spet zler R, Wilson CB. Barbit urates for protect ion from 46. New ell DW, Eskridge JM, Mayberg MR, Grady MS, Win n HR. Angioplast y
cerebral isch em ia in an eur ysm su rger y. Act a Neurol Scan d Su ppl 1977; for th e t reat m ent of sym ptom at ic vasospasm follow ing subarach n oid
64:158–159 h em orrh age. J Neurosurg 1989;71(5 Pt 1):654–660
26. Majew ska MD, St roszn ajder J, Lazarew icz J. Effect of isch em ic an oxia an d 47. Allpor t LE, Parson s MW, Butch er KS, et al. Elevated h em atocrit is associ-
barbit u rate an esth esia on free radical oxidat ion of m itoch on drial ph os- ated w ith redu ced rep erfu sion an d t issu e su r vival in acu te st roke. Neu rol-
ph olip ids. Brain Res 1978;158:423–434 ogy 2005;65:1382–1387
27. Kaw aguchi M, Furuya H, Patel PM. Neuroprotect ive effect s of an esthet ic 48. Tan n e D, Molsh at zki N, Merzeliak O, Tsabari R, Toashi M, Sch w am m en thal
agen t s. J An esth 2005;19:150–156 Y. Anem ia st at us, h em oglobin con cent rat ion an d outcom e after acute
28. Doyle PW, Mat t a BF. Bu rst suppression or isoelect ric en ceph alogram for st roke: a coh or t st udy. BMC Neurol 2010;10:22
cerebral protect ion : eviden ce from m et abolic suppression st udies. Br J 49. Br un o A, Levin e SR, Fran kel MR, et al; NINDS r t-PA St roke St udy Group.
An aesth 1999;83:580–584 Adm ission glucose level and clin ical outcom es in th e NINDS rt-PA St roke
29. Zausinger S, Westerm aier T, Plesn ila N, Steiger HJ, Sch m id-Elsaesser R. Trial. Neu rology 2002;59:669–674
Neuroprotect ion in t ran sien t focal cerebral isch em ia by com bin at ion drug 50. Li PA, Liu GJ, He QP, Floyd RA, Siesjö BK. Product ion of hydroxyl free radi-
th erapy an d m ild hyp oth erm ia: com parison w ith cu stom ar y th erapeu t ic cal by brain t issu es in hyperglycem ic rat s subjected to t ran sien t forebrain
regim en . St roke 2003;34:1526–1532 isch em ia. Free Radic Biol Med 1999;27:1033–1040
30. Ston e JG, Young W L, Maran s ZS, et al. Con sequen ces of elect roenceph alo- 51. Siem kow icz E, Han sen AJ. Brain ext racellular ion com posit ion an d EEG
grap h ic-su p pressive doses of propofol in conju n ct ion w ith deep hypo- act ivit y follow ing 10 m in u tes isch em ia in n orm o- an d hyp erglycem ic
th erm ic circu lator y arrest . An esth esiology 1996;85:497–501 rat s. St roke 1981;12:236–240
31. Alpers BJ, Berr y RG, Paddison RM. An atom ical st udies of th e circle of Wil- 52. Alvarez-Sabín J, Molin a CA, Mon t an er J, et al. Effect s of adm ission hyper-
lis in norm al brain. AMA Arch Neurol Psychiatry 1959;81:409–418 glycem ia on st roke outcom e in reperfused t issue plasm in ogen act ivator–
32. Lopez-Bresnah an MV, Kearse LA Jr, Yan ez P, Young TI. An terior com m un i- t reated pat ien t s. St roke 2003;34:1235–1241
cat ing arter y collateral flow protect ion again st isch em ic change du ring 53. Parson s MW, Barber PA, Desm on d PM, et al. Acute hyperglycem ia ad-
carot id en dar terectom y. J Neurosu rg 1993;79:379–382 versely affect s st roke ou tcom e: a m agn et ic reson an ce im aging an d sp ec-
33. van Rooij W J, Sluzew ski M, Met z NH, et al. Carot id balloon occlusion for t roscopy st udy. An n Neurol 2002;52:20–28
large an d giant an eur ysm s: evaluat ion of a n ew test occlu sion protocol. 54. Hoyte L, Barber PA, Buch an AM, Hill MD. Th e rise an d fall of NMDA an -
Neurosu rger y 2000;47:116–121, discussion 122 t agon ist s for isch em ic st roke. Curr Mol Med 2004;4:131–136
34. David CA, Prado R, Diet rich W D. Cerebral protect ion by in term it ten t re- 55. Ikon om idou C, Tu rski L. W hy did NMDA receptor an t agon ist s fail clin ical
perfu sion d u ring tem p orar y focal isch em ia in th e rat . J Neu rosu rg 1996; t rials for st roke an d t raum at ic brain injur y? Lan cet Neurol 2002;1:383–
85:923–928 386
35. Stein berg GK, Pan ah ian N, Sun GH, Maier CM, Kun is D. Cerebral dam age 56. Aart s M, Liu Y, Liu L, et al. Treat m ent of isch em ic brain dam age by per-
caused by interrupted, repeated arterial occlu sion versus un in terrupted t urbing NMDA receptor–PSD-95 protein in teract ion s. Scien ce 2002;298:
occlusion in a focal ischem ic m odel. J Neurosurg 1994;81:554–559 846–850
36. van Doorm aal TP, van der Zw an A, Ver w eij BH, Regli L, Tulleken CA. Gian t 57. Cook DJ, Teves L, Tym ian ski M. Treat m en t of st roke w ith a PSD-95 in h ibi-
an eu r ysm clip p ing u n d er p rotect ion of an excim er laser-assisted n on - tor in the gyrencephalic prim ate brain. Nature 2012;483:213–217
occlusive an astom osis bypass. Neurosu rger y 2010;66:439–447, discus- 58. Hill MD, Mar t in RH, Miku lis D, et al; ENACT t rial invest igators. Safet y an d
sion 447 efficacy of NA-1 in pat ien t s w ith iat rogen ic st roke after endovascular an -
37. Hongo K, Horiuchi T, Nit t a J, Tan aka Y, Tada T, Kobayash i S. Double-insu r- eur ysm repair (ENACT): a ph ase 2, ran dom ised, double-blin d, placebo-
an ce bypass for in ternal carot id ar ter y an eur ysm surger y. Neurosurger y con t rolled t rial. Lan cet Neurol 2012;11:942–950
2003;52:597–602, discussion 600–602 59. Miles AN, Majda BT, Melon i BP, Kn u ckey NW. Post isch em ic in t raven ou s
38. Ash ley W W, Am in -Hanjani S, Alaraj A, Sh in JH, Ch arbel FT. Flow -assisted adm in ist rat ion of m agn esiu m sulfate in h ibit s h ippocam pal CA1 n euron al
surgical cerebral revascularization. Neurosurg Focus 2008;24:E20 death after t ran sient global isch em ia in rat s. Neurosurger y 2001;49:1443–
39. Am in -Hanjan i S, Du X, Mlin arevich N, Meglio G, Zh ao M, Ch arbel FT. Th e 1450, discu ssion 1450–1451
cut flow in dex: an int raoperat ive predictor of th e success of ext racran ial- 60. Hallak M, Ber m an RF, Ir ten kau f SM, Jan u sz CA, Cot ton DB. Magn e-
in t racran ial bypass for occlusive cerebrovascu lar disease. Neurosu rger y siu m su lfate t reat m en t decreases N-m ethyl-D-aspar t ate receptor bin d ing
2005;56(1, Suppl):75–85, discussion 75–85 in th e rat brain : an au toradiograph ic st udy. J Soc Gyn ecol Invest ig 1994;1:
40. Hayash i S, Neh ls DG, Kieck CF, Vielm a J, DeGirolam i U, Crow ell RM. Ben - 25–30
eficial effect s of in d u ced hyp er ten sion on exp er im en t al st roke in aw ake 61. Ch ah al H, D’Souza SW, Barson AJ, Slater P. Modu lat ion by m agn esium of
m on keys. J Neurosurg 1984;60:151–157 N-m ethyl-D-aspart ate receptors in developing h um an brain . Arch Dis
41. MacKen zie ET, St ran dgaard S, Grah am DI, Jon es JV, Harper AM, Farrar JK. Ch ild Fet al Neon at al Ed 1998;78:F116–F120
Effect s of acutely in duced hyper ten sion in cat s on pial arteriolar caliber, 62. Muir KW, Lees KR, Ford I, Davis S; In t raven ous Magn esium Efficacy in
local cerebral blood flow, an d th e blood-brain barrier. Circ Res 1976; St roke (IMAGES) St udy Invest igators. Magn esium for acu te st roke (In t ra-
39:33–41 ven ous Magn esium Efficacy in St roke t rial): ran dom ised cont rolled t rial.
42. Wit yk RJ. Blood pressure augm en t at ion in acute isch em ic st roke. J Neu rol Lan cet 2004;363:439–445
Sci 2007;261:63–73 63. Saver JL, Kidw ell C, Eckstein M, St arkm an S; FAST-MAG Pilot Tr ial Inves-
43. Sm rcka M, Ogilvy CS, Crow RJ, Mayn ard KI, Kaw am at a T, Am es A III. In - t igators. Preh ospit al n eu rop rotect ive th erapy for acu te st roke: resu lt s of
du ced hyper ten sion im proves region al blood flow an d p rotect s again st th e Field Ad m in ist rat ion of St roke Th erapy-Magn esiu m (FAST-MAG) pilot
in farct ion during focal isch em ia: t im e cou rse of ch anges in blood flow t rial. St roke 2004;35:e106–e108

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64. Ch an MT, Boet R, Ng SC, Poon WS, Gin T. Magn esium sulfate for brain pro- 67. Barker FG II, Ogilvy CS. Efficacy of prophylact ic nim odipin e for delayed
tect ion during tem porar y cerebral arter y occlu sion . Act a Neuroch ir Suppl isch em ic deficit after subarach n oid h em orrhage: a m et aan alysis. J Neu ro-
(Wien ) 2005;95:107–111 surg 1996;84:405–414
65. Sh u aib A, Hu ssain MS. Th e p ast an d fu t u re of n eu rop rotect ion in cerebral 68. Macdon ald RL, Plu t a RM, Zh ang JH. Cerebral vasospasm after su barach -
isch aem ic st roke. Eur Neurol 2008;59:4–14 n oid hem orrh age: th e em erging revolut ion . Nat Clin Pract Neurol 2007;
66. Kassell NF, Sasaki T, Coloh an AR, Nazar G. Cerebral vasospasm follow ing 3:256–263
an eur ysm al subarach n oid h em orrh age. St roke 1985;16:562–572

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13 Principles and Techniques of
Hypothermia and Cardiac Arrest
for Neurovascular Anomalies
Javier Lorenzo and Richard A. Jaffe

Th e obser vat ion th at hyp oth erm ia can posit ively affect ou tcom es flow to th e periph er y; in con t rast , vasocon st rict ion keeps m et a-
is as old as m odern m ed icin e. Hip pocrates, con sidered th e first bolic h eat in th e core, in creasing th e core-to-periph eral tem per-
m odern doctor, advocated packing w ounded soldiers in snow and at u re gradien t . Metabolism is th e on ly in tern al sou rce of h eat in
ice.1 A Fren ch su rgeon in Napoleon’s arm y ast u tely n oted th at body t issu es, an d h eat p rod u ct ion is p rop or t ion al to m et abolic
in fan t r ym en kept aw ay from t h e fire h ad bet ter su r vival rates rate. Th e breakd ow n of p rotein an d glu cose can yield as m u ch
t h an t h ose w h o w ere w ar m .1 In t h e 1950s, an est h esiologist s as 9.3 kcal/kg an d 4.1 kcal/kg, respect ively. Th e brain an d m ajor
used hypoth erm ia at 25°C to protect th e brain from isch em ia organ s in th e t run k are th e m ost m etabolically act ive t issues an d
during cerebral an eu r ysm su rger y.2 Both cardioth oracic su r- th e prim ar y h eat gen erators at rest .
geon s an d n eu rosu rgeon s hypoth esized th e poten t ial ben efits of W it h ou t fail, m ost p at ien t s u n d ergoin g gen eral an est h esia
in t raoperat ive hypoth erm ia.3,4 At first , th ey cooled pat ien ts to becom e hypoth erm ic by 1° to 3°C. Factors su ch as am bien t tem -
deep tem p erat u res bu t fou n d th at th e cooling w as accom pan ied perat u re, su rgical exp osu re, an d t ype of an esth esia can affect th e
by com plicat ion s in clu ding cardiac arrest , arrhyth m ias, an d h igh degree of h eat loss. Th e in du ct ion of an esth esia cau ses direct
in fect ion rates. Th e pract ice soon fell from favor. It w as n ot un t il periph eral vasodilat ion , w h ich allow s core h eat to flow dow n th e
1987, w h en invest igators dem on st rated th at reducing core tem - tem perat ure gradien t to th e periph eral t issues. Th is in tern al re-
p erat u re by on ly 1° to 2°C sign ifican t ly p rotected rat brain s dist ribu t ion of h eat low ers th e core body tem perat u re an d in -
again st exp erim en tal st roke,5 th at in terest in th e u se of hypo- creases the peripheral com partm ent tem perature w ith a constant
th erm ia revived. n et h eat loss to th e environ m en t .
In 2002, t wo sim ultaneously publish ed landm ark hum an st ud- Heat loss to th e environ m en t occu rs by radiat ion , con du ct ion ,
ies, on e con ducted in Eu rope an d th e oth er in Au st ralia, dem on - convect ion , an d evap orat ion . At rest an d u n der n orm al con di-
st rated th e ben eficial effect s of m ild hyp oth erm ia app lied after t ion s, 50 to 70% of h eat loss in an aw ake p at ien t occu rs th rough
cardiac arrest .6 Sin ce th en , th e use of t argeted tem perat ure m an - radiat ion .8 No direct con tact w ith th e pat ien t is requ ired, an d
agem en t to m oderately redu ce core tem perat u re h as exp an ded, th ere is n o h eat t ran sfer m ediu m . Heat loss du e to radiat ion does
an d cooling th erapy con t in ues to be explored. Th is ch apter re- n ot depen d on th e tem perat ure of th e in ter ven ing air bet w een
view s th e physiology an d p hysics of th erapeu t ic hypoth erm ia, objects.
p rop osed m ech an ism s by w h ich hyp ot h er m ia ach ieves n eu ro- W hen a cool surface is applied to a patient’s skin, heat is trans-
an d cardioprotect ion , uses an d tech n iqu es of hypoth erm ia, an d fer red t h rough con d u ct ion . If a p at ien t is st an d ing, con d u ct ion
its side effect s. is n egligible; if a pat ien t is lying on a poorly in sulated surface,
con d u ct ion can be sign ifican t . We review cooling m eth ods in
w h ich clin ician s purposely keep a h igh tem perat ure gradien t be-
t w een th e pat ien t’s skin an d th e cooling su rfaces on w h ich th e
■ Physiology and Physics of pat ien t lies.
Convection describes th erm al en ergy t ran sferred by m olecu-
Therapeutic Hypothermia lar m ovem en t w ith in a flu id or gas. Th e diffu sion of convect ive
In today’s operat ing room , hypoth erm ia is used to reduce isch - h eat occu rs prim arily th rough th e ran dom Brow n ian m ot ion of
em ic brain an d cardiac injur y. To u n derstan d h ow hypoth erm ia in dividu al part icles in th e m edium . Du ring in du ct ion of hypo-
is ach ieved requ ires review ing som e h u m an p hysiology an d th erm ia, for exam p le, a fan blow ing air on to a p at ien t can drive
t h e p hysics of t h er m al t ran sfer an d h eat p rod u ct ion , as w ell as convect ive h eat loss. Convect ion rem ain s th e secon d m ost im -
t h e su bst an t ial t h er m al p er t u rbat ion s t h at occu r d u r in g gen - por t an t source for h eat loss during an esth esia an d surger y.
eral an est h esia. Evap orat ion is th e t ran sfer of h eat from a liqu id to a gas p h ase.
In h um an s, h om eost at ic m ech an ism s regulate core com par t- Evap orat ion is a cooling process. On ce th e m olecu les in th e liqu id
m ent tem perature w ithin a set, lim ited tem perature range (36.60° m ediu m at t ain en ough en ergy, th ey escap e th e liquid in to th e
± 0.38°C). Th e core com p ar t m en t con sists of th e t r un k an d h ead, gas ph ase, taking th at en ergy (h eat) w ith th em . As th is process
exclu ding th e skin , an d accou n t s for 50 to 60% of th e body’s con t in u es th e liqu id left beh in d h as less th erm al en ergy (cooler
m ass.7 Th e p erip h eral com p ar t m en t con sist s of th e skin an d ex- tem perat ure). Clin ically, convect ion an d evaporat ion can be
t rem it ies. Its low er tem p erat u res are less st rictly regu lated th an com bin ed to speed th e in duct ion of hypoth erm ia. A skin su rface
th ose of th e core. Vasocon st rict ion an d vasodilat ion m ain t ain w et w ith a liquid m edium (w ater/alcoh ol) cools upon th e evapo-
n orm oth erm ia by sh un t ing blood bet w een th ese t w o com par t- rat ion of th e liqu id, bu t th e skin cools even faster if a fan blow s
m en t s. Th erm oregulator y vasodilat ion allow s m et abolic h eat to air over th e w et skin .

175

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176 II Evaluation and Treatment Considerations for Neurovascular Disease

hypoth erm ia. Redu ced CMRO2 slow ed th e dep let ion of ATP in an
■ Cellular Ischemic Injury isch em ic hypoth erm ic brain .18 Oth ers recogn ized th at m ech a-
and Hypothermia n ism s besides CMRO2 redu ct ion w ere involved w ith th e p rotec-
After an isch em ic insult (cardiac arrest, stroke, or tem porary arte- t ive m ech an ism of th erapeut ic hyp oth erm ia.19,20
rial occlusion), blood flow is decreased, and less oxygen is avail- In th e 1980s an d 1990s, several research ers sh ow ed th at m ild
able for energy production at the cellular level. Decreased oxygen hypoth erm ia reduced brain injur y in rat m odels of global an d
even tually depletes aden osin e triph osphate (ATP) levels and leads focal isch em ia.5,21 Th ese st udies ren ew ed in terest in m ild hypo-
to accu m u lat ion of in organ ic p h osp h ate, lact ate, an d H +. In t h e th erm ia, especially as th e tem perat ure range (33° to 34°C) could
brain , th ese con dit ion s cause an oxic depolarizat ion an d th e re- be readily ach ieved in th e operat ing room . Cerebral an eur ysm
lease of glu tam ate from th e in t racellu lar com par t m en t to th e su rger y is p erfectly su ited for th erap eu t ic hyp oth erm ia becau se
ext racellu lar sp ace. Glu t am ate part ially st im u lates N-m ethyl-D- t h ere is su fficien t t im e to in d u ce hyp ot h er m ia before clip p in g
aspar t ate (NMDA) receptors an d in creases in t racellular calcium ,8 th e an eu r ysm an d for safely rew arm ing th e p at ien t du ring clo-
w h ich in t u rn leads to m em bran e dest abilizat ion an d m itoch on - sure of th e cran iotom y.
d r ial dysfu n ct ion . Th e cells exp osed to isch em ia m ay becom e Because th e isch em ic inju r y is predict able, hypoth erm ia can
n ecrot ic or apoptot ic, or th ey m ay recover if t im ely reperfusion is com m en ce before th e isch em ia an d th ereby th eoret ically m in i-
est ablish ed . Even w ith rep erfu sion , fu r th er inju r y can st ill occu r. m ize dam aging processes. An eu r ysm al r u pt u re an d th e u se of
Th e accu m u lat ion of react ive oxygen sp ecies can cau se peroxida- tem porar y clipping m ay presen t substan t ial risks for focal isch -
t ion of lipid s, p rotein s, an d n u cleic acids, over w h elm ing th e cell’s em ia. Th erefore, t h e u se of m ild hyp ot h er m ia w as exam in ed
an t ioxidan t system s. p rospect ively in cerebral an eur ysm surger y pat ien ts.22 Th e In -
In th e past , invest igators assum ed th at th e protect ion afforded t raoperat ive Hypoth erm ia for An eu r ysm Su rger y Trial22 (IHAST)
by hypoth erm ia w as on ly th e result of decreased cellu lar m et ab - w as design ed to com pare th e effects of m ild hypoth erm ia (32.5°
olism . Metabolism decreases 6 to 7% for ever y drop of 1°C in to 33.5°C) and norm otherm ia (36° to 37°C) on the long-term neu-
tem perat ure.9 How ever, th is can n ot be th e on ly protect ive m ech - rologic outcom es of pat ien ts w ith docum en ted an eur ysm al sub -
an ism . Th e ben eficial effects of hypoth erm ia appear to be m uch arach n oid h em orrh age w ith in th e t w o w eeks preceding surger y.
greater th an can be explain ed by ch anges in m etabolism alon e. Altogeth er, 1001 pat ien ts w ere ran dom ized to th e tem perat ure
More recen t st u dies h ave h igh ligh ted th e im por t an ce of hyp o- grou ps. Th e p rim ar y depen den t variable, th e Glas gow Ou tcom e
th erm ia in blun t ing or m it igat ing m any of th e dest ru ct ive pro- Scale (GOS) score, w as d eter m in ed 3 m on t h s after su rger y. Pa-
cesses act ivated after an isch em ic in su lt . t ien t s in th e hypoth erm ia grou p h ad n o adverse effect oth er th an
Invest igators h ave sh ow n th at hypoth erm ia can preven t isch - a sligh tly greater in ciden ce of postoperat ive hyper th erm ia. At
em ic cells from en tering apoptosis by in h ibit ing casp ase act iva- 3 m on th s th ere w as n o clear ben efit from in t raoperat ive hypo-
t ion .10,11 Hypoth erm ia also in h ibits n eu roexcitator y p rocesses in th erm ia. Length of st ay (h osp it al an d in ten sive care u n it [ICU]),
brain cells during isch em ia an d rep erfu sion . Hypoth erm ia lim its m or t alit y rate, an d disch arge dest in at ion w ere n o differen t be-
the increase of intracellular calcium , w hich would otherw ise cause t w een th e t w o grou ps. Th e n u m ber of pat ien ts w ith a favorable
m itochondrial dysfunction, depolarization of cell m em branes, and GOS score of 1 w as sim ilar bet w een groups (66% versu s 63%, p =
release of glu t am ate in to th e ext racellu lar sp ace.12 Accum ulat ion 0.32). Neurocognitive deficits were frequently obser ved at the 15-
of ext racellular glut am ate, w h ich fur th er st im ulates calcium in - m onth follow -up, but there w as no difference bet w een groups.23
flu x th rough act ivat ion of calcium ch an n els, results in an excito- Th e absen ce of effect in th e IHAST st u dy m ay be con fou n ded
toxic injury cycle. In anim al m odels hypotherm ia has im proved ion by th e variable effects of inju r y at th e t im e of or im m ediately
h om eostasis an d m it igated m any of th e hyperexcitat ion injuries after an eur ysm al ru pt u re (e.g., vasospasm -in duced isch em ia).
th at resu lt from persisten t glu tam ate.13,14 Pat ien t s w ith th ese injuries could n ot ben efit from m ild hypo-
th erm ia becau se hyp oth erm ia w as in d u ced on ly briefly du ring
surger y, w h ich m ay h ave been perform ed as long as 14 days after
rupt ure. Fu r th erm ore, in t raoperat ive isch em ic even ts th at cou ld
■ Beneficial Effects of Hypothermia have benefited from m ild hypotherm ia w ere uncom m on because
tem porar y ar terial clipping eith er w as n ot used or w as of ver y
Th e accepted prim ar y clin ical in dicat ion for th erapeu t ic hyp o- lim ited du rat ion in m ost pat ien t s. Th e absen ce of a ben eficial ef-
th erm ia is after ou t-of-h osp it al cardiac arrest , th e p u rp ose being fect in th e IHAST st udy does n ot n egate th e posit ive resu lt s of
cerebral protect ion in adults. How ever, th e uses of th erapeut ic hypoth erm ia dem on st rated in m any carefu lly con t rolled labora-
hyp ot h erm ia con t in u e to exp an d an d it is n ow rou t in ely u sed tor y an d clin ical st u dies. In our op in ion , w ith h olding th is poten -
for in -h ospital arrests, for in n eon ates w ith hypoxic isch em ic en - t ially ben eficial t reat m en t from n eu rovascu lar su rger y pat ien ts
ceph alopathy 15 an d after som e t ypes of t raum at ic brain injur y at risk for in t raoperat ive isch em ia seem s ill advised.
(TBI).16,17 For years, th erap eu t ic hypoth erm ia h as also been u sed
in n eurosurgical p rocedu res an d cardiac su rger y. Th is sect ion re-
view s som e of th e clin ical u ses of hypoth erm ia. Cardiac Surgery
Mild an d m oderate hyp oth erm ia, w idely em ployed in cardiac
patients, is intended to provide n eurologic and cardiac protection
Cerebrovascular Surgery an d to sh ield oth er organ s from injur y during cardiopulm on ar y
In 1954, Rosom off an d Holaday 4 sh ow ed th at cerebral blood flow bypass. Neurologic injur y an d n eu rocogn itive declin e after car-
an d cerebral m et abolic rate for oxygen con su m pt ion (CMRO2 ) diac su rger y are com m on an d likely to h ave m u lt ifactorial cau ses
decreased as tem perat u re decreased du ring m ild an d m oderate in h um an s.24,25 Th e m ech an ism s un derlying th ese inju ries are

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13 Hypothermia and Cardiac Arrest for Neurovascular Anomalies 177

likely to include gaseous and particulate em bolism , inflam m atory thors have com m en ted, the results of their t rial do not support the
respon ses to bypass, p latelet act ivat ion , an d global hypop erfu- abandonm ent of any tem perature m anagem ent strategy.
sion. Several random ized, prospective trials failed to dem onstrate
th at hypoth erm ia p reven t s postoperat ive n eu rologic an d n eu ro-
cognitive deficits. How ever, the trials’ assessm ent m ethods varied,
Hypothermia in Traumatic Brain Injury
as did target tem perat ures for th e hypoth erm ic in ter ven t ion an d Because hypoth erm ia redu ces in t racran ial pressure 32 an d raises
rewarm ing strategies. Other studies showed a hypertherm ic over- th e th resh old for seizu res, it h as been u sed in p at ien t s w ith TBI.
sh oot du ring rap id rew arm ing in h u m an s.26 In an im al st u dies An im al st udies suggest th at if hypoth erm ia is in duced w ith in a
even m in or hyper th erm ia m arkedly exacerbates isch em ic brain few h ours of th e prim ar y injur y, th e n eu rologic ou tcom e m ay
injur y.27 Th e adverse effect of hyper th erm ia follow ing rew arm - im prove.33 There still rem ain s con siderable uncertaint y surround-
ing after cardiop u lm on ar y bypass h as likely con foun ded clin ical in g t h e u se of hyp ot h er m ia to t reat TBI in h u m an s. Th e m ost
t rials assessing th e efficacy of in t raoperat ive hyp oth erm ia. recen t m et a-an alyses w ere in con clu sive regard in g lon g-ter m
Slow er rew arm ing an d avoidan ce of hyp er th erm ia con fer an n eu rologic ou tcom es or a decrease in th e m or talit y rate of hypo-
added ben efit to th e m ildly hypoth erm ic pat ien t . Nath an et al28 th erm ic p at ien t s com pared w ith n orm oth erm ic p at ien t s.17 Th e
cooled 233 p at ien t s u n dergoing a carot id ar ter y byp ass graft to t reat m en t w in d ow for t h e in d u ct ion of hyp oth er m ia in p a-
32°C as a n eu roprotect ive st rategy du ring th e su rger y. Pat ien ts t ien t s w ith TBI an d th e opt im al du rat ion of hyp oth erm ia rem ain
w ere th en ran dom ized to a rew arm ing t arget tem perat ure of con t roversial.
37°C or 34°C. Patients rew arm ed to 34°C had few er postoperative
n eu rocogn it ive deficits w h en exam in ed 1 w eek postoperat ively
t h an d id t h ose rew ar m ed to 37°C. At 3 m on t h s, t h e d ifferen ces Deep Hypothermic Circulatory Arrest
in n eu rocogn it ive d eficit s w ere st ill n ot iceable alth ough less ro- Advan ces in en dovascular tech n iques an d th e use of tem porar y
bust . At th e 5-year follow -up, effor t s to iden t ify differen ces w ere clipp ing h ave im proved th e safet y of t reat ing com p lex or gian t
in con clu sive.29 Alth ough laborator y eviden ce for th e n eu ropro- in t racran ial an eu r ysm s. How ever, su rgical t reat m en t of som e
tect ive effect of m ild hypoth erm ia after isch em ia/reperfusion is an eu r ysm s rem ain s tech n ically ch allenging, an d t h e n eed for a
irrefu t able, invest igators h ave been u n able to dem on st rate a p er- blood less su rgical field in w h ich t h e an eu r ysm can be safely
sisten t ben efit in h u m an s. Th is fin ding suggests th e p ossibilit y clipp ed st ill m ay requ ire cardiac st an dst ill. Pon ce et al34 an alyzed
th at isch em ia m ay n ot be th e p rim ar y m ech an ism u n derlying t h e r isk an d lon g-ter m clin ical ou tcom es associated w it h t h e
n eu rocogn it ive declin e after cardiac su rger y. u se of deep hyp oth erm ic circu lator y arrest for th e t reat m en t of
in t racran ial an eur ysm s. Th eir ret rospect ive st udy of 105 deep
hypotherm ic circulatory arrest procedures found that the overall
Cardiac Arrest com bin ed t reat m en t-related m orbidit y an d m or t alit y w as rate
32%. At a m ean long-term follow -u p of 9.7 years, 63% of pat ien ts
Th e ben efit of m ild hyp ot h er m ia for card iac ar rest related to h ad th e sam e or bet ter st at us after su rger y. Th e auth ors agreed
ven t ricu lar fibrillat ion or pu lseless ven t ricu lar t achycardia is th at com pared w ith th e n at u ral h istor y of th e disease, th e risk
w ell kn ow n . Both th e Am erican Hear t Associat ion an d th e In ter- associated w ith deep hypoth erm ic circulator y arrest w as accept-
n at ion al Liaison Com m it tee on Resuscitat ion recom m en d in duc- able. New er, low er risk en dovas cu lar altern at ives m ay be appro-
t ion of su st ain ed m ild hyp oth erm ia after ret u rn of sp on t an eou s priate for selected p at ien t s w ith com plex lesion s.
circulat ion in pat ien ts w h o rem ain com atose after a cardiac ar-
rest . In a lan dm ark Au st ralian st u dy, Bern ard et al30 st u died 77
pat ien ts in cardiac arrest w h o w ere cooled du ring cardiopu lm o-
n ar y resuscitat ion at th e scen e or early du ring t ran spor t to h os- ■ Effects of Hypothermia
pital. Their target tem perature, 33°C, was m aintained for 12 hours
Th e body respon ds to hyp oth erm ia w ith a series of com p en sa-
after h ospital adm ission . In th e hypoth erm ic group, 49% (21/43)
tor y h om eostat ic m ech an ism s. Th e in it ial an d fastest respon se is
of pat ien ts h ad a favorable n eurologic outcom e com pared w ith
to m inim ize heat loss, m ainly th rough an increase of sym pathetic
26% (9/34) in t h e con t rol grou p (p = 0.046), w it h an adju sted
ton e an d periph eral vasocon st rict ion . Th e body also at tem pts to
odd s rat io for good ou tcom e of 5.25. A com p arable Eu rop ean
in crease h eat produ ct ion by sh ivering an d by in creasing m et abo-
st u dy, in w h ich 273 card iac ar rest p at ien t s w ere cooled (32° to
lism . Ever y organ system is affected by hyp oth erm ia (Table 13.1).
34°C) for 24 h ou rs, also sh ow ed favorable ou tcom es for th e hy-
poth erm ic grou p (55% good ou tcom e vs 39% for con t rols).
Recen tly, Nielsen et al.31 failed to dem on st rate th e ben efit of
hypoth erm ia to 33°C com pared to 36°C in un con scious sur vivors
of ou t -of-h osp it al cardiac ar rest . Th is m u lt icen ter t r ial involv-
■ Techniques for Hypothermia
in g 36 ICUs en rolled 950 adu lt s, an d tem perat ure con t rol w as With th e in creasing use of th erapeu t ic hypoth erm ia as a tool to
ach eived w ith in 8 h ours follow ing arrest . Th is st udy suggests ach ieve n europrotect ion an d cardioprotect ion , at ten t ion is sh ift-
th at th e sim p le avoidan ce of hyper th erm ia m ay h ave ben efit s ing to th e eviden ce su pport ing th e efficacy an d safet y of th e vari-
com p arable to m ild hyp ot h er m ia in p ost -resu scit at ion care. ous tech n iqu es by w h ich hypoth erm ia can be in duced. Several
St u dy lim itat ion s (in clu d ing delayed in it iat ion of hypoth erm ia, ch aracter ist ics sh ou ld be con sid ered w h en t h e efficacy of cool-
rapid rew arm ing, use of propofol sedation, var ying degrees of car- in g d evices is ju dged . First , an id eal tech n iqu e sh ou ld in d u ce
diovascular im pairm ent) do n ot perm it the iden tification of those hypoth erm ia w ith speed an d precision , an d it sh ou ld avoid over-
patient subgroups that m ay benefit from hypotherm ia. As the au- shooting the target tem perature. It also should perm it m aintenance

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178 II Evaluation and Treatment Considerations for Neurovascular Disease

Table 13.1 Summary of Main Physiological Effects of Hypothermia by Organ Systems

System Effects of Mild Hypothermia (33°–35°C)

Cardiovascular system Vasoconstriction of peripheral vasculature increases systemic venous resistance.40


Sinus tachycardia initially, then sinus bradycardia with decreasing temperatures (< 35°C).
Prolonged PR and QT intervals with widening of the QRS complex.
Risk of ventricular fibrillation increases with temperatures below 30°C. A hypotherm ic fibrillating heart is unlikely to
respond to defibrillation and antiarrhythmic drugs. These potentially life-threatening rhythms become difficult to
treat without rewarming.
Pulmonary system Peripheral vascular resistance is increased and hypoxic pulmonary vasoconstriction is at tenuated.41
Because the metabolic rate is decreased, any ventilated patient would need adjustm ent of their minute ventilation
to m aintain PCO2 in the normal range.
Pneum onia becom es a risk with prolonged cooling.
Renal system Renal perfusion decreases, along with an associated decrease in glomerular filtration rate.42
Hypothermia decreases reabsorption of solute in the ascending limb of the loop of Henle 43 and suppresses the
release of antidiuretic horm one, which can lead to significant fluid loss.
Hypovolemia from diuresis may have adverse consequences for patients with subarachnoid hemorrhage or with
TBI, because even brief episodes of hypotension can adversely affect outcom e.44
Hypokalemia is comm on in hypothermia because potassium is shifted intracellularly.
Hepatic/gastrointestinal The anesthetic minimum alveolar concentration decreases with hypotherm ia. Changes in protein-binding and
system decreased hepatic and renal blood flow have all been suggested as mechanisms for prolonged effects of
anesthetics.45 Hepatic dysfunction is rare after hypothermia.
Coagulation Hypothermia causes reversible platelet dysfunction due to platelet sequestration and can cause coagulopathy by
decreasing enzyme-m ediated reactions of the coagulation cascade.46 However, in most neurosurgical patients
these effects are not clinically significant.
Endocrine system During hypotherm ia, insulin release and insulin sensitivit y are diminished, t ypically resulting in hyperglycemia.47
Close monitoring of glucose level is recomm ended during hypothermia. Corticosteroid release from the adrenal
cortex does not appear to be affected during short periods of hypothermia but may decrease with prolonged
exposure.48
Immune system Hypothermia can impair immune function; in fact, inhibition of inflammatory responses has been proposed as one
of hypotherm ia’s protective mechanism s. Hypothermia suppresses both chemotactic m igration of leukocytes
and phagocytosis.49
Hyperglycemia during hypothermia can further increase the risk of infection.
Some studies have reported a higher risk of wound infection in hypothermic patients, but short-term cooling
(< 24 hour) does not appear to increase the risk of infection.
Musculoskeletal system Shivering is one mechanism for producing heat. The neuroprotective effect of hypothermia m ay be lost if shivering
is not well controlled.50 Methods to control shivering include counter-cooling, adequate sedation, and even
paralytic agents. In counter-cooling, the awake patient’s head and arms are warm ed, while the core is cooled.
During muscle relaxation, unrecognized nonconvulsive epileptic activit y is a risk, especially in patients with TBI or
anoxic injury.

of hypotherm ia w ith m in im al tem perat u re flu ct uat ion . It should on t h e tem p erat u re grad ien t , t h e area exp osed an d available
provide a controlled rewarm ing phase. It should also have a favor- for h eat t ran sfer, an d th e th erm al con duct ivit y. W h en an act ive
able side-effect profile, an d be cost-effect ive in term s of both cooling process is in it iated, con duct ion an d convect ion in creases
m aterials an d n ursing/m edical st aff effor t . th e am ou n t of h eat loss, an d th e sh u n t ing of blood from th e core
Th e in du ct ion an d m ain ten an ce of hyp oth erm ia can be ch al- to th e periph er y facilitates h eat t ran sfer. Many m eth ods an d de-
lenging depen ding on a p at ien t’s physical ch aracterist ics. Un der vices are available for in du cing an d m ain t ain ing hypoth erm ia.
n orm al con dit ion s, th e h om eost at ic m ech an ism s u sed to m ain - Th ey can be categorized as extern al or n on invasive m eth ods, in -
tain core tem perat ure n eed to be blun ted or ablated to ach ieve clu ding w ater-circu lat ing p ads, air blan ket s, an d ice p acks, an d
hypoth erm ia. Som e pat ien t ch aracterist ics, in clu ding young age invasive m ethods, w hich use intravascular heat-exchange devices,
an d a h igh body m ass in dex, can reduce th e effect iven ess of ex- cold in t raven ou s in fusion s, an d bladder or periton eal lavage.
tern al cooling tech n iques. Th e in ten sit y of th e sh ivering respon se Most st udies using int ravascular heat-exchangers report h ighly
also varies for m uscles in th e periph er y an d m uscles n ear th e reliable m ain ten an ce of core tem perat u re an d relat ively rapid
core. In th e operat ing room , th e in du ct ion of gen eral an esth esia cooling rates on ce th e cath eter is in place. On e of th e disadvan -
assist s in th e developm en t of core hypoth erm ia. Th e m ain te- tages of invasive devices is th at an in ser t ion procedure is re-
n an ce of hypoth erm ia an d th e rate of rew arm ing in th e operat ing qu ired before cooling can be in it iated. W h en th e device is u sed in
room presen t th eir ow n set of ch allenges. t h e op erat in g room for elect ive cases, t h e con t rolled environ -
All of th e m ech an ism s of h eat loss review ed earlier (e.g., ra- m en t an d th e lack of u rgen cy m ake th is a great m et h od for th e
diat ion , con du ct ion , convect ion , evap orat ion ) can be u sed du ring in du ct ion of hyp oth er m ia. Even w h en t h e “even t -to -t arget -
cooling. Th e am ou n t of h eat loss a pat ien t exp erien ces dep en ds tem perat ure” t im e is crit ical, th e greater efficacy of invasive

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13 Hypothermia and Cardiac Arrest for Neurovascular Anomalies 179

tech n iqu es m ay m ore t h an offset t h e t im e lost in im p lem en - th is m eth od provides a ver y rapid rate of cooling (8°–10°C/h ) at
t at ion . Obviously, th e availabilit y of p hysician s adept w ith th e m in im al cost . In th e in ten sive care un it surface cooling w ith ice
tech n ique an d ready access to appropriate im aging for device packs is p ossible bu t m ay be labor in ten sive for th e n u rsing staff.
placem en t m u st also be con sidered . It also can pose th e risk of skin dam age.
Most p at ien t s w ith a body m ass in dex less th an 30 can be
cooled su ccessfu lly (2° to 3°C/h ) an d rew arm ed (~ 1°C/h ) w ith
Circulating Cold Water
su rface m eth ods w ith or w ith ou t bladder irrigat ion . More inva-
sive m eth ods are requ ired for obese pat ien ts. No device h as yet The LRS Therm osuit System (Life Recover y System s, Kinnelon, NJ)
been ap proved for th e p reven t ion or t reat m en t of in t raop erat ive m ay be the fastest cooling system on the m arket. In anim al studies,
isch em ic injur y. Th e u se of any tem perat u re m an agem en t device cooling rates reach ed 10°C/h .35 It provides circulat ing cold w ater
to m it igate n eu rologic inju r y con st it u tes an off-label applicat ion directly again st th e skin of th e pat ien t w h ile th e p at ien t rem ain s
in th at pop ulat ion . With th at in m in d, m any d evices are used in partly su bm erged in an in flatable bed as th e w ater circu lates.
th e crit ical care set t ing an d du ring th e p eriop erat ive p eriod w ith Th e system is for cooling on ly. Th ere is n o m ech an ism for m ain -
good resu lt s. Based on m ost t rials com p aring t h e efficacy of tain ing target tem perat ure. With th e rapid rate of cooling, cau-
w ater-cooling an d air-cooling blan kets, w ater-cooling blan kets t ion sh ou ld be exercised becau se rapid sh ifts in th e levels of elec-
h ave been m ore efficien t for cooling t h an for w ar m ing. Non in - t rolytes can h ave adverse effects.
vasive an d invasive tech n iques are described below w ith a brief
discu ssion of th eir m ech an ics an d p roposed u se.
Water-Circulating Cooling Blankets and Cooling Pads
Hypoth erm ia occurs th rough con duct ion h eat loss as cold w ater
Noninvasive Methods circulates th rough pads th at con t act th e pat ien t but th at do n ot
adh ere directly to th e skin . Th e abilit y to con t rol th e circulat ing
Passive Cooling w ith Skin Exposure (w ith or Without
w ater tem perat ure en h an ces safet y an d decreases n ursing labor.
Water/Alcohol Sprays)
Th e u se of t w o cooling blan ket s san dw ich ing th e p at ien t in th e
Sin ce th e ver y begin n ing of th erap eu t ic hyp oth erm ia, exposu re m iddle can greatly in crease th e rate of cooling. Som e m an ufac-
of th e skin to am bien t air h as been used to cool pat ien ts (radia- t u rers (e.g., CoolBlu e Su rface Pad System , In n erCool Th erap ies,
tion ). Th is m ethod of passive cooling is easy an d inexpensive, w ith San Diego, CA) p rovide disp osable vest s an d th igh w rap s th at are
n o procedu ral risk. After an esth esia is in duced, exposu re of th e relat ively in expen sive. Oth ers produ ct s h ave som e reu sable p ar t s
pat ien t to th e cold environ m en t of th e operat ing room p rom otes (e.g., Ban ket rol II/III Hyp er-Hyp ot h er m ia, Su b -Zero Com p any,
hypoth erm ia. Th e u se of in h aled an esth et ics results in vasodila- Cin cin n at i, OH).
t ion an d sp eeds u p th e rate of cooling. Th e sp eed of cooling w ith Hydrogel-coated w ater circulating pads (e.g., Arctic Sun Tem -
exp osure to air m ay be slow (~ 0.5°C/h ), an d it is im pract ical for perat u re Man agem en t System , Medivan ce, In c., Lou isville, CO)
th e m ain ten an ce ph ase. Environ m en t al exposu re can n ot be u sed con sist s of adh esive hydrogel-coated w ater circu lat ing p ads th at
du ring th e rew arm ing p h ase becau se m ost st aff m em bers w ork- st ick to th e pat ien t , w h ile th e circu lat ing w ater is cooled in an
ing in th e operat ing room w ill n ot tolerate th e h igh am bien t tem - extern al device. Th e hydrop h ilic gel on th e p ads con du ct s h eat
perat u res th at w ou ld be requ ired. Using th e cooling effect s of an d m ain tain s close con tact bet w een th e skin an d pads. Because
evaporat ion , pat ien ts can be sprayed w ith w ater or alcoh ol an d skin contact is m axim ized, less of the patient’s surface area n eeds
exp osed to air w ith or w ith ou t th e u se of a fan . Alcoh ol sp rays to be covered. Th e Arct ic Sun is less labor in ten sive an d m ore
are m ore effect ive th an w ater sprays an d can speed th e rate of u ser frien dly th an oth er w ater circulat ing blan ket s, an d relat ively
cooling by as m u ch as 1°C/h . Draw backs of th is m eth od in clu de h igh cooling rates can be ach ieved (~ 1.5°–2°C/h ). Th e d evice
th e n eed for sign ifican t n u rsing labor, th e possibilit y of a fire can be u sed reliably in th e m ain ten an ce an d rew arm ing p h ase,
h azard, an d its in effect iven ess for rew arm ing. alth ough skin burn s h ave been obser ved. Its efficien cy, relat ive
safet y (n o vascu lar com p licat ion s an d th e in frequ en cy of over-
cooling or bu rn inju r y), an d ease of u se m ake it a su it able cooling
Air-Circulating Cooling Blankets
d evice in th e cr it ical care set t ing. It p roved to be su p er ior to
Th e u se of circu lat ing cooling blan ket s (Polar Air, Bair Hugger, r u bber w ater-circulat ing blan ket s for th e m an agem en t of fever
3M Health Care, Lough borough , Leicestersh ire) is relat ively in ex- in pat ien ts w ith severe st roke.36 Un like rubber blan ket s, th e pads
pen sive. Th e equ ip m en t is already available in m ost operat ing are n ot reusable, an d th e cost of th e un it can be h igh . Th ere is a
room s an d in ten sive care un it s du e th e ubiqu it y of th ese m odali- poten t ial for th erm al inju r y, and th e device sh ould n ot be used
t ies for p at ien t w arm ing or for m ain tain ing n orm oth erm ia du r- on pat ien t s on h igh doses of vasocon st rictors, in th ose w ith im -
ing su rger y. Cooling w ith an air circulat ing blan ket is n o m ore paired left ven t ricu lar fu n ct ion , or in th ose n eeding circu lator y
effect ive th an skin exp osure, an d th e rate of cooling can be ver y arrest in th e operat ing room .
slow (~ 0.5°C/h ).

Invasive Methods (Core Cooling )


Immersion in Cold Water and Surface Cooling w ith
In fu sion of ice-cold (4°C) flu ids is a ver y rapid m eth od to in duce
Ice Packs
hypoth erm ia. It can be u sed in conju n ct ion w ith oth er m eth ods
Th e com p lete im m ersion of th e pat ien t in cold w ater is im p ract i- described earlier. Rap id in fu sion of cold cr ystalloid or 5% albu -
cal in th e operat ing room or in ten sive care u n it . For rap id in du c- m in solut ion s can cool at rates of ~ 2.5° to 3.5°C/h . A draw back of
tion of hypotherm ia in the field or in oth er austere environ m ents, th is m eth od is th e p oten t ial for volu m e overload an d p u lm on ar y

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180 II Evaluation and Treatment Considerations for Neurovascular Disease

edem a. Th is tech n iqu e is n ot w ell su ited for th e m ain ten an ce of Th e Celsiu s Con t rol System (In n ercool Th erap ies) is a tem per-
hypotherm ia, so its use should be com bined w ith other m ethods. at u re-con t rol system in w h ich w ater circu lates th rough a flexible
Bern ard et al30 used large volum es (30 m L/kg) of cold lactated m et allic cath eter placed in th e in ferior ven a cava. Th e cath eter
Ringer’s solut ion to cool 22 com atose su r vivors of out-of-h ospi- design in d u ces t u rbu len t flow an d facilit ates h eat exch ange. It is
tal cardiac arrest an d successfully decreased core tem perat ure h igh ly effect ive in providing p recise tem perat u re con t rol. Un like
from 35.5° to 33.8°C w ith in 30 m in u tes w ith n o adverse con se- th e Alsiu s system , th e In n erCool device does n ot ser ve as a cen -
qu en ces. In other st u dies, tem p erat ure w as d ecreased by 2° to t ral ven ou s lin e. Th e system is n ot approp riate for aw ake/m obile
4°C w ith ou t decreasing th e left ven t ricular systolic fun ct ion or pat ien ts becau se th e large-bore fem oral in sert ion site (10.7–14
cardiac ou t put an d w ith ou t frequ en t p u lm on ar y edem a.37 Fren ch ) requ ires th at p at ien t s rem ain m ot ion less w ith m in im al
h ip flexion . Th e cath eter can easily be in ser ted in th e operat ing
room an d in ten sive care u n it . Th e posit ion of t h e cath eter w ith
Intravascular Catheters
th e dist al t ip ju st below th e diaph ragm can be con firm ed w ith
Th e u se of in t ravascu lar cat h eters (CoolLin e, Coolgard , an d por t able flu oroscopy or a ch est X-ray. In t ravascular cooling sys-
For t iu s, Alsiu s Cor p orat ion , Ch elm sford , MA; In n erCool Ph ilip s tem s are expen sive to purch ase an d ut ilize, but th ey m ay be cost-
Health care, San Diego, CA; Celsiu s Con t rol System s, SetPoin t , an d effective w hen nursing tim e, com plications, and patient outcom es
Reprieve, Radian t Medical, Redw ood Cit y, CA) is in creasing as are con sidered.
t h ey con t in u e to be sh ow n to be effect ive an d safe for t h e in -
d u ct ion an d m ain ten an ce of hypoth erm ia. In a m ulticen ter t rial,
cooling rates in en dovascu lar an d su rface cooling grou ps w ere
com p ared du ring clipp ing of u n ru pt u red cerebral an eu r ysm s.
■ Conclusion: Areas of Uncertainty
Th e en dovascu lar grou p con sisten tly ach ieved th e t arget tem - Alth ough th e im pressive protect ive effect s of hypoth erm ia foun d
perat u re of 33°C by th e t im e th e an eu r ysm w as clipped com - in an im al m odels of cerebral isch em ia are w ell est ablish ed, th e
pared w ith th e su rface cooling grou p (99%versu s 20%, p < 0.001). clin ical u sefu ln ess of hyp oth erm ia in th e h u m an brain h as been
Th e rate of coolin g w as sign ifican t ly m ore rap id in t h e en d o - questioned. Detractors of intraoperative hypotherm ia hypothesize
vascu lar grou p (4.77°C/h ) t h an in t h e su r face cooling grou p th at th e cellu lar m ech an ism s of isch em ic inju r y in lissen ceph alic
(0.87°C/h ). Th e rew arm ing rate w as also sign ifican tly faster for an im als (e.g., roden ts) are m ore respon sive to th e ben eficial ef-
th e en dovascular tech n ique (1.88° vs 0.69°C/h , p < 0.001), en sur- fects of hyp oth erm ia th an th ey are in h um an s w ith our com plex
ing n orm oth erm ia in m ore th an 80% of th e cases by th e en d of gyrencephalic brains. Typically, they cite the IHAST study 22 to sup -
surger y.38 por t th eir posit ion , ign oring th e fact th at IHAST w as n ot design ed
All of devices cited in th is sect ion use an in dw elling cen t ral to answ er th at question directly. The m olecular m ech anism s that
ven ou s h eat exch anger th at can be in ser ted via th e fem oral vein , u n derlie isch em ia-in du ced apoptosis seem to be w ell conser ved
w h ile ster ile salin e, cooled in an exter n al d evice, is p u m p ed in n euron s from com plex prim ates to n eu ron s in th e sim ple soil
t h rough t h e h eat exch an ger. Th is p rocess cools core blood d i- n em atode Caenorhabdit is elegans.
rect ly. In t h e case of t h e CoolLin e d evice, sm aller cat h eters As Yenari and Han 39 state in their review, “hypotherm ia affects
can be in ser ted via t h e su bclavian or in ter n al jugu lar vein s. Th e n early ever y invest igated cell death path w ay, in cluding path w ays
CoolLin e cath eter con t ain s a tem p erat u re p robe, an d t w o p or ts leading to excitotoxicit y, apoptosis, in flam m at ion , an d free radi-
for cen t ral ven ous access th at can be u sed to sam ple blood an d cal p rod u ct ion , an d it is likely t h at n o sin gle factor can exp lain
to adm in ister m edicat ion . For th e CoolLin e cath eter, m a xim u m it s u n derlying ben eficial effect .” On e th ing is clear: Th e clin ical
cooling rates in pu blish ed st u dies h ave averaged 2° to 2.5°C/h . ap plicat ion of m ild hypoth erm ia is likely to be ben eficial in n eu-
How ever, all en dovascu lar m eth ods requ ire an in ser t ion p roce- rosurgical patients at risk for intraoperative ischem ia, but its suc-
du re th at cou ld delay th e on set of cooling, an d th ey h ave been cessful im plem en tat ion requires th e use of st rict protocols an d
associated w ith an in creased risk for deep ven ou s th rom bosis. vigilan ce by th e physician s an d n u rsing st aff.

References
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5. Busto R, Diet rich W D, Globus MY, Valdés I, Sch ein berg P, Gin sberg MD. 11. Adach i M, Soh m a O, Tsu neish i S, Takada S, Nakam ura H. Com bin at ion ef-
Sm all differen ces in in t raisch em ic brain tem perat u re crit ically determ in e fect of system ic hypotherm ia and caspase inhibitor adm inistration against
th e exten t of isch em ic n euron al injur y. J Cereb Blood Flow Met ab 1987;7: hyp oxic-isch em ic brain dam age in n eon at al rat s. Ped iat r Res 2001;50:
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12. Siesjö BK, Bengt sson F, Gram pp W, Th ean der S. Calcium , excitotoxin s, and 31. Nielsen N, Wet tersley J, et al. Targeted tem perat u re m an agem en t at 33°C
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13. Winfree CJ, Baker CJ, Con n olly ES Jr, Fiore AJ, Solom on RA. Mild hypoth er- 32. Clifton GL, Miller ER, Ch oi SC, et al. Lack of effect of in du ct ion of hypother-
m ia reduces pen um bral glut am ate levels in th e rat perm an en t focal cere- m ia after acute brain injur y. N Engl J Med 2001;344:556–563
bral isch em ia m odel. Neurosurger y 1996;38:1216–1222 33. Clark RS, Koch an ek PM, Marion DW, et al. Mild post t raum at ic hypoth er-
14. Globu s MY, Alon so O, Diet rich W D, Busto R, Gin sberg MD. Glut am ate re- m ia reduces m or t alit y after severe con t rolled cor t ical im pact in rat s. J
lease an d free radical product ion follow ing brain injur y: effect s of post- Cereb Blood Flow Met ab 1996;16:253–261
t raum at ic hypotherm ia. J Neuroch em 1995;65:1704–1711 34. Pon ce FA, Spet zler RF, Han PP, et al. Cardiac st an dst ill for cerebral an eu-
15. Jacobs S, Hun t R, Tarn ow -Mordi W, In der T, Davis P. Cooling for n ew born s r ysm s in 103 pat ien t s: an update on th e experience at th e Barrow Neuro-
w ith hypoxic isch aem ic encephalopathy. Coch rane Database Syst Rev 2007; logical In st it ute. Clin ical ar t icle. J Neurosurg 2011;114:877–884
4:CD003311 35. Jan at a A, Weih s W, Bayegan K, Sch rat ter A, Holzer M, Beh ringer W, Sch ock
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rot raum a 2007;24(Suppl 1):S1–S106 w ith a n ovel surface cooling device im proves n eurologic outcom e after
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brain injur y: a system at ic review an d m et a-an alysis. J Neurot raum a 2008; 36. Mayer SA, Kow alski RG, Presciut t i M, et al. Clin ical t rial of a n ovel surface
25:62–71 cooling system for fever con t rol in n eurocrit ical care pat ien t s. Crit Care
18. Mich en felder JD, Th eye RA. Th e effect s of an esthesia an d hypotherm ia on Med 2004;32:2508–2515
can in e cerebral ATP an d lact ate during an oxia produced by decapit at ion . 37. Polderm an KH, Rijn sburger ER, Peerdem an SM, Girbes AR. In du ct ion of
An esth esiology 1970;33:430–439 hypoth erm ia in pat ien t s w ith various t ypes of n eurologic injur y w ith use
19. Busto R, Globus MY, Diet rich W D, Mart in ez E, Valdés I, Gin sberg MD. Ef- of large volum es of ice-cold in t raven ous fluid. Crit Care Med 2005;33:
fect of m ild hypoth erm ia on isch em ia-in duced release of n eurot ran sm it- 2744–2751
ters an d free fat t y acids in rat brain . St roke 1989;20:904–910 38. Stein berg GK, Ogilvy CS, Sh uer LM, et al. Com parison of en dovascular an d
20. Clifton GL, Jiang JY, Lyeth BG, Jen kin s LW, Ham m RJ, Hayes RL. Marked surface cooling during un r upt ured cerebral an eur ysm repair. Neurosu r-
protect ion by m oderate hypoth erm ia after experim en t al t raum at ic brain ger y 2004;55:307–314, discussion 314–315
injur y. J Cereb Blood Flow Met ab 1991;11:114–121 39. Yen ari MA, Han HS. Neuroprotect ive m ech an ism s of hypoth erm ia in brain
21. Riden our TR, Warn er DS, Todd MM, McAllister AC. Mild hypoth erm ia re- isch aem ia. Nat Rev Neurosci 2012;13:267–278
du ces in farct size resu lt ing from tem p orar y bu t n ot perm an en t focal isch - 40. Reu ler JB. Hypoth erm ia: path ophysiology, clinical set t ings, an d m an age-
em ia in rat s. St roke 1992;23:733–738 m en t . An n In tern Med 1978;89:519–527
22. Todd MM, Hin dm an BJ, Clarke W R, Torn er JC; In t raoperat ive Hypoth erm ia 41. Ben um of JL, Wah ren brock EA. Depen den cy of hypoxic pu lm onar y vaso-
for An eu r ysm Su rger y Trial (IHAST) Invest igators. Mild in t raop erat ive hy- con st rict ion on tem perat ure. J Appl Physiol 1977;42:56–58
poth erm ia during su rger y for in t racran ial an eur ysm . N Engl J Med 2005; 42. Boylan JW, Hong SK. Regulat ion of renal fun ct ion in hypoth erm ia. Am J
352:135–145 Physiol 1966;211:1371–1378
23. Sam ra SK, Giordan i B, Caven ey AF, et al. Recover y of cogn it ive fun ct ion 43. Wong KC. Physiology an d p h ar m acology of hyp ot h erm ia. West J Med
after su rger y for an eur ysm al subarach n oid h em orrh age. St roke 2007;38: 1983;138:227–232
1864–1872 44. Th e Brain Trau m a Foun dat ion . Th e Am erican Associat ion of Neurological
24. Roach GW, Kan ch uger M, Mangan o CM, et al; Mu lt icen ter St u dy of Periop - Su rgeon s. Th e Join t Sect ion on Neu rot rau m a an d Cr it ical Care. Gu id e-
erat ive Ischem ia Research Group and th e Isch em ia Research and Educa- lin es for cerebral p er fu sion p ressu re. J Neurot raum a 2000;17:507–511
t ion Fou ndat ion Invest igators. Adverse cerebral outcom es after coronar y 45. Heier T, Caldw ell JE, Sessler DI, Miller RD. Mild in t raoperat ive hypoth er-
bypass surger y. N Engl J Med 1996;335:1857–1863 m ia in creases d u rat ion of act ion an d spon t an eou s recover y of vecu ron iu m
25. New m an MF, Math ew JP, Grocot t HP, et al. Cen t ral n er vous system injur y blockade during n it rous oxide-isofluran e an esth esia in h um an s. An esth e-
associated w ith cardiac surger y. Lan cet 2006;368:694–703 siology 1991;74:815–819
26. Grocot t HP, New m an MF, Crough w ell ND, W h ite W D, Low r y E, Reves JG. 46. Dout rem epuich C. Haem ost asis defect s follow ing cardio-pu lm on ar y by-
Con t in u ou s jugu lar ven ou s versu s n asop h ar yngeal tem p erat u re m on i- pass based on a st udy of 1350 pat ien t s. Th rom b Haem ost 1978;39:539–
tor ing during hypoth erm ic cardiopulm on ar y bypass for cardiac surger y. 541
J Clin An esth 1997;9:312–316 47. Kan ter GS. Ren al clearan ce of glucose in hypoth erm ic dogs. Am J Physiol
27. Diet rich W D, Busto R, Valdes I, Loor Y. Effect s of n orm oth erm ic versus 1959;196:866–872
m ild hyperth erm ic forebrain isch em ia in rats. Stroke 1990;21:1318–1325 48. MacPh ee IW, Gray TC, Davies S. Effect of hypoth erm ia on th e adren ocor t i-
28. Nath an HJ, Wells GA, Mun son JL, Wozny D. Neuroprotect ive effect of m ild cal respon se to operat ion . Lan cet 1958;2:1196–1199
hypoth erm ia in pat ien t s u n dergoing coron ar y arter y su rger y w ith cardio- 49. Salm an H, Bergm an M, Bessler H, Alexan drova S, Beilin B, Djaldet t i M.
pulm onar y bypass: a random ized trial. Circulation 2001;104(12, Suppl 1): Hypotherm ia affects the phagocytic activit y of rat peritoneal m acrophages.
I85–I91 Act a Physiol Scan d 2000;168:431–436
29. Nath an HJ, Rodriguez R, Wozny D, et al. Neuroprotect ive effect of m ild 50. Pold erm an KH, Peerdem an SM, Girbes AR. Hyp op h osp h atem ia an d hy-
hypoth erm ia in pat ien t s un dergoing coron ar y arter y surger y w ith cardio- p om agn esem ia in d u ced by coolin g in p at ien t s w it h severe h ead inju r y.
pulm on ar y bypass: five-year follow -up of a ran dom ized t rial. J Th orac J Neurosurg 2001;94:697–705
Cardiovasc Su rg 2007;133:1206–1211
30. Ber n ard S, Bu ist M, Mon teiro O, Sm it h K. In d u ced hyp ot h erm ia u sing
large volu m e, ice-cold in t raven ou s flu id in com atose su r vivors of ou t-of-
hospital cardiac arrest: a prelim inary report. Resuscitation 2003;56:9–13

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14 Invasive and Noninvasive Imaging
of the Vasculature
Joseph E. Heiserm an

Th e in t racran ial vascu lat u re is tech n ically ch allenging to visu al- n u m ber of elem en t s along each lin ear d im en sion is called t h e
ize becau se of th e p resen ce of th e calvaria, an d th e h igh vascu lar m at rix (M), a t ypical valu e of w h ich is 1024. Th e field of view
den sit y an d com plex cou rse of th e in tracran ial ar teries. How - (FOV) describes th e an atom ic area projected on th e input side of
ever, in 1927 a team led by Egas Mon iz, a professor of n eurology th e detector. A sm all FOV resu lt s in m agn ificat ion of th e area of
at th e Un iversit y of Lisbon , su cceeded in radiograph ically visu al- in terest . Th u s th e im age is divided in to M 2 pict ure elem en t s (pix-
izing the in tracran ial course of an arter y in a 20-year-old patien t.1 els). Th e resolu t ion of th e im aging system depen ds on th e p ixel
Mon iz w as able to diagn ose a pit u it ar y t u m or from disp lacem en t size an d focal sp ot size as w ell as on oth er factors. W h en sm all
of t h e vessels com p ared w it h p reviou s cadaver inject ion s an d cerebral vessels are im aged, a spat ial resolut ion as est im ated by
t h u s in t rod u ced a n ew tool for t h e d etect ion of in t racran ial le- a pixel size of 0.2 m m is t ypical. In addit ion to h igh spat ial reso-
sion s. Th e u se of cerebral angiograp hy for th e diagn osis of lu t ion , DSA can be p erform ed at h igh fram e rates, for exam p le, to
m asses h as sin ce been su p ersed ed by cross-sect ion al im agin g. differen t iate ar terial from ven ou s st ru ct u res. For diagn ost ic cere-
Non et h eless, m odern digit al su bt ract ion angiography (DSA) re- bral angiography, 4 fram es/secon d w ou ld be a t ypical value.
m ain s th e referen ce stan dard for th e diagn osis of in t racran ial Cerebral angiograp hy is t ypically perform ed w ith a bip lan ar
vascu lar lesion s. im aging system to obt ain t w o p roject ion s sim u lt an eously, u su -
Early on , cerebral angiograp hy w as associated w ith a m or t al- ally at r igh t an gles to each ot h er. A sign ifican t advan ce w as
it y rate of ~ 1.5%. Today, angiograp hy is far safer. St ill, even in th e ach ieved w it h t h e in t rod u ct ion of t h ree-d im en sion al (3D) ro-
best h an ds, conven t ion al cerebral angiography rem ain s an inva- t at ion al angiography (RA). Du ring a con t in u ous inject ion of ra-
sive an d t im e-con su m in g p roced u re. Th e n eed for n on invasive d iograp h ic con t rast m ater ial in to t h e vessel of in terest , rap id
or at least less invasive altern at ives w as clear, bu t 50 years passed sequen ce im aging is obtain ed during th e com puter-con t rolled
before advan ces in tech n ology p rovided th e an sw er. rot at ion of th e angiograp h ic gan t r y t h rough a h alf circle cen tered
Th e first opt ion for n on invasive im aging w as act u ally m ore of n ear th e region of in terest . Th e result is a 3D represen t at ion of
a supplem en t th an an altern at ive. Carot id an d t ran scran ial Dop - th e injected vessel, t yp ically u sing volu m e ren dering, w h ich can
pler u lt rason ograp hy cam e in to gen eral u se in th e early 1980s, t h en be rot ated in to any d esired view in g an gle. Alter n at ively,
an d it en abled a fairly lim ited but n on invasive an d por t able eval- reform at ted slices th rough th e region of interest can be obt ain ed
uat ion of th e cer vical an d cen t ral in t racran ial arteries. In addi- at any project ion angle. High -perform an ce angiograp h ic equ ip -
t ion , in 1954, soon after n u clear m agn et ic reson an ce (NMR) w as m en t is n eeded for good results. Rot at ion t im es of 180 degrees
in t rod u ced , t h e effect of blood flow on NMR sign als w as d e- per 5 to 10 secon ds, w ith 100 to 200 im ages collected, are t yp i-
scribed. How ever, rep or ts describing tech n iqu es th at led to clin i- cal. Som e degree of sp at ial resolu t ion is sacrificed to obt ain th e
cal m agn et ic reson an ce (MR) angiography on ly began to app ear rapid im aging, resu lt ing in ~ 0.5 m m isot ropic volum e elem en t s
around 1985. With the developm ent of spiral and especially m ul- (voxels) in th e fin al im ages.
tidetector com pu ted tom ography (CT) scan n ers, CT angiography During angiography, h igh -speed rot ation of th e gan t r y can
becam e p ract ical. Th e first rep or t of ap p lying CT angiograp hy also be u sed to obtain cross-sect ion al im ages. Th is tech n ology is
to cerebrovascu lar im agin g w as in 1992. Th u s, by t h e daw n ing kn ow n as flat-d etector or C-ar m con e-beam CT. Th e resu lt ing
of th e 21st cen t u r y, m u lt iple m eth ods w ere available for im aging im ages ap p roach t h e resolu t ion of st an dard m u lt id etector CT
an d evaluat ing th e n eurovasculat ure. Th is ch apter exam in es cur- scan s. How ever, th e con t rast resolu t ion (rat io of sign al-to-back-
ren tly available tech n iqu es an d discusses th eir st rength s, w eak- grou n d n oise) is lim ited by X-ray scat ter. Th ese system s are also
n esses, an d diagn ost ic applicat ion s. su bject to several ar t ifact s, alth ough th ey do h ave u ses in su rgi-
cal an d en dovascular th erapy set t ings.

Risks
■ Conventional Cerebral Angiography In several recen t st u d ies, n eu rologic even t s tem p orally related
Digit al su bt ract ion angiography system s con sist of a source of to th e angiograph ic procedure occu rred in ~ 1%of cerebral angio-
X-rays collim ated to a sm all focal sp ot an d a detector. Essen t ially, gram s, abou t h alf of w h ich w ere t ran sien t . Im aging in dicat ion s
th is d evice is an X-ray cam era, eith er an im age-in ten sifier u n it of su barach n oid h em orrh age an d ath erosclerot ic cerebrovascu -
or, n ow, m ore com m on ly, a solid -state detector. Th ese t w o com - lar disease are p redict ive of a factor of 2.5 elevated risk of n eu ro-
pon en t s are p laced on opp osite sides of th e pat ien t , an d X-rays logic com p licat ion com p ared w ith p at ien t s w ith ou t th ese risk
n ot absorbed by th e pat ien t register at th e detector. Th e detector factors.2 Th e overall m or t alit y rate is ver y low, ~ 0.3%. Iat rogen ic
is divided in to m ult iple sep arate elem en ts in a squ are array. Th e dissect ion occu rs in 0.4% of st u dies, u su ally involving a ver tebral

182

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14 Invasive and Noninvasive Imaging of the Vasculature 183

ar ter y, but it is rarely sym ptom at ic.3 Tran sien t cor t ical blin dn ess resolut ion , an d th e FOV d ivided by th e m at rix for th e in -plan e
is associated w ith 0.3 to 1%of st u dies, an d it is u su ally associated (t ran sverse) resolu t ion or pixel size. Typical m in im um values are
w ith ver tebral ar ter y inject ion an d th ough t to be related to n eu - 0.5 to 0.6 m m for both in - an d th rough -plan e, w h ich is t w o to
rotoxicit y from t h e con t rast .4 Du r ing d iagn ost ic an giograp hy, three tim es larger th an the pixel dim ension obtainable w ith DSA.
cerebral an eur ysm s rerupt ure w ith an in ciden ce of 1 to 2%, an d Con t rast resolu t ion determ in es h ow readily a par t icu lar im age
it is associated w ith h igh su bsequ en t m orbid it y an d m ortalit y feat ure can be dist inguish ed from th e backgroun d. It depen ds on
rates.5 Rerupt u re is likely related to h em odyn am ic ch anges as- X-ray dose an d en ergy. Par t ial-volu m e effects arise w h en t issues
sociated w ith inject ion of a bolu s of con t rast . Th e risk m igh t be w it h d ifferen t X-ray at ten u at ion (e.g., bon e an d blood vessel)
sligh tly h igh er w ith 3D RA becau se th e adm in ist rat ion of a con - con t r ibu te to a sin gle voxel. In t h is case, t h e br igh t n ess of t h e
t rast bolus is prolonged . associated pixel in th e CT im age is a volu m e average of th e con -
Anaphylact ic reactions associated w ith in traarterial injection t ribut ing t issu es.
of iod in ated con t rast m ed ia are rare, ~ 0.06%. Con t rast -in d u ced Th is last effect is an im p or t an t sou rce of art ifact s in CT angi-
n eph ropathy is th ough t to be related to th e deteriorat ion of ren al ograp hy. For exam p le, calcified p laqu e alon g t h e m argin of a
fun ct ion after angiography is thought to prim arily affect patien ts blood vessel op acified by radiograp h ic con t rast m ater ial m ay
w h ose ren al fu n ct ion is im p aired before angiography. In som e resu lt in a p ar t ial-volu m e ar t ifact th at m in im izes th e ap p earan ce
st u dies, in t raar terial con t rast inject ion h as been associated w ith of n arrow ing of th e adjacen t vessel lum en . Th e ar t ifact is m in i-
about t w ice th e risk of con t rast-in duced n eph ropathy com pared m ized by increased spatial resolution (sm all voxels) and im proved
w ith int raven ous inject ion s.6 To preven t th is com plicat ion , hy- con t rast resolu t ion (red u ct ion in backgrou n d n oise en h an ces
drat ion is u sed as a p rop hylact ic m easu re. Th e efficacy of oth er visu alizat ion of th e differen ces in at ten u at ion bet w een calciu m
agen t s for prop hylaxis an d t reat m en t is n ot w ell su p por ted .7 For- and contrast m aterial). Partial-volum e effects can also be reduced
m erly, gadolin ium -based con t rast agen ts for MR im aging w ere by post processing. Th ere are t rade-offs in CT angiography be-
used for cerebral angiography in th e set t ing of p reexist ing ren al t w een m axim u m spat ial resolut ion an d scan t im e an d bet w een
in su fficien cy. How ever, d oing so is n o longer recom m en ded be- acceptable con t rast an d spat ial resolu t ion an d radiat ion dose.
cau se of sim ilar ren otoxic effect s an d th e p ossibilit y for n eph ro- Full coverage of th e adult brain requires a detector array of at
genic system ic fibrosis, w hich is also now know n to be associated least 256 elem en t s 0.5-m m long. Scan n ers w ith detector arrays
w ith h igh doses of gadolin ium injected in pat ien t s w ith im paired w ith as m any as 320 elem en t s are available. Th ese m ach in es,
ren al fu n ct ion .8 Occasion ally, CO2 gas h as been u sed as a safe an d w ith less th an a 1-secon d rotat ion t im e, can acquire a t im e series
effect ive con t rast agen t in p at ien ts allergic to con t rast or in th ose of im ages of th e w h ole brain w ith 0.5-m m spat ial resolut ion an d
w ith ren al in sufficien cy. less than 1-secon d tem poral resolution. These param eters are ad-
equ ate to resolve th e ar terial an d ven ou s p h ases of th e cerebral
circu lat ion , alth ough n ot at qu ite t h e sam e level as DSA. Alter-
n at ively, acqu isit ion can be gated to th e cardiac cycle to produce
cin e im ages of path ology such as an eu r ysm s.
■ Computed Tomography Angiography Becau se m u lt id etector CT an giograp hy can gen erate a large
Th e cerebral vascu lat u re is a low -resist an ce bed, w ith an ar terio- n u m ber of im ages in a br ief t im e, p ost p rocessing m et h od s are
ven ou s circu lat ion t im e of ~ 4 secon ds. Th us, accurate t im ing of cru cial to its usefuln ess.9 Because th e resolut ion is alm ost isot ro-
con t rast bolu s an d rap id sequ en cing are requ ired to im age du r- pic, im ages can be review ed in several p lan es, t yp ically sagit tal,
ing th e arterial ph ase. Modern m u lt idetector CT scan n ers, w h ich axial, an d coron al. Th is process is kn ow n as m u lt iplan ar refor-
t ypically h ave at least 64 detectors, can acqu ire th e en t ire vol- m at t ing, an d it com bin es im ages to produce sligh tly th icker sec-
u m e of th e h ead in a few secon ds an d th u s m ake angiograph ic t ion s. Cu r ved reform at s can be obtain ed by sp ecifying a lin e th at
im aging possible. follow s a vascular lum en, producing a linear project ion of the ar-
To acquire im ages, th e gan t r y con t ain ing th e X-ray gen erator ter y of in terest . Volum e-ren dering soft w are can p rovide im ages
an d detectors is rapidly rotated w h ile th e pat ien t is slow ly ad- of th e vessels th at resem ble angiogram s, an d th ey can be rotated
van ced in to th e m ach in e. Th e resu lt is a h elical scan , w h ich can in real t im e to evaluate com plicated an atom y. Maxim um in ten -
be post processed via in terpolat ion an d back project ion to pro- sit y p roject ion (MIP) im ages can be obt ain ed by select ing t h e
du ce axial im ages. Coverage is determ in ed by th e p itch , defin ed brigh test pixel along radially orien ted rays cast th rough th e im -
for a single detector as th e dist an ce th e pat ien t t ravels per rota- ages, again producing p roject ion s th at resem ble angiogram s.
t ion divided by th e X-ray beam w idth . A pitch of 1 corresp on ds to Th e m ost ser iou s lim it at ion associated w it h CT an giograp hy
con t in u ou s coverage, a p itch of less t h an 1 resu lt s in overlap , an d is th e passage of vessels th rough den se bon e n ear th e skull base.
a pitch of m ore th an 1 creates a gap but results in faster scan n ing. Th e den sit y of th e in t ravascu lar con t rast is sim ilar to bon e, an d
W h en th ere are m u lt ip le d etectors, th e p rocessing is m ore com - the tort uosit y of th e vessels m akes them difficult to evaluate. This
plicated bu t th e p rin cip les are th e sam e. A volu m e equ al to th e issue can be addressed in several w ays. For exam ple, a precon -
length of th e detector ban k is acqu ired w ith each rot at ion , greatly t rast im age set can be obtain ed an d u sed for su bt ract ion or for
accelerat ing acqu isit ion of th e scan . m asking bon e, an alogous to DSA. Dual-en ergy CT scan s th at si-
Th ree factors con t ribu te to th e qu alit y of a CT scan : sp at ial m ultan eously create t w o im age sets, t ypically using 80 kVp an d
resolu t ion , con t rast resolu t ion , an d part ial-volu m e effect s. Many 140 kVp X-rays, can discr im in ate bet w een bon e an d con t rast
factors com bin e to d eter m in e t h e sp at ial resolu t ion in m u lt i- m aterial an d allow th e rem oval of bon e.10
d etector CT, in clu ding X-ray beam w id t h , d etector size, recon - Each p ost p rocessin g step is associated w it h lim it at ion s an d
st r u ct ion filter, m at rix, an d disp lay FOV. We can u se th e detector ar tifacts as w ell as w ith addit ion al radiat ion dose if a precon t rast
w idth to approxim ate th e th rough -plan e (along th e pat ien t axis) m ask sequen ce is acquired. Th e m ore processing th at takes place,

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184 II Evaluation and Treatment Considerations for Neurovascular Disease

t h e greater is t h e loss of in for m at ion an d p oten t ially t h e gen - Table 14.1 Representative Values for Effective Dose for Selected
erat ion of ar t ifact . Th u s, m u lt iplan ar reform at t ing is less affected Examinations in Adults and Children*
th an volum e ren dering an d MIP im ages. In volu m e-ren dering
Adult Child
im ages, focal calcifications can resem ble sm all aneurysm s; struc- Modality (mSv) (mSv)
t u res w it h in t h e vessel su ch as a d issect ion flap w ill n ot be
seen .11 In MIP im ages, sten oses are overest im ated, an d adjacen t CT brain 2.7 2
bon e calcium or en h an cem en t can be depicted as a vascu lar CT angiography brain 1.6 6
st ru ct u re. Becau se of th ese d ifferen ces, th e m eth ods sh ou ld be CT angiography neck 3.8 14
CT perfusion † 4.9 10
regarded as com p lem en tar y. In difficu lt cases, careful review of
Cerebral angiography 5‡ 10 ‡
th e source im ages can usu ally resolve th e u n cer tain t y.
*Adult values for CT examinations for 64-slice scanner50 ; adult value for
angiography51 ; child values.52
Risks Associated w ith Ionizing Radiation †Dose to the target organ (brain) exceeds 100 m Sv, which with repeated

examinations can lead to deterministic effects such as skin erythem a and possibly
High X-ray doses are kn ow n to be h azardou s. How ever, th e m ag- cognitive effect s.
n it u de of th e risks of exposure to low X-ray doses su ch as th ose ‡Average value; the range is quite large, depending on difficult y and operator

received du ring angiography an d CT angiograp hy is less clear. experience.


We are all exposed to n at u rally occu rring radiat ion on a daily Abbreviation: CT, computed tom ography

basis. Th e source of th is radiat ion is a com bin at ion of cosm ic


rays, terrest rial sou rces, an d ingested sou rces from decay of ra-
Th is d ose, m easu red in m Sv, reflect s t h e su m of t h e t issu e-
dioact ive isotop es n orm ally p resen t in food. In m ed ical im aging,
w eigh ted equivalen t doses for all (directly or in directly) irradi-
th e absorbed X-ray dose is u su ally rep or ted as th e equ ivalen t
ated organ s. Rep resen t at ive effect ive doses for variou s CT st u dies
dose (u n its of m illisiever t , m Sv). Th e equ ivalen t dose related to
are listed in Table 14.1.
the background radiation varies from place to place but is ~ 3 m Sv
Th e effect ive dose can be u sed in conju n ct ion w ith risk dat a
per year.
to est im ate risks—for exam ple, th e in duct ion of a fut ure can cer.
W h en su fficien tly en erget ic, rad iat ion can ion ize m at ter. In
How ever, several factors m ake th is est im ate im precise. Th e fac-
biological t issue, th is ion izat ion can lead to som at ic cell dam age
tors range from t h e u n cer t ain t y in low -dose ext rap olat ion to
at h igh en ough doses, term ed a determ in ist ic effect . It can also
issues related to age, w eigh t , sex, an d th e cum ulat ive effect of
resu lt in dam age to DNA, term ed a stoch ast ic or ran dom effect . If
exp osu re to m u lt iple st u dies. Even so, u sefu l gu idelin es h ave
th is dam age is n ot rep aired, it can lead to n eop lasia of som at ic
been publish ed.12 For exam ple, th e radiat ion -in duced can cer risk
cells an d can cause deleterious m utat ion s of gam ete gen om es,
related to a 10-m Sv exposu re for a 30-year-old w om an w ould be
poten t ially an d cu m u lat ively affect ing later gen erat ion s. Dat a re-
~ 0.1% (1/1000), w h ereas th e risk for a sim ilarly exposed in fan t
garding th e abilit y of radiat ion to in duce can cer in h um an s pri-
girl would be 5 tim es higher at ~ 0.5%. However, these data should
m arily com e from longit udin al st udies of su r vivors of th e atom ic
be com pared w ith th e lifet im e risk of developing a can cer, w h ich
bom b blasts (Life Span St udy) 12 for doses as low as 50 m Sv. From
is ~ 41%16 ; t h u s, t h e ad d ed r isk related to rad iat ion exp osu re
th ese dat a, est im ates of th e risk of d evelop ing solid can cers an d
in t h is exam p le is on ly an in crease of ~ 0.2% for t h e ad u lt . Fu r-
leu kem ia as w ell as th e risk of death from can cer can be derived .
t h er m ore, th is is a rough est im ate; th e addit ion al rad iat ion risk
How ever, for t h ese est im ates to be u sefu l at d oses w ell below
sh ou ld be com p ared w ith th e risk of develop ing a can cer in th e
50 m SV, assum pt ion s m u st be m ade, p rim arily regarding th e re-
fu t u re an d so is con dit ion al on th e pat ien t’s cu rren t age. Th e can -
lat ion sh ip of risk to dose at m edically im p or tan t (1 to 10 m Sv)
cer m or talit y rate for adult s is abou t h alf th e lifet im e risk of de-
doses. Most discu ssion s of risk are based on a lin ear ext rap ola-
veloping a can cer, an d th e sam e is t ru e for th e m or t alit y rate of
tion and involve a variet y of assum pt ion s. Despite the uncertaint y
radiat ion -in du ced can cers, so th e added risk percen t age of 0.2%
associated w ith th ese assum pt ion s, th e poten t ial for carcin oge-
is t rue for m or t alit y as w ell.
n icit y of radiat ion , specifically X-rays at en ergies an d doses used
Th e availabilit y of CT scan s is of en orm ou s diagn ost ic ben efit
in m edical diagn osis, is fairly w ell accepted, part icu larly regard-
to pat ien t s. W h en a scan is likely to provide im por t an t in form a-
ing its effect s in ch ildren .13
t ion th at can affect t reat m en t , th e risk of h arm to an in dividu al
Not su rp risingly, th e in cid en ce of can cers is age depen den t .
pat ien t is likely to be far ou t w eigh ed by th e ben efit . From th is
Ch ildren are sm aller an d so receive poten t ially larger p er kilo-
persp ect ive, th e can cer risk sh ou ld be view ed as an im por t an t
gram doses, an d th ey are m ore sen sit ive to a given dose becau se
pop u lat ion p roblem , reflect ing th e ver y large n u m ber of CTs per-
of act ive cell division . Ch ildren also h ave a longer fut ure life span
form ed each year. Ch ildren are at in creased risk, an d th us special
du ring w h ich to m an ifest can cers. Based on th ese con siderat ion s,
at ten t ion sh ou ld be p aid to scan n ing th em . We best ser ve th e
th e risk of can cer is exp ected to be dram at ically h igh er in in fan t s
in terests of ou r pat ien t s by elim in at ing u n n ecessar y scan s, lim it -
an d young ch ildren .14 Wom en , an d especially girls, are also at a
ing scan s to th e region of in terest , opt im izing scan protocols to
h igh er risk due to th e sen sit ivit y of breast an d ovarian t issue to
m in im ize dose, an d u sing altern at ive m odalit ies su ch as MR im -
radiat ion . Conversely, th e risk of radiat ion -in du ced can cer is re-
aging w h en possible.17
du ced in p at ien t s w ith a sh or ten ed expected life sp an related to
seriou s con dit ion s.
Modern CT scan n ers are opt im ized to lim it th e X-ray dose.
How ever, w ith th e rap idly in creasing u se of CT scan s, m edical
im aging has becom e an im portant source of radiation exposure.15
■ Magnetic Resonance Angiography
A dose m et ric kn ow n as th e effect ive dose can be com p u ted by W h en th e hydrogen atom s of w ater are p olarized in a st rong
sum m ing th e con tributions from each organ absorbing radiat ion . m agn et ic field, an d th is align m en t is th en pert urbed by a w eak

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14 Invasive and Noninvasive Imaging of the Vasculature 185

perpen dicu lar m agn et ic field, th e atom s p recess abou t th e direc- especially for a diseased vessel, th is issue represen ts a lim it at ion
t ion of th e m ain m agn et ic field like top s as th ey gradu ally spiral of the technique. Recent novel acquisition schem es have addressed
back in to align m en t . During th is rela xat ion , th e atom s (com - con cern s related to th e t im e-in ten sive n at u re of p h ase-con t rast
m on ly referred to as spin s) radiate en ergy as radiofrequen cies. MR angiography an d m ay open th e door to ap p licat ion s of qu an -
W h en th is sign al is collected, im ages of th e object con t ain ing th e t itat ive flow m easurem en t s.21
w ater can be form ed. Alth ough greatly oversim p lified, th is con - Both TOF an d especially p h ase-con t rast MR angiograph ic ac-
cept is th e basis of MR im aging.18 Th ere is a ch aracterist ic t im e qu isit ion s are t im e-in ten sive p rocesses. Th is lim it at ion an d oth -
for th e spin s to ret urn to align m en t along th e m ain m agn et ic ers are addressed w ith con t rast-en h an ced MR angiography. For
field , w h ich is kn ow n as T1. Becau se hyd rogen atom s in d iffer- th is ap proach , ver y rap id im aging is p erform ed du ring th e in t ra-
en t ch em ical environ m en t s p recess at differen t rates, th ere is a venou s adm in ist rat ion of a bolus of MR con t rast m aterial. Th is
gradu al loss of syn ch ron izat ion . Th is p rocess is ch aracterized by approach is essen t ially a lum en -opacificat ion tech n ique in th e
a secon d ch aracterist ic t im e, term ed T2. A t rain of per t urbing sp irit of CT angiography, but w ith th e ben efit of absen t in terfer-
m agn et ic fields or radiofrequ en cy pulses can be used to m an ipu- en ce from adjacen t bon e. On th e m in u s side, con t rast-en h an ced
late th e sp in s to ext ract in form at ion abou t differen t t issu es. An MR angiograp hy requ ires con t rast inject ion , w ith it s associated
am azing range of t issue proper t ies can be st udied by ch oosing cost s of t im e an d m on ey. Th ere are also sm all risks, ranging from
specifically designed sequences of pulses. In particular, sequences ext ravasat ion of con t rast m ater ial to an ap hylact ic react ion s. In
can be design ed th at are sen sit ive to flow, m aking MR angiogra- patients w ith im paired renal function, the gadolinium -based con-
phy possible. Th ere are m u lt iple w ays to im age flow u sing m ag- trast agents are also associated w ith the risk of a serious condit ion
n et ic reson an ce.19 kn ow n as n eph rogen ic system ic fibrosis.22
The techniques of MR angiography fall into three broad classes: Acqu isit ion of a p h ase-con t rast MR angiogram can be syn -
t im e of fligh t (TOF), p h ase con t rast (PC), an d con t rast en h an ced ch ron ized to t h e card iac cycle by gat in g, m akin g p ossible cin e
(CE). Each tech n ique in cludes m ult iple varian ts. Th e m ost com - MR angiograp hy, w h ich displays systolic an d diastolic ch anges in
m on ly em ployed tech n iques are TOF varian t s.20 Th ese m eth ods flow. How ever, th e acquisit ion takes several m in u tes, an d so t rue
are based on th e differen ce bet w een st at ion ar y tissu e an d flow - t im e-resolved im aging is n ot p ossible w ith th is tech n iqu e. On
ing blood. Un like st at ion ar y soft t issu es, th e sp in s of in flow ing th e oth er h an d, th e t im e requ ired to acqu ire con t rast-en h an ced
blood h ave n ot been su bject to prior m an ip u lat ion. Con sequ en tly, MR angiograp hy is n early fast en ough to resolve th e ar terial an d
th e flow ing blood app ears m u ch brigh ter in app rop riately de- venous phases of flow through the brain. To bridge the gap, m eth -
sign ed MR im aging sequ en ces, an d in form at ion regarding blood ods h ave been developed to reduce th e t im e requ ired to collect
vessels can be ext racted . Th e m ot ion of th e blood it self is respon - im ages.23 Typically, a m eth od kn ow n gen erically as keyh ole im -
sible for th e d etected sign al, a m ech an ism kn ow n as TOF con - aging is used . In th is ap proach , on ly som e of th e data collected
trast. Im ages can be form ed using thin (1.5 m m ) sequent ial slices, con t ain s th e in form at ion to con st ru ct fu ll-resolu t ion im ages.
kn ow n as t w o-d im en sion al (2D TOF), or u sing a t h icker (1 to Th ese fu ll-resolut ion im ages are u pdated periodically, an d th e
2 cm ) slab partitioned into thin slices, term ed three-dim ensional inform ation is shared to reconstruct the m ore frequent lower res-
(3D TOF). Th e 2D TOF m eth od is ch aracterized by m oderate reso- olut ion im ages. Doing so allow s vascular im ages to be acqu ired
lu t ion an d h igh sen sit ivit y to slow flow . It su ffers from an ar t i- ever y 1 to 2 secon ds w ith lin ear voxel dim en sion s of ~ 1 m m . Th e
fact associated w ith sign al loss in areas of disordered flow, for ad d it ion of an in it ial p recon t rast m ask allow s su bt ract ion of
exam ple, dist al to an irregu lar vascu lar sten osis or w ith in an an - backgroun d sign al.24 In an oth er in n ovat ive approach , HYPR-CE
eu r ysm . Th e 3D TOF varian t en ables h igh er resolu t ion an d less (an acronym for High lY con st rain ed back-PRoject ion Con t rast-
sen sit ivit y to disordered flow bu t su ffers from sign al loss in areas En han ced) MR angiography, the tem poral an d spatial inform ation
of slow flow. Because th e angiograph ic im ages are essen t ially T1 is acqu ired separately.25 In addit ion to an atom ic in form at ion ,
w eigh ted, st ruct ures th at are hyperin ten se on T1-w eigh ted im - th ese t im e-resolved, or fou r-dim en sion al, MR angiograp h ic (4D
aging, su ch as fat or blood, can m im ic th e ap p earan ce of flow. MRA) m et h ods provide physiological dat a regarding flow veloc-
It is possible to apply a m agn et ic field th at varies from poin t it y an d direct ion an d poten t ially diagn ost ic in form at ion related
to poin t . In such a field, th e spin s associated w ith flow ing blood to t im ing, such as th e appearan ce of an early drain ing vein . Th ese
exp erien ce a differen t am ou n t of precession per u n it of t im e dat a app roach th e in form at ion p rovided by DSA, albeit at low er
com p ared w ith stat ion ar y sp in s due to th eir m otion . Th is differ- sp at ial an d tem p oral resolu t ion .
en ce in p recession can be u sed to form im ages in w h ich vascu lar As w ith CT angiograp hy, im ages obt ain ed during MR angiog-
st r u ct u res ap p ear br igh t . Acqu isit ion s sen sit ive to flow an d a rap hy sequ en ces (sou rce im ages) are often d isp layed in or t h og-
com p arable sequ en ce w ith ou t flow sen sit ivit y are su bt racted, on al view s u sing m ult iplan ar reform ats or are post processed to
essen t ially elim in at ing backgrou n d sign al from soft t issu e. Th is produ ce project ion im ages sim ilar in app earan ce to angiogram s.
process form s th e basis of th e ph ase-con t rast MR angiograp hy Th ese p ost p rocessed im ages can be rot ated in teract ively an d
tech n ique.20 Un like TOF m eth ods, ph ase-con t rast MR angiogra- view ed at any desired angle, a defin ite advan t age. How ever, any
p hy allow s qu an t ificat ion of m agn it u d e an d d irect ion of flow . post p rocessing sch em e h as th e p oten t ial to in t rod u ce ar t ifact s,
To som e d egree, t h ese tech n iqu es su ffer from ar t ifact s related an d th e sou rce im ages rem ain useful in evaluat ing problem at ic
to disordered flow. In addit ion , to acquire a ph ase-con t rast MR cases.
angiogram , th e user m u st supply an est im ate of th e m axim um Th e st rength of th e m ain m agn et ic field in an MR scan n er
velocit y w ith in th e vessel of in terest , th e so-called en coding ve- determ ines the am oun t of signal available to create an im age. In -
locit y. If th e su p p lied valu e is too sm all, t h e sign al w it h in t h e creasing t h e st rengt h of th is m agn et ic field im p roves t h e sign al-
vessel w ill be ar t ifact ually low (aliasing ar t ifact). If th e en coding to-n oise rat io of th e im ages. Curren t clin ical scan n ers operate at
velocit y is too h igh , th e sen sit ivit y to slow flow w ill be reduced. eith er 1.5 or 3 tesla (T). Th e field st rength of exp erim en t al u n it s
Becau se th e u ser u sually can n ot p redict th e m axim u m velocit y, can be as h igh as 7 T. Doubling th e field st rength ap proxim ately

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186 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

Fig. 14.1a,b Maxim um intensit y projections of m agnetic resonance an- visualization of peripheral arteries, and bet ter background suppression
giogram s depicting a small paraophthalmic artery aneurysm at (a) 1.5 and than the 1.5-T image. (Courtesy of Barrow Neurological Institute.)
(b) 3 tesla (T). The 3-T image dem onstrates higher spatial resolution, bet ter

dou bles th e sign al-to-n oise rat io, allow ing h igh er resolu t ion or w it h dyn am ic su scept ibilit y con t rast -en h an ced p erfu sion MR
faster scan n ing, or som e of both . im aging (DSC P-MRI); h ow ever, qu an t ificat ion is m ore difficu lt
High er field st rength p rovides oth er ben efit s for MR angiogra- t h an w it h CT p er fu sion . Th e accu racy of t h ese st u d ies can be
phy.26 Becau se th e T1 relaxat ion t im e of st at ion ar y soft t issues is sen sit ive to im aging p aram eters as w ell as to p ost p rocessin g
prolonged at a h igh er field st rength , th ere is less recover y of lon - m eth ods.28
git udin al m agn et izat ion . Con sequ en tly, th ere is less sign al from
backgrou n d soft t issues com pared w ith vascular sign al for TOF
m et h od s (Fig. 14.1). For sim ilar reason s, t h e con sp icu it y of in -
t raven ou s con t rast m aterial is in creased at h igh er fields, lead ing ■ Applications
to im proved vascular con t rast-to-backgroun d rat ios. Th e h igh er
sign al-to-n oise rat ios at h igh field st rength also en able th e u se of Vascular Stenosis and Occlusion
specialized techniques such as parallel im aging, w hich can shorten
Both CT angiography an d MR angiography are sen sit ive for th e
scan tim es. However, artifacts associated w ith differences in m ag-
d etect ion of occlu sion of first - an d secon d -ord er bran ch es of
n et ic proper t ies bet w een air or bon e an d soft t issues (suscept i-
t h e in t racran ial vessels, alth ough false-posit ive readings of oc-
bilit y ar t ifact s) are accen t uated at h igh field st rength s an d can
clu sion can occu r in cases of ver y h igh -grad e sten osis. Moderate-
lead to a loss of vascu lar sign al n ear th e sku ll base. Overall, h igh er
to-severe focal sten osis can also be iden t ified, par t icularly in
field strength is favorable for MR angiography, especially for tim e-
larger, proxim al vessels. Accu racy for grading th e degree of ste-
resolved m eth ods.
n osis is ult im ately lim ited by th e spat ial resolu t ion of th e tech -
n ique. Fur th erm ore, TOF MR angiography ten ds to overest im ate
sten osis related to th e sign al loss th at is associated w ith disor-
dered flow w ithin and distal to the narrow ing. This tendency, how -
■ Perfusion Imaging ever, h as th e effect of in creasing th e sen sit ivit y of th is tech n iqu e,
Th e tech n iqu es described so far p rovide in form at ion regarding m aking it a useful feat ure in screen ing exam in at ion s. Calcifica-
m idsized to sm all vascular st ruct ures. Perfusion im aging adds t ion an d osseou s st r u ct u res n ear th e sku ll base can lead to over-
in form at ion regarding th e m icrovasculat u re. CT p erfu sion im ag- or u n derest im at ion of th e degree of sten osis on CT angiography,
ing is obt ain ed by repeated im aging du ring th e passage of a bolu s dep en ding on th e p ost processing tech n iqu es ap p lied . In CT angi-
of iodin ated con t rast . To ap p roach fu ll brain coverage, at least ograp hy, bon e-rem oval tech n iqu es ten d to be associated w ith an
256 detectors are required. By sam pling pu re ar terial an d ven ous overest im at ion of sten osis.29 In all cases, sou rce im ages are least
con t rast at ten u at ion , t h e p er fu sion valu es can be qu an t ified . affected. Perfusion im aging also h as an applicat ion in th is set-
Map s of p ixel-w ise cerebral blood flow, cerebral blood volu m e, t ing, par t icu larly in th e set t ing of st roke. CT angiograp hy is th e
and m ean transit tim e are generated.27 Sim ilar data regarding rel- best tech n ique for evaluat ing flow -lim it ing vasospasm of proxi-
at ive flow using an in t raven ous con t rast bolu s can be gen erated m al vessels, bu t CT perfu sion is also u sefu l. Neith er tech n iqu e is

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14 Invasive and Noninvasive Imaging of the Vasculature 187

reliable for im aging su btle n arrow ing, for exam ple, th at associ- Arterial Dissection
ated w ith vasculit is, so th is en t it y m ay ben efit from DSA.
Th e n on invasive an d less invasive m eth ods of im aging each h ave
Both CT angiograp hy an d MR angiography are usefu l for eval-
advan t ages for detect ing an d ch aracterizing ar terial dissect ion .33
u at ing sten osis involving th e cer vical carot id bifu rcat ion . Both
CT angiograp hy is m ore sen sit ive for d etect ing t h e su bt le vas-
m et h od s ten d to overest im ate t h e d egree of sten osis for t h e
cu lar con tour abn orm alit ies associated w ith in t im al or st retch
reason s m en t ion ed above. Because con t rast-en h an ced MR angi-
injur y. It is also easily obtain ed at th e t im e of an in it ial t raum a
ograp hy is less sen sit ive to flow -related sign al loss, it d oes n ot
evalu at ion an d is an appropriate screen ing exam in at ion for vas-
su ffer from t h is p it fall an d so is likely t h e m ost accu rate of t h e
cular injur y in an appropriate h igh -risk populat ion .34,35 A few
less invasive m eth od s.30 For screen ing or con fir m in g fin d in gs
days after on set , MR angiography an d MR im aging can dem on -
from Dop p ler u lt rason ograp hy, TOF is u su ally ad equ ate. Less
st rate su bacu te th rom bu s in a false lu m en , w h ich im p roves th e
invasive tech n iqu es are too in sen sit ive to d etect sm all u lcer-
specificit y of th e diagn osis (Fig. 14.3). CT angiography st u dies
at ion s. CT angiograp hy is u su ally p referable for evalu at ing ver-
can also be u sed to iden t ify m u ral h em atom as.36 Th e t w o m eth -
tebral sten osis, because th e sligh tly h igh er spat ial resolut ion
ods can both be obt ain ed in h igh -risk cases to com plem en t each
m ore accurately ch aracterizes n arrow ing in th ese sm all vessels.
oth er. Both CT angiography an d MR angiography are subject to
Con t rast-en h an ced MR angiography cou ld also be u sefu l for th is
several artifacts th at can sim ulate th e findings of dissection. Th us,
applicat ion .31
th ese st u dies m u st be in terpreted caut iou sly.37
Movin g beyon d lu m in al n ar row in g, p laqu e ch aracter izat ion
is an em erging tech n ology of great p rom ise. High -resolu t ion MR
im aging can visu alize th e ar terial w all at th e carot id bifu rcat ion
an d ch aracterize plaque com posit ion .32 CT angiograp hy can also
Venous Sinus Thrombosis
provide u sefu l in form at ion , par t icu larly regarding th e presen ce St an dard MR im agin g h as a h igh sen sit ivit y for su bacu te d u ral
of calcificat ion . sin u s t h rom bosis.38 From a few days u n t il 1 to 2 w eeks after
Both CT angiograp hy an d con t rast-en h an ced MR angiography on set , th e affected sin uses appear hyperin ten se on T1-w eigh ted
h ave been used for preprocedural assessm en t before sten t ing. im ages. Th e fin dings are m ore su btle during th e acute ph ase,
MR angiography su ffers from ar t ifact in th e region of m ost vas- w ith loss of the norm al flow void on T1-weighted im ages but con-
cular sten ts; h ow ever, CT angiography can be useful in evaluat- tin u ed ver y low sign al in ten sit y on T2-w eigh ted im ages, w h ich
ing th e paten cy of som e sten t t ypes (Fig. 14.2). m im ics flow. These im aging sequences are subject to flow -related

a b

Fig. 14.2a,b Multiplanar reform at from (a) computed tomography angiogram dem onstrates in-stent restenosis, which was confirm ed on (b) digital
subtraction angiogram . (Courtesy of Barrow Neurological Institute.)

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188 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig. 14.3a–c (a) Axial im age from computed tomogra-


phy angiogram shows irregularit y of the contour of the
left internal carotid artery, suggesting the presence of a
dissection. (b) Axial source im age from t wo-dimensional
tim e of flight (TOF) m agnetic resonance (MR) angiogra-
phy confirms abnorm al contour. (c) Axial T1-weighted MR
image demonstrates hyperintense throm bus in false lumen
lateral to a narrowed residual vessel lum en. (Courtesy of
Barrow Neurological Institute.)

ar t ifacts, w h ich decrease th eir sp ecificit y. Because of th e rela- provides good visualization of cortical veins. For the dural sinuses
t ively slow flow w ith in th e sin u ses, 2D TOF MR angiograp hy to be visualized opt im ally, a few addit ion al secon ds of delay are
w it h it s su p erior sen sit ivit y to slow flow is an excellen t n on in - added to the bolus tim ing during acquisition, a technique referred
vasive su p p lem en t (Fig. 14.4). How ever, t h e MR an giograp hy to as CT ven ography.
sequen ce suffers from sign al loss in sin uses cou rsing w ith in th e Bot h MR- an d CT-based m et h od s are su bject to im p or t an t
plan e of sect ion , t yp ically th e coron al p lan e. Th is affects th e dis- p it falls an d ar t ifacts.39 As m en t ion ed, flow -related sign al ch anges
tal su perior sagit t al an d t ran sverse sin u ses. Fur th erm ore, th e can confound th e interpretation of MR venography. Hyperintense
evalu at ion of sm all cor t ical vein s w ith th is tech n ique is su bopt i- th rom bus can m im ic flow on MR ven ography, alth ough th is is
m al. However, th e com bin at ion of th e im aging st udy an d 2D TOF less of a problem w hen using 2D TOF because of its excellent back-
MR angiograp hy provides an excellen t screen ing exam in at ion . At ground suppression. Sim ilarly, hyperdense throm bus or con t rast
som e cen ters, con t rast-en h an ced MR angiography or occasion - en h an cem en t of ch ron ic th rom bus cou ld poten t ially m im ic flow
ally ph ase-con t rast MR angiography is subst it uted for th e TOF on CT ven ography.
series, but th ese sequ en ces are associated w ith th eir ow n sh or t-
com ings. Con t rast-en h an ced MR angiography is a good ch oice
w h en isolated cor t ical vein th rom bosis is a diagn ost ic quest ion .
Cerebral Aneurysms
Com pu ted tom ograp hy angiograp hy is also sen sit ive for de- Less invasive an d n on invasive m eth ods are useful for th e detec-
tect ing throm bosis an d, like con t rast-en h an ced MR angiography, t ion of in t racran ial ber r y an eu r ysm s larger t h an ~ 3 m m .40 MR

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14 Invasive and Noninvasive Imaging of the Vasculature 189
Fig. 14.4a,b (a) Sagit tal T1-weighted m agnetic reso-
nance (MR) im age of the brain demonstrates hyperinten-
sit y within the dural sinuses due to subacute thrombosis.
(b) Maxim um intensit y projection of a t wo-dim ensional
tim e of flight MR venogram confirm s lack of blood flow
throughout m ost of the dural sinuses, with som e sparing
of the sigm oid sinuses. (Courtesy of Barrow Neurological
Institute.)

angiography is usually preferred for screening at-risk populations rospect ively in m ult iple plan es an d view ing angles. In difficu lt
an d for evaluat ing un r upt ured an eur ysm s. Th ree-tesla TOF MR cases, DSA m ay be n eeded, for exam p le, to dist ingu ish a sm all
angiography is par t icularly useful because of its h igh resolut ion an eur ysm from a vascular in fun dibulum . Conven t ion al angiog-
an d superior su ppression of backgroun d sign al. Flow -related sig- raphy also h as a role in fu rth er evaluat ion w h en less invasive
n al loss, likely related prim arily to stagn an t flow, can occur in st u dies are n egat ive. Exam p les in clu de evalu at ion for su barach -
larger an eu r ysm s. In th e set t ing of recen t su barach n oid h em or- n oid h em orrh age to exclu de an occu lt an eur ysm , su ch as a blis-
rh age, CT angiograp hy is th e p referred test becau se th e sh or t ter an eur ysm , as a sou rce.
scan t im e is best for th is crit ically ill p op u lat ion an d becau se of In postoperat ive pat ien t s after an eur ysm clipping, h elical-
th e su p erior con t rast resolu t ion of den se in t ravascu lar con t rast scan CT angiography sh ow s ar t ifacts, th e severit y of w h ich de-
in th e set t ing of adjacen t su barach n oid h em orrh age. With bon e pen ds on th e n u m ber, size, an d com posit ion of th e clips. Sm all
su bt ract ion or d u al-en ergy tech n iqu e, sen sit ivit y is h igh for all t itan iu m clip s are u su ally associated w ith m ild ar t ifact , an d CT
bu t th e sm allest an eu r ysm s. Ven ou s con t am in at ion , par t icularly angiography can iden t ify residual filling as sm all as 2 m m in th is
in th e cavern ou s sin u ses, can redu ce sen sit ivit y in th is region for set t ing (Fig. 14.5).41 MR angiography usually dem on st rates u n -
CT angiography an d con t rast-en h an ced MR angiography. Both acceptable art ifact related to suscept ibilit y. On th e oth er h an d,
CT angiography an d MR angiography dat a can be evaluated ret- aft e r e n d ovascu lar coilin g, CT an giograp h y is associat e d w it h

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190 II Evaluation and Treatment Considerations for Neurovascular Disease

a b

Fig. 14.5a,b Computed tomography angiograms show a small recurrent right m iddle cerebral artery aneurysm adjacent to a titanium clip in the (a) axial
and (b) sagit tal planes. (Courtesy of Barrow Neurological Institute.)

exten sive art ifact , bu t MR angiography can detect sm all residu al Vascular Malformations
or in terstit ial filling (Fig. 14.6).42 In th is app licat ion , TOF is u su -
ally adequate alth ough con t rast-en h an ced MR angiography is St an dard less invasive or n on invasive tech n iqu es can im age th e
occasion ally in form at ive. Flat-panel angiograph ic CT, also kn ow n n idus of cerebral ar terioven ous m alform at ion s an d are u sefu l for
as con e-beam CT angiograp hy, w ith in t raven ou s bolu s inject ion diagn osis an d staging. How ever, th ey are n ot sen sit ive for detect-
of con t rast h as been st u died to evaluate residu al after an eur ysm ing su btle m alform at ion s, especially fist u las. Fu rth erm ore, th ey
clip ping. Th is st udy, w h ich can be perform ed at th e com plet ion can n ot iden t ify early ven ou s filling becau se t im e resolu t ion is
of th e procedure in th e operat ing room , can dem on st rate resid- lacking. Th e t im e-resolved varian t s of MR angiograp hy an d CT
ual adjacen t to a single sm all clip. How ever, it s accuracy de- angiography can provide in form at ion related to t im ing an d are
creases in th e presen ce of m u lt iple or large clips.43 poten t ially u sefu l in th is set t ing, especially w h en perform ed at

Fig. 14.6a,b (a) Tim e of flight m agnetic resonance angiography shows a


sm all am ount of residual filling at the base of a left parophthalmic aneu-
rysm, confirmed by (b) angiography of the carotid artery in the lateral plane.
a (Courtesy of Barrow Neurological Institute.)

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14 Invasive and Noninvasive Imaging of the Vasculature 191

3 T. Evalu at ion of brain ar terioven ous m alform at ion s by 4D CT acterizing fist ulas, th e less invasive m eth ods sh ould be useful
angiography h as been repor ted w ith 0.5-m m isot ropic voxels du ring follow -u p of selected lesion s.
an d a tem p oral resolu t ion of 1 secon d, w ith an equ ivalen t radia- Magn et ic reson an ce im agin g an d MR an giograp hy are com -
t ion d ose of ~ 5 m Sv.44 Im provem en t s in tem poral resolu t ion m on ly u sed in ser ial follow -u p of lesion s after t reat m en t .
w ou ld en t ail h igh er doses of radiat ion . A st u dy evalu at ing 4D MR W h en a t reated n idu s resolves an d con t rast en h an cem en t
angiography w ith a voxel size of 1.1 × 1.4 × 1.1 m m an d a tem po- clears on conven t ion al MR im agin g, DSA is obt ain ed to con fir m
ral resolu t ion of 0.6 secon d fou n d sim ilar resu lt s.45 Both 4D MR obliterat ion .
angiography an d CT angiography can depict feeding ar teries an d
n idus an d can usually iden t ify drain age path w ays. Both st udies
rep or ted good cor relat ion w it h DSA for d eter m in at ion of t h e Spine
Sp et zler-Mar t in grad e in m ost cases; h ow ever, su bt le d eep ve- Im aging of spin al cord vascular lesion s is a ch allenge w ith less
n ou s drain age an d in t ran idal an eu r ysm s can be m issed w it h invasive m eth ods because of th eir sm all size an d com pact an at -
th ese m odalit ies. Th e h igh er resolu t ion an d film ing rate of DSA om y. How ever, MR angiograp hy 48 an d , to a lesser d egree, CT
are th us st ill n eeded for opt im al evalu at ion of com plex or subtle angiograp hy 49 are u sed as screen in g exam in at ion s for sp in al
lesion s. vascular lesions, par t icu larly spin al dural fist ulas. Neith er ex-
Historically, du ral ar terioven ou s fist u las (AVFs) have been d if- am in at ion is as sen sit ive as spin al angiography for th e detect ion
ficult to diagn ose w ith less invasive tech n iques. Tim e-resolved of sm all radicular feeding bran ch es, n or as specific as DSA in th e
m eth ods app ear to im p rove ch aracterizat ion . In on e st u dy, 4D ch aracter izat ion of t h e locat ion of t h e fist u la. Before DSA an d
MR angiograp hy w ith a voxel size of 1 × 1 × 1.5 m m an d a tem po- d efin it ive th erapy are pursued, 4D MR angiography is useful for
ral resolu t ion of ~ 2 secon ds dem on st rated fairly good agree- iden t ifying th e origin of th e ar ter y of Adam kiew icz.
m en t w ith DSA for ch aracterizing dural AVFs.46 A st u dy u sing 4D
CT angiography w ith an isot ropic 0.5-m m voxel dim en sion an d
1-secon d tem poral resolu t ion repor ted sim ilar results.47 Th e su -
perior sp at ial resolu t ion of th e CT-based m eth od is an advan t age,
alth ough th e lack of bon e sign al on MR angiography is desirable
■ Conclusion
because m any of th ese lesion s are n ear th e skull base. It is likely Th e availabilit y of so m any m odalit ies m akes it p ossible to
th at both m odalit ies w ill be in sen sit ive to ver y sm all arterial ch oose m et h od s t h at m in im ize r isk w h ile p rovid in g accu rate
feeders, and they m ay also be insensitive for the detection of low - and clinically useful results. In m any cases m ore than one choice is
volum e lesion s. Alth ough DSA is superior for detect ing and ch ar- possible. Table 14.2 lists suggestions for several clinical questions.

Table 14.2 Summary of Applications for Imaging Modalities

Modality Method Risk Application

MR angiography 2D TOF Noninvasive Carotid bifurcation screening


Intracranial venous sinus screening
3D TOF Noninvasive Carotid bifurcation screening
Cervical dissection evaluation
Intracranial arterial evaluation for aneurysm , stenosis
(3T preferred)
Aneurysm postcoiling evaluation
Phase contrast Noninvasive Quantitation of flow magnitude and direction
Contrast enhanced Less invasive Carotid bifurcation evaluation
Vertebral origin stenosis evaluation
CT angiography Multidetector Less invasive Acute stroke comprehensive evaluation
Aneurysm detection in the set ting of subarachnoid
hem orrhage
Evaluation for residual aneurysm after clipping
Cervical dissection evaluation
Evaluation of stent patency
MR angiography/CT angiography 4D Less invasive Techniques currently evolving
Potentially useful for evaluation and follow-up of
selected vascular lesions
Digital subtraction angiography Biplanar Invasive Resolution of problematic cases
Detection of subtle narrowing (vasculitis, mild
vasospasm)
Endovascular therapy
RA Invasive Evaluation of vascular anatomy, particularly in
complex regions and adjacent to aneurysms
Abbreviations: CT, computed tom ography; MR, magnetic resonance; RA, rotational angiography; TOF, time of flight.

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192 II Evaluation and Treatment Considerations for Neurovascular Disease

The pace of innovation in neurovascular im aging that began w ith angiography an d CT angiography are just a few of th e areas of
Mon iz an d h is first angiogram con t in u es. High er-field st rength act ive cu rren t research . Ju dging from prior experien ce, th e m ost
MR, faster m u lt idetector CT system s, m eth ods for red ucing radi- excit ing advan ces w ill likely com e from in n ovat ion s n ot yet even
at ion exposu re, an d n ovel p ost processing sch em es for both MR im agin ed.

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th eir p reven t ion . AJR Am J Roen tgen ol 2005;185,3:772-783 of t h e cer vical ar ter ial w all: w h at t h e rad iologist n eed s to kn ow . Rad io -
12. Hall EJ, Bren n er DJ. Can cer risks from diagnost ic radiology. Br J Radiol graph ics 2009;29:1413–1431
2008;81:362–378 33. Proven zale JM, Sarikaya B. Com p arison of test p erform an ce ch aracteris-
13. Kleinerm an RA. Cancer risks follow ing diagnostic and therapeutic radiation t ics of MRI, MR angiography, an d CT angiography in th e diagn osis of ca-
exposure in children. Pediatr Radiol 2006;36(Suppl 2):121–125 rot id an d vertebral arter y dissect ion : a review of the m edical literat ure.
14. Bren ner D, Elliston C, Hall E, Berdon W. Est im ated risks of radiat ion - AJR Am J Roen tgen ol 2009;193:1167–1174
in du ced fat al can cer from pediat ric CT. AJR Am J Roen tgen ol 2001;176: 34. Sliker CW. Blu n t cerebrovascu lar inju r ies: im aging w it h m u lt id etector
289–296 CT angiograp hy. Rad iograp h ics 2008;28:1689–1708, discu ssion 1709–
15. Bren n er DJ, Hall EJ. Com puted tom ography—an in creasing sou rce of radia- 1710
t ion exposure. N Engl J Med 2007;357:2277–2284 35. Steen bu rg SD, Sliker CW, Sh an m ugan ath an K, Siegel EL. Im aging evalu a-
16. Sur veillan ce, Epidem iology, an d En d Result s Program . Can cer St at ist ics tion of penetrat ing neck injuries. Radiographics 2010;30:869–886
Review. 1975–2009 (Vin t age 2009 Populat ion s). Beth esda, MD: Nat ion al 36. Lu m C, Ch akrabor t y S, Sch lossm ach er M, et al. Ver tebral ar ter y dissect ion
Can cer In st it u te; 2012 w ith a n orm al-appearing lum en at m ult isect ion CT angiography: th e im -
17. Bren n er DJ. Medical im aging in th e 21st cen t ur y—get t ing th e best bang por t an ce of iden t ifying w all h em atom a. AJNR Am J Neu roradiol 2009;30:
for th e rad. N Engl J Med 2010;362:943–945 787–792
18. Jacobs MA, Ibrahim TS, Ouw erkerk R. AAPM/RSNA physics t utorials for 37. Proven zale JM, Sarikaya B, Hacein -Bey L, Win term ark M. Cau ses of m isin -
residen t s: MR im aging: brief over view an d em erging applicat ion s. Radio- terp ret at ion of cross-sect ion al im aging st u d ies for dissect ion of th e cra-
graph ics 2007;27:1213–1229 niocer vical arteries. AJR Am J Roen tgen ol 2011;196:45–52
19. Ivancevic MK, Geer t s L, Weadock W J, Ch en ever t TL. Tech nical prin ciples 38. Poon CS, Ch ang JK, Sw arn kar A, Joh n son MH, Wasen ko J. Rad iologic diag-
of MR angiography m eth ods. Magn Reson Im aging Clin N Am 2009;17: nosis of cerebral ven ous th rom bosis: pictorial review. AJR Am J Roen t-
1–11 gen ol 2007;189(6, Suppl):S64–S75
20. Miyazaki M, Lee VS. Non en h an ced MR angiography. Radiology 2008;248: 39. Proven zale JM, Kran z PG. Du ral sin u s th rom bosis: sou rces of error in
20–43 im age in terpret at ion . AJR Am J Roen tgen ol 2011;196:23–31
21. Turk AS, Joh n son KM, Lu m D, et al. Physiologic an d an atom ic assessm en t 40. Hacein -Bey L, Proven zale JM. Curren t im aging assessm en t an d t reat m en t
of a can in e carot id ar ter y stenosis m odel ut ilizing ph ase con t rast w ith of in t racran ial an eur ysm s. AJR Am J Roen tgen ol 2011;196:32–44
vastly u n dersam p led isot ropic p roject ion im aging. AJNR Am J Neu roradiol 41. Zach en h ofer I, Cejn a M, Sch u ster A, Don at M, Roessler K. Im age qu alit y
2007;28:111–115 and ar tefact gen erat ion post-cerebral an eur ysm clipping using a 64-row

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14 Invasive and Noninvasive Imaging of the Vasculature 193

m u lt islice com p u ter tom ograp hy an giograp hy (MSCTA) tech n ology: a 47. Willem s PW, Brouw er PA, Barfet t JJ, terBrugge KG, Krings T. Detect ion and
ret rospect ive st u dy an d review of th e literat ure. Clin Neurol Neurosurg classificat ion of cran ial dural ar terioven ous fist ulas using 4D- CT angiog-
2010;112:386–391 raphy: in it ial experien ce. AJNR Am J Neuroradiol 2011;32:49–53
42. Schaafsm a JD, Velthuis BK, Majoie CB, et al. Intracranial aneur ysm s treated 48. Backes W H, Nijen h uis RJ. Advan ces in spin al cord MR angiography. AJNR
w ith coil placem en t: test ch aracterist ics of follow -u p MR angiography— Am J Neuroradiol 2008;29:619–631
m ult icen ter st u dy. Radiology 2010;256:209–218 49. Yam agu ch i S, Nagayam a T, Egu ch i K, Takeda M, Ar it a K, Ku r isu K. Accu -
43. Psych ogios MN, Wach ter D, Moh r A, et al. Feasibilit y of flat pan el angio- racy an d pitfalls of m u lt idetector-row com pu ted tom ography in detect-
grap h ic CT after in t raven ou s con t rast agen t ap p licat ion in th e p ostop era- ing spin al dural arterioven ous fist ulas. J Neurosu rg Spin e 2010;12:243–
tive evaluation of patients w ith clipped aneur ysm s. AJNR Am J Neuroradiol 248
2011;32:1956–1962 50. Mnyu siw alla A, Aviv RI, Sym on s SP. Radiat ion dose from m ult idetector
44. Willem s PW, Taesh in eet an akul P, Sch en k B, Brouw er PA, Terbrugge KG, row CT im aging for acute stroke. Neuroradiology 2009;51:635–640
Kr ings T. Th e u se of 4D- CTA in t h e d iagn ost ic w ork-u p of brain ar terio - 51. Met tler FA Jr, Huda W, Yosh izum i TT, Mah esh M. Effect ive doses in radiol-
ven ous m alform at ion s. Neuroradiology 2012;54:123–131 ogy an d diagn ost ic n u clear m edicin e: a cat alog. Radiology 2008;248:254–
45. Hadizadeh DR, Gieseke J, Beck G, et al. View -sh aring in keyh ole im aging: 263
Par t ially com pressed cen t ral k-space acqu isit ion in t im e-resolved MRA at 52. Raelson CA, Kanal KM, Vavilala MS, et al. Radiat ion dose an d excess risk of
3.0 T. Eu r J Radiol 2011;80:400–406 can cer in ch ildren un dergoing n euroangiography. AJR Am J Roen tgen ol
46. Nish im ura S, Hirai T, Sasao A, et al. Evaluat ion of dural ar terioven ou s fis- 2009;193:1621–1628
t ulas w ith 4D cont rast-en h an ced MR angiography at 3T. AJNR Am J Neu-
roradiol 2010;31:80–85

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15 Applications of Indocyanine
Green Video Angiography in
Neurovascular Surgery
Jack y T. Yeung, M. Yashar S. Kalani, and Peter Nak aji

Main t ain ing t issu e perfu sion is th e m ost essen t ial asp ect in n eu - h ealthy pat ien ts is 18 to 24%per m in ute. No m ore th an 4%of th e
rovascu lar su rger y. Neu rosu rgeon s visu ally in sp ect vessel p a- in it ial con cen t rat ion sh ou ld be p resen t 20 m in u tes after in t rave-
ten cy w ith th e aid of an operat ing m icroscope during operat ion s. n ous inject ion of th e dye. Th e recom m en ded dose of ICG dye for
How ever, it is difficu lt to con firm th e com p lete obliterat ion of an videoangiography is 0.2 to 0.5 m g/kg, an d th e daily dose of dye
an eur ysm , th e occlusion of a dural fist ula, th e in tegrit y of a par- injected sh ou ld n ot exceed 5 m g/kg.3
en t or perforat ing vessel, or th e p aten cy of a bypass graft by sim -
ple visu al in sp ect ion . Alth ough in t ra- an d p ostoperat ive d igit al
su bt ract ion angiography (DSA), th e gold st an dard for assessm en t
in n eu rovascu lar proced u res, en ables th e visu alizat ion of vessel ■ History
paten cy, it requ ires m u ch t im e an d m obilizat ion of resources.
In docyan in e green dye w as in it ially approved by th e Food an d
The use of intraoperative indocyanine green (ICG) dye is a revolu-
Drug Adm in ist rat ion in 1959 to evaluate cardiocircu lator y an d
tion in n eu rovascu lar su rger y as it en ables in t raoperat ive visu al-
liver fun ct ion s. Begin n ing in 1969, ICG w as also used in research
izat ion of vessel p aten cy. Its in tegrat ion w ith a su itably equ ipped
on an d diagn osis of subret in al processes in th e eye.4 It is w idely
m icroscope precludes th e n eed to m ove th e m icroscope ou t of
u sed by p last ic surgeon s for in t raoperat ive evalu at ion of flap
th e field or p erform any m an ip u lat ion . Th is ch apter p rovides
perfu sion an d by abdom in al su rgeon s for assessm en t of blood
backgrou n d on th e biological prin ciples of ICG dye, an d discusses
flow d u r in g an astom osis p roced u res. Th e u se of ICG dye as a
th e m eth odology of it s in t raop erat ive u ses an d cu rren t ap p lica-
n on invasive m et h od of st u dyin g cerebral h em odyn am ics w as
t ion s in t reat ing various n eu rovascular disorders.
invest igated by Hongo et al5 in 1995. In t raoperat ive m icroscope-
based ICG vid eo angiograp hy (ICG-VA) w as first in t rod u ced by
Raabe et al6 in 2003 for th e clip p ing of in t racran ial an eu r ysm s.
A subsequen t st udy by th e sam e au th ors com pared th e fin dings
■ Pharmacology of Indocyanine of ICG-VA w ith in t ra- or postoperat ive DSA an d con cluded th at
Green Dye ICG-VA is com p arable to DSA in 90% of cases.3 Sin ce t h en , t h e
set t ings of ICG-VA h ave expan ded to ext racran ial-to-in t racran ial
Indocyanin e green (C43 H47 N2 NaO6 S2 ) dye is a w ater-soluble, near-
(EC–IC) bypass,7 ext racran ial ver tebral ar ter y surger y,8 cort ical
in frared (NIR) fluorescen t t ricarbocyan in e dye (Fig. 15.1). It h as
perfusion m easu rem en ts du ring h em icran iectom y,9 cerebral ar-
a peak spect ral absorpt ion at 800 nm an d h as peak em ission at
terioven ous m alform at ion (AVM),10 an d in t racran ial11 an d spin al
835 n m , a range w h ere absorpt ion due to en dogen ou s ch rom o-
du ral ar terioven ous fist ula (DAVF).12
p h ores is low . Follow ing in t raven ou s inject ion , 95% of ICG is
rap id ly bou n d to p lasm a albu m in . It u n d ergoes n o sign ifican t
ext rah ep at ic or en teroh apt ic circu lat ion . Th e dye is m ostly in er t
in th e h u m an body, as th ere is n egligible ren al, p eriph eral, lu ng,
or cerebrospin al u ptake of th e dye. Th e dye is taken up exclu- ■ Methodology
sively by h epat ic paren chym al cells an d secreted in to bile, a ch ar- Microscope Integration of the Near-Infrared
acterist ic th at m akes it u sefu l in assessing h epat ic fun ct ion .
Technology
Th e dye prep arat ion con t ain s n o m ore th an 5% of sodiu m io-
dide, bu t it sh ou ld be u sed w ith cau t ion in p at ien t s w h o h ave an Carl Zeiss Co. (Oberkoch en , Germ any) in tegrated th e m icroscop e
allergic h istor y to iodides. An aphylact ic an d u r t icarial react ion s w ith ICG videoangiography technology. The system integrates NIR
h ave been rep or ted in p at ien t s w ith ou t kn ow n allergic h istor y im aging in to th e su rgical m icroscop e to obt ain h igh -resolut ion
to iodides. Th e rates of adverse reaction s are com parable to th ose and high-contrast NIR im ages.13 A specially designed dielectric fil-
of oth er con t rast m edia, ranging from 0.05% to 0.2%.1,2 ICG dye is ter for excitat ion of th e flu orescen ce en ables th e p assage of ligh t
a pregn an cy categor y C drug as n o an im al st u dies h ave been con - in the NIR w avelength that exactly fits the absorption band of ICG.
du cted; it sh ou ld be u sed in p regn an t w om en on ly if th ere are A beam split ter in th e m icroscope directs th e ICG fluorescen ce
st rong clin ical in dicat ion s. ligh t tow ard a black-an d-w h ite cam era. An obser vat ion ban d-
Heparin p reparat ion s con tain ing sodiu m bisu lfate m ay re- pass filter w as u sed to detect th e ICG flu orescen ce. Th is set u p
du ce th e absorpt ion peak of ICG in blood. Th e h alf-life of ICG dye facilitates th e visualizat ion of high -resolut ion NIR im ages based
is 2.5 to 3.0 m inutes. The percent disappearance rate of ICG dye in on ICG flu orescen ce w ith ou t the in fluen ce of am bien t ligh t .

194

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15 Indocyanine Green Video Angiography in Neurovascular Surgery 195
- O cran ial an eu r ysm s. Th ey rep or ted excellen t im age qu alit y an d
O resolut ion , en abling in t raoperat ive real-t im e assessm en t of th e
S cerebral circulat ion . Th e set up t im e ranged from 1 to 3 m in utes,
O an d th e t im e required for invest igat ion an d in terpret at ion ranged
from 30 to 40 secon d s. Ar terial, cap illar y, an d ven ou s p h ases
cou ld be differen t iated from on e an oth er, sim ilar to obser vat ion s
m ade w ith DSA. More im portantly, sm all and perforating arteries
(< 0.5 m m ) could be visualized. Th is sem in al repor t w as th e first
to n ote th at postoperat ive angiograph ic resu lt s correspon ded to
N th e in t raoperat ive ICG-VA fin dings. Th e u t ilizat ion of ICG-VA in
th eir series sign ifican tly ch anged th e cou rse of th e su rgical p ro-
cedu re in th ree of 12 p at ien ts.
CH3 Th e u se of ICG-VA w as fu r t h er evalu ated p rosp ect ively, in
H 3C
w h ich 124 an eu r ysm s in 114 p at ien t s w ere clip p ed .3 Th e p a-
ten cy of p aren t , bran ch ing, an d p er forat ing ar ter ies an d clip
+ occlu sion of th e an eur ysm as sh ow n by ICG-VA w ere com pared
Na w ith in t raoperat ive or postoperat ive fin dings from DSA. Th e re-
sults of ICG-VA corresponded w ith intra- or postoperative DSA in
90% of cases. Intriguingly, it w as confirm ed that ICG-VA allow ed
blood flow to be assessed in sm all vessels, even those w ith a sub-
H 3C O m illim eter diam eter (Fig. 15.2).
+ -
N O
H 3C S
Advantages of ICG-VA Compared w ith DSA
O
Th e u t ilizat ion of t h e in t raop erat ive ICG-VA tech n iqu e vast ly
im proved th e sim plicit y an d decreased th e t im e by w h ich th e
procedu re can be accom plish ed. Th e decreased t im e lapse be-
t w een clip assessm en t an d clip reposit ion ing en ables th e n eu ro-
su rgeon to act im m ed iately to rem ove or cor rect th e p osit ion
Fig. 15.1 Chem ical structure of indocyanine green. of an an eu r ysm clip before cr it ical cerebral isch em ia can occu r.
ICG-VA p rovid es h igh sp at ial resolu t ion com p ared w it h t rad i-
t ion al DSA. Even in com p lex cases t h at requ ire in t raop erat ive
DSA, ICG-VA m ay st ill be used as an adjun ct to ch eck th e paten cy
Intraoperative Application
of perforat ing vessels th at can n ot be assessed using in traopera-
Th e op erat ive field is illu m in ated by a ligh t sou rce t h at h as a t ive DSA. In t raop erat ive DSA requ ires an experien ced team an d a
w avelen gt h cover in g p ar t of t h e ICG absor pt ion ban d (range m in im u m of 20 m in utes to perform th e procedure, w h ich m ay
700–850 n m , m axim um 805 n m ).3 A stan dard 25-m g dose is exceed th e isch em ic lim it in m ore com plex cases.14 Clip readjust-
prep ared by dissolving in 5 m L of w ater. ICG dye is adm in istered m en t for th e occlu ded vessels after seeing t h e in t raoperat ive DSA
as a bolus inject ion in to a periph eral vein . Th e recom m en ded w as associated w it h a 33% rate of st roke.15 Th e t im e saved by
dose of ICG-VA is 0.2 to 0.5 m g/kg. We u se a st an dard d ose of u sing ICG-VA sh ould th eoret ically lead to decreased in ciden ces
25 m g/inject ion for all p at ien ts at Barrow Neurological In st it u te. of cerebral isch em ia during in t raoperat ive assessm en t .
A repeat dose can be adm in istered 10 m in utes after th e prior
dose or u n t il th e residu al flu orescen ce clears. After th e dye solu -
Disadvantages of ICG-VA Compared w ith DSA
t ion arrives in th e vessels of in terest , ICG flu orescen ce is in du ced.
Th e flu orescen ce (range 780–950 n m , m a xim u m 835 n m ) is re- In docyan in e green video angiography is rest ricted by th e opera-
corded by a n on -in ten sified video cam era. An opt ical filter blocks t ive field covered by th e su rgical m icroscope. Its u t ilit y is con -
both am bien t an d excit at ion ligh t so th at on ly ICG-in duced fluo- fin ed to m ore superficial vessels th at can be visually assessed by
rescen ce is collected. Ar terial, cap illar y, an d ven ou s angiograph ic th e n eu rosu rgeon . Any vessel covered by blood clot s, an eu r ysm ,
im ages can be obser ved on any video screen in real-t im e. or brain t issue can n ot be obser ved using th is tech n ique.16 Th ere-
fore, on e sh ould be suspicious of an in com plete occlusion an d
residu al filling of th e an eur ysm sac w h en th ere is slow filling of
th e con t rast m aterial. W h ereas DSA can reveal sluggish filling of
■ Applications in Intracranial distal vessels, h em odyn am ically relevan t sten osis after clip p ing
Vascular Lesions can be m issed by ICG-VA. In th e st u dy by Raabe et al,3 ICG-VA
m issed m ild but h em odyn am ically irrelevan t sten osis that w as
Aneurysms
eviden t on DSA in 7.3% of cases. Th ree cases (on e h em odyn am i-
Th e first ap p licat ion of in t raop erat ive m icroscop e-in tegrated cally relevan t sten osis an d t w o residu al an eu r ysm n ecks [2.7%of
ICG-VA w as m ain ly for clip p ing in t racran ial an eu r ysm s, as d e- cases]) w ith angiographically relevan t findings w ere m issed using
scr ibed by Raabe et al,6 w h o exam in ed 12 p at ien t s w it h in t ra- ICG-VA. In on e of th ese th ree cases, a 4-m m residual n eck m igh t

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196 II Evaluation and Treatment Considerations for Neurovascular Disease

Fig . 15.2a,b Application of indocyanine green video


angiography (ICG-VA) in intracranial aneurysm clipping.
(a) The aneurysm is highlighted along with the feeding
artery and draining vein after ICG was injected intrave-
nously. (b) ICG-VA indicated the cessation of blood flow
into the aneurysm al sac after clipping and maintenance of
blood flow through the sm all, perforating arteries. (Used
with perm ission from Barrow Neurological Institute.)

h ave required a secon d procedure. Neck residuals beh in d an eu - rh age from th e AVM.19 Th e u se of in t raoperat ive DSA h as been
r ysm s are difficult to detect w ith ICG-VA.17 Mer y et al18 rep or ted w ell establish ed for iden t ificat ion of th e AVM n idus an d com -
that after aneur ysm clipping in t w o patien ts, even though ICG-VA plete excision .20,21 Sim ilar to th e case of in t racran ial an eur ysm
sh ow ed absen ce of resid u al filling, slow dye ext ravasat ion w as clipp ing, th e u se of DSA in creases op erat ing t im e an d requ ires
fou n d after in cising th e an eur ysm dom e. In deed, false-n egat ive th e ext rapolat ion of in form at ion of th e DSA back to th e su rgical
fin d in gs w ere associated w it h u p to 9% of an eu r ysm s.3 Calci- field . Fu r th erm ore, it h as been rep or ted th at 3.7 to 27.3% of in -
ficat ion s an d t h ick-w alled at h erosclerot ic vessels or p ar t ially/ t raoperat ive DSA scan s sh ow un exp ected residual AVM.22,23
com p letely th rom bosed an eu r ysm s m ay obscu re th e sign al in In a prospect ive st udy by Killor y et al,10 ICG-VA w as u t ilized
ICG-VA. In th ese cases, in t raoperat ive DSA rem ain s th e m eth od for AVM resect ion in 10 pat ien t s. In eigh t pat ien t s, it h elped to
of ch oice for su ch cases an d for com plex or gian t an eur ysm s w ith d ist ingu ish AVM vessels. In t h ree of fou r pat ien t s u n d ergoing
ICG-VA as an adjun ct for visu alizing sm all, p erforat ing vessels. a post resect ion inject ion , ICG-VA sh ow ed no residual ar teriove-
n ous sh un t ing.10 Conversely, in t raoperat ive DSA sh ow ed residual
AVM in t w o pat ien t s requiring fu rth er resect ion of AVM n ot vi-
Arteriovenous Malformations su alized by ICG-VA d u r ing su rger y. ICG-VA cou ld id en t ify ar te-
Alt h ough th ere h ave been m ajor advan ces in p reop erat ive em - r ioven ou s sh u n t ing an d h elped th e su rgeon to d iscern th e AVM
bolizat ion , im age gu idan ce, an d in t raop erat ive m on itoring, in - ar ter ies, d rain ing vein s, an d cor t ical vein s based on t h e t im ing
t racran ial AVMs in eloqu en t areas rem ain ch allen gin g for n eu - of flu orescen ce w ith th e dye. An oth er st udy by Hänggi et al24 in
rosu rgeon s. Microsu rgical excision of th ese lesion s is th e on ly 2010 provided con sisten t fin dings in 15 AVM pat ien t s, an d n oted
t reat m en t opt ion th at im m ediately elim in ates th e risk of h em or- th at ICG-VA detect ion of residu al sh un t flow in to m ajor drain ing

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15 Indocyanine Green Video Angiography in Neurovascular Surgery 197
Fig . 15.3a,b Application of indocyanine green video
angiography (ICG-VA) in intracranial arteriovenous malfor-
m ation (AVM) obliteration. (a) The AVM nidus was high-
lighted after ICG was injected intravenously. (b) The AVM
was obliterated along with the feeding arteries. (Used with
perm ission from Barrow Neurological Institute.)

vein s resulted in fur th er resect ion . Fig. 15.3 illu st rates a case of giving th e surgeon m ore con fiden ce in resect ing AVM arteries
AVM resect ion using ICG-VA. w h ile p reser ving drain ing vein s.

Advantages of ICG-VA Compared w ith DSA Disadvantages of ICG-VA Compared w ith DSA
Th e in tegrat ion of ICG im aging w ith th e op erat ive m icroscop e Th e u t ilit y of ICG-VA is lim ited in d eep -seated AVMs becau se
h as m ad e acqu ir ing in for m at ion m ore st ream lin ed w it h m in i- th eir locat ion s requ ire long an d n arrow corridors for exp osu re
m al logist ic ch anges in th e operat ing room . As ICG flu orescen ce an d th e n idus can be obscured by blood clots an d brain t issue.10
clears rapidly, m u lt iple inject ion s can be p erform ed th rough ou t Ath erosclerot ic an d calcified vessels also obscure th e resu lt s of
th e op erat ion to h elp gu ide AVM resect ion . It s safet y is also w ell ICG-VA. In th ese cases, in t raop erat ive DSA rem ain s th e gold st an -
est ablish ed w ith ou t any m ajor inject ion -related m orbidit y or dard in t raoperat ive im aging tool, w ith ICG-VA being a useful ad-
m or talit y repor ted .10 jun ct for assessing sm all, perforat ing vessels.
Th e m ajor advan t age of ICG-VA is th at th e acqu ired in form a-
t ion is im m ediately in tegrated in to th e su rgical view. Th e tech -
Dural Arteriovenous Fistulas
n ique is ideal for early iden t ificat ion of AVM ar teries an d vein s,
h elping th e surgeon to decide th e course an d exten t of resect ion . Alth ough m ost in t racran ial DAVFs could be t reated by en dovas-
Th e in form at ion can poten t ially m ake su rger y safer an d faster, cu lar obliterat ion , som e st ill requ ire op en su rgical t reat m en t

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198 II Evaluation and Treatment Considerations for Neurovascular Disease

because of anatom ic constraints.25 Surgical m anagem ent of intra- sels du ring m icrosu rger y m ay h ave u t ilit y in t u m or resect ion by
cran ial DAVFs is supplem en ted by direct visu alizat ion un der an iden t ifying t u m oral an d perit u m oral exposed vessels. Ar terial,
operat ing m icroscop e, m icrovascular Doppler son ograp hy,26 an d cap illar y, an d ven ou s ph ase cou ld be recogn ized in all cases.35,36
in t raoperat ive DSA.27 Th e in t roduct ion of ICG-VA in to n eurovas- Th e ICG t ran sit t im e in t u m oral vessels w as fou n d to be n orm al
cular surger y h as prom pted th e st u dy of th is m odalit y in th e sur- or sh or ten ed such as in cases of m align an t t um or.37 A sh or t flow -
gical t reat m en t of DAVFs. In th e largest pu blish ed series to date, t im e, du e to path ological low -resistan ce vessels th at resu lts in
Sch u et te et al11 u t ilized ICG-VA in 13 p at ien t s w ith in t racran ial ar terioven ous sh un t ing, w as foun d to be com m on in h igh -grade
DAVFs, an d ICG-VA dem on st rated th e fist ula w ith precision an d gliom as, as is th e presen ce of n eovascular arch itectu re, dysplas-
docu m en ted it s obliterat ion in each case. How ever, th e au th ors t ic vessels, an d th rom bosed vein s.37 ICG-VA m igh t perm it bet ter
n oted th at it is im por t an t to fully expose th e en t ire ven ou s drain - assessm en t of th e p erit u m oral vessels an d, especially, th e drain -
age of th e fist u la; for exam p le, in on e of th eir p at ien ts w ith an ing vein s post resect ion .36 How ever, th e u se of ICG-VA is st ill in it s
an terior fossa DAVF w ith bilateral ven ous drain age, ICG-VA could in fan cy an d it s efficacy in im proving pat ien t outcom e in in t ra-
h ave been m isleading if th e falx h ad n ot been open ed.11 cran ial t u m or resect ion rem ain s to be d eterm in ed.
In vivo NIR laser con focal en dom icroscopy w ith ICG is cur-
ren tly being st udied to delin eate invasive t u m or m argin s in m ac-
Extracranial to Intracranial Bypass roscopically n orm al-app earing t issue, w h ile preser ving n orm al
Cerebral revascu larizat ion h as a m ajor role in t reat ing com plex brain t issue.38 In m ice injected w ith GL261-lu c cells, NIR con focal
in t racran ial an eu r ysm s,28–31 m oyam oya disease,32 an d oth er dis- en d om icroscopy w as perform ed u sing ICG, an d it revealed in di-
orders cau sing cerebral isch em ia.7,33 A key factor in en suring a vidual t u m or cells an d satellites w ith in p erit um oral t issue w ith
su ccessfu l EC–IC byp ass is th e in t raoperat ive evalu at ion of graft st riking h istological defin it ion . In vivo ICG im aging cou ld allow
paten cy. In t raoperat ive DSA is th e gold st an dard for assessing iden t ificat ion of m icroscopic m argin s of t u m or cell in filt rat ion ,
graft paten cy.34 How ever, oth er m odalit ies, such as u lt rason og- su bstan t ially im p roving in t raoperat ive d ecision s.38 Th e efficacy
raphy an d th erm al ar ter y im aging, h ave been p reviou sly used of th is m odalit y w ill n eed to be evaluated in a clin ical t rial.
w ith im aging lim it at ion s.7
Th e reliabilit y of ICG-VA in detect ing sten osis an d n on fu n c-
t ion ing byp asses h as already been rep or ted.7,29 It s usefuln ess h as
been show n in superficial tem poral arter y (STA)–m iddle cerebral
ar ter y (MCA) byp ass su rger y, STA–p osterior cerebral ar ter y by-
■ Applications in Spinal
pass, and saphenous vein high-flow bypass surgery.7 The findings Vascular Lesions
from ICG-VA correlated w ith p ostoperat ive DSA an d com p u ted
Spinal Arteriovenous Malformation
tom ograp hy (CT) angiography.29 Th e p aten cy rate of EC–IC by-
pass h as been rep or ted to reach 100% w ith th e u se of ICG-VA.7 At Barrow Neurological In st it ute, th e auth ors h ave begu n in cor-
Overall, ICG-VA is a u sefu l m odalit y in assessing vessel paten cy porat ing ICG-VA in to th e t reat m en t of sp in al AVM to h elp iden -
in t raoperat ively (Fig. 15.4). t ify feeding ar teries, AVM n idu s, an d drain ing vein s. Th e con cept
for ICG-VA in such surgeries is iden t ical to th at in in t racran ial
AVM resection. The goal of using ICG-VA is to m axim ize the resec-
Intracranial Tumors tion of AVM ar teries w h ile preser ving drain ing vein s. Curren tly,
Alth ough th e use of ICG-VA h as focused prim arily on vascular its u se as an adju n ct to DSA is being st u died an d it s efficacy re-
lesion s, its fu n ct ion in m on itoring blood flow in th e exp osed ves- m ain s to be determ in ed.

Fig. 15.4 Application of indocyanine green video angi-


ography (ICG-VA) in superficial temporal artery–m iddle
cerebral artery bypass. ICG-VA indicates patency of the
bypass. (Used with perm ission from Barrow Neurological
Institute.)

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15 Indocyanine Green Video Angiography in Neurovascular Surgery 199
Fig. 15.5a,b Application of indocyanine green video an-
giography (ICG-VA) in spinal dural arteriovenous fistula
(DAVF) obliteration. (a) ICG-VA was used to assess the ab-
norm al blood flow through the DAVF. (b) ICG-VA indicates
complete obliteration of the DAVF. (Used with perm ission
from Barrow Neurological Institute.)

Spinal Arteriovenous Fistula ■ Conclusion


Sim ilar to th e u se of ICG-VA in t racran ially, ICG-VA also can be In docyan in e green video angiography is a valuable tool in n euro-
u sed in th e t reat m en t of sp in al DAVF to assist w ith iden t ificat ion vascu lar surger y due to its in tegrat ion w ith th e surgical m icro-
of the fistula site and potential involvem ent of adjacent levels and scope th at en ables im m ediate feedback to th e su rgical field an d
to assess discon n ect ion (Fig. 15.5). Even w ith th e preoperat ive sen sit ivit y to sm all, p erforat ing vessels. Th e overall safet y of ICG
gold-stan dard DSA, in t raoperat ive an alysis by th e n eurosurgeon is w ell est ablish ed, w ith n o m ajor adverse react ion s reported. It
is n eeded to iden t ify th e locat ion of a fist u la an d it s feeding ar- h as been sh ow n to correlate w ell w ith in t ra- an d postoperat ive
teries and drain ing veins.12 Identification of true draining veins is DSA for in t racran ial an eu r ysm clipping an d AVM resect ion s. Its
crit ical because in adver tent ven ou s sacrifice w ith out discon n ec- lim it at ion s occur in cases w h ere a vascu lar lesion is deep w ith in
t ion of th e fist u la can lead to cat ast roph ic con sequen ces. ICG-VA th e brain or is obscu red by overlying blood clot or brain t issu e.
h as been sh ow n to be a u sefu l adju n ct in t h e su rgical m an age- Th e early dat a for ICG-VA in th e m icrosu rgical t reat m en t of in t ra-
m en t of DAVFs for localizat ion an d con fir m at ion of com p lete cran ial an d spin al DAVFs are prom ising but w ill n eed to be fur-
obliterat ion .11,12,39,40 In a series by Han el et al,12 ICG-VA h elp ed to th er st u died to evalu ate it s efficacy again st th e gold st an dard
rule out in on e case th e possible par t icipat ion of an ar ter y from DSA. ICG-VA can be used as an in depen den t form of angiography
an adjacen t level. Th e use of ICG-VA m ay also help to iden t ify a or as an adju n ct to in t ra- or postoperat ive DSA.
drain ing vein as it en ters th e sp in al can al in rare DAVFs th at are
occult on preoperat ive DSA.40

References
1. Coch ran ST, Bom yea K, Sayre JW. Tren ds in adverse even t s after IV adm in- 4. Fein del W, Yam am oto YL, Hodge CP. In t racarot id fluorescein angiography:
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2. Hope-Ross M, Yan n uzzi LA, Gragoudas ES, et al. Adverse react ion s due to Med Assoc J 1967;96:1–7
in docyan in e green . Oph th alm ology 1994;101:529–533 5. Hongo K, Kobayash i S, Oku dera H, Hokam a M, Nakagaw a F. Non invasive
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6. Raabe A, Beck J, Gerlach R, Zim m er m an n M, Seifer t V. Near-in frared in - 23. Zh ao JZ, Wang S, Yuan G, Xu J, Jin M. [Int raoperat ive angiography in t reat-
docyan in e green video angiograp hy: a n ew m et h od for in t raop erat ive m en t of n eurovascular disorders]. Zh ongh ua Yi Xue Za Zh i 2006;86:1044–
assessm en t of vascu lar flow. Neurosu rger y 2003;52:132–139, discu ssion 1047
139 24. Hänggi D, Et m in an N, Steiger HJ. Th e im p act of m icroscop e-in tegrated
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cran ial-in t racran ial byp ass p aten cy by n ear-in frared in d ocyan in e green ger y of ar teriovenou s m alform at ion s an d dural ar terioven ous fist ulae.
vid eoangiography. J Neurosurg 2005;102:692–698 Neurosurger y 2010;67:1094–1103, discussion 1103–1104
8. Brun eau M, Sauvageau E, Nakaji P, et al. Prelim in ar y person al experien ces 25. Andres RH, Bar th A, Gu zm an R, et al. En dovascular an d surgical t reat m en t
w ith th e applicat ion of n ear-in frared in docyan in e green videoangiogra- of spinal dural ar terioven ous fist ulas. Neuroradiology 2008;50:869–876
phy in ext racran ial ver tebral ar ter y surger y. Neurosurger y 2010;66:305– 26. Padovan i R, Farn et i M, Maida G, Gh adirpour R. Spin al du ral ar terioven ous
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un dergoing h em icran iectom y for m align an t st roke. St roke 2006;37:1549– phy for th e t reat m en t of spinal arteriovenous fist ula. J Spin al Disord Tech
1551 2007;20:442–448
10. Killor y BD, Nakaji P, Gon zales LF, Pon ce FA, Wait SD, Sp et zler RF. Pro- 28. Quiñ on es-Hinojosa A, Law ton MT. In sit u bypass in th e m anagem en t of
sp ect ive evalu at ion of su rgical m icroscop e-in tegrated in t raop erat ive com plex in t racran ial an eu r ysm s: tech n iqu e applicat ion in 13 pat ient s.
n ear- in frared in d ocyan in e green an giograp hy d u ring cerebral ar terio- Neurosurger y 2005;57(1, Suppl):140–145, discussion 140–145
ven ou s m alfor m at ion su rger y. Neu rosu rger y 2009;65:456–462, discu s- 29. Ma CY, Sh i JX, Wan g HD, Hang CH, Ch eng HL, Wu W. In t raop erat ive in -
sion 462 d ocyan in e green angiograp hy in in t racran ial an eu r ysm su rger y: m icro-
11. Sch u et te AJ, Caw ley CM, Barrow DL. In docyan in e green videoangiography su rgical clipping and revascularizat ion . Clin Neurol Neu rosurg 2009;111:
in th e m an agem en t of dural arterioven ous fist ulae. Neurosurger y 2010; 840–846
67:658–662, discussion 662 30. Kalan i MY, Zabram ski JM, Nakaji P, Spet zler RF. Byp ass an d flow red u ct ion
12. Han el RA, Nakaji P, Sp et zler RF. Use of m icroscop e-in tegrated n ear- for com plex basilar an d ver tebrobasilar ju nct ion an eur ysm s. Neu rosur-
in frared in docyan in e green vid eoangiograp hy in th e su rgical t reat m en t ger y 2013;72:763–775, discu ssion 775–776
of spin al du ral ar terioven ous fist ulae. Neu rosurger y 2010;66:978–984, 31. Kalan i MY, Zabram ski JM, Hu YC, Spet zler RF. Ext racran ial-in t racran ial
discussion 984–985 bypass an d vessel occlusion for th e t reat m en t of u n clippable gian t m iddle
13. Raabe A, Beck J, Seifert V. Tech nique an d im age qualit y of in t raoperat ive cerebral ar ter y aneur ysm s. Neu rosurger y 2013;72:428–435, discussion
in docyan in e green angiography during an eur ysm su rger y u sing surgical 435–436
m icroscope in tegrated near-in frared video tech n ology. Zen t ralbl Neu ro- 32. Aw an o T, Sakat an i K, Yokose N, et al. EC-IC bypass fun ct ion in Moyam oya
ch ir 2005;66:1–6, discussion 7–8 disease an d n on -Moyam oya isch em ic st roke evalu ated by in t raoperat ive
14. Balam urugan S, Agraw al A, Kato Y, San o H. In t ra operat ive in docyan in e in docyan ine green fluorescence angiography. Adv Exp Med Biol 2010;
green video-angiograp hy in cerebrovascu lar su rger y: an over view w ith 662:519–524
review of literat ure. Asian J Neu rosurg 2011;6:88–93 33. Aw an o T, Sakat an i K, Yokose N, et al. Int raoperat ive EC-IC bypass blood
15. Batjer HH, Fran kfurt AI, Pu rdy PD, Sm ith SS, Sam son DS. Use of etom idate, flow assessm en t w ith in docyanin e green angiography in m oyam oya an d
tem porar y arterial occlusion , an d int raoperat ive angiography in su rgical n on -m oyam oya isch em ic st roke. World Neu rosu rg 2010;73:668–674
t reat m en t of large an d gian t cerebral an eur ysm s. J Neurosu rg 1988;68: 34. Yan aka K, Fujit a K, Noguch i S, et al. In t raoperat ive angiograph ic assess-
234–240 m ent of graft paten cy during ext racran ial-in t racran ial bypass procedures.
16. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessm en t of flow Neurol Med Ch ir (Tokyo) 2003;43:509–512, discussion 513
in perforat ing arteries du ring in t racran ial aneur ysm su rger y u sing int ra- 35. Ferroli P, Nakaji P, Acerbi F, Alban ese E, Broggi G. In docyan in e green (ICG)
operat ive n ear-in frared in docyanin e green videoangiography. Neurosu r- tem p orar y clip p ing test to assess collateral circu lat ion before ven ou s sac-
ger y 2007;61(3, Suppl):63–72, discussion 72–73 rifice. World Neurosurg 2011;75:122–125
17. Dash t i R, Laakso A, Niem elä M, Porras M, Hernesn iem i J. Microscope- 36. Kim EH, Ch o JM, Ch ang JH, Kim SH, Lee KS. Applicat ion of in t raoperat ive
in tegrated n ear-in frared in docyan in e green videoangiography during in docyan ine green videoangiography to brain t um or surger y. Act a Neu ro-
surger y of in t racran ial an eu r ysm s: th e Helsin ki experience. Surg Neurol ch ir (Wien ) 2011;153:1487–1495, discussion 1494–1495
2009;71:543–550, discussion 550 37. Ferroli P, Acerbi F, Alban ese E, et al. Applicat ion of in t raoperat ive in docya-
18. Mer y FJ, Am in -Hanjan i S, Ch arbel FT. Is an angiograph ically obliterated n in e green angiography for CNS t um ors: result s on th e first 100 cases.
an eur ysm alw ays secure? Neurosurger y 2008;62(4):979-82; discussion Act a Neuroch ir Suppl (Wien) 2011;109:251–257
982 38. Mar t irosyan NL, Cavalcan t i DD, Esch bach er JM, et al. Use of in vivo n ear-
19. Pikus HJ, Beach ML, Harbaugh RE. Microsurgical t reat m en t of ar terio- infrared laser confocal endom icroscopy w ith indocyanine green to detect the
ven ou s m alform at ion s: an alysis an d com p arison w ith stereot act ic rad io- boundary of infiltrative tum or. J Neurosurg 2011;115:1131–1138
surger y. J Neu rosurg 1998;88:641–646 39. Spiot t a AM, Bain M, Moskow it z S. In t raoperat ive in docyan in e green angi-
20. An egaw a S, Hayash i T, Torigoe R, Harada K, Kih ara S. In t raoperat ive angi- ography as a subst it u te for conven t ion al angiography in th e surgical m an -
ography in the resect ion of arterioven ous m alform at ion s. J Neurosurg agem en t of spin al dural arterioven ous fist ulae. J Neuroin ter v Surg 2011;
1994;80:73–78 3:182–185
21. Mun sh i I, Macdon ald RL, Weir BK. In t raoperat ive angiography of brain 40. Killor y BD, Nakaji P, Maugh an PH, Wait SD, Sp et zler RF. Evalu at ion of
arteriovenous m alform ations. Neurosurgery 1999;45:491–497, discussion angiographically occult spin al du ral ar terioven ous fist ulae w ith surgical
497–499 m icroscope-in tegrated int raoperative n ear-in frared indocyan in e green an -
22. Bauer BL. In t raoperat ive angiography in cerebral an eur ysm an d AV- giography: repor t of 3 cases. Neurosurger y 2011;68:781–787, discussion
m alform at ion . Neurosu rg Rev 1984;7:209–217 787

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III Ischemic Stroke and
Vascular Insufficiency

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Neurosurgery Books Full
16 The Pathophysiology of Cerebral Ischemia
Andrew M. Bauer and Robert J. Dem psey

Cen t u ries of w ork h ave resu lted in accu m u lat ion of a w ealth of delivered to th e t issu e.3 Cerebral in farct ion occurs after death of
kn ow ledge regarding th e path ophysiology of brain isch em ia. Th e n eu ron al or glial cells in th e affected region .
relat ion sh ip bet w een blood flow an d cerebral fu n ct ion w as rec- Isch em ia can be classified as eith er com plete or in com plete,
ogn ized as early as th e 6th cen t ur y BC w h en Alcm aeon of Croton , an d global or focal. Global isch em ia, such as th at caused by car-
th e st u den t of Pyth agoras, recogn ized t h at th e ebb an d flow of diac arrest , affects blood flow to all areas of th e brain sim ilarly.
blood in th e cerebral vein s w as im por tan t in cerebral fun ct ion .1 Th ere is lit tle oppor t u n it y for collateral sup ply, an d variabilit y in
Leon ardo da Vin ci recogn ized th at com pression of th e vessels of volum e of in farct ion is caused by region al variat ion s in su scept i-
th e n eck w ou ld p rodu ce u n con sciou sn ess, an d th erefore blood bilit y to isch em ia. Th e durat ion of global isch em ia th at is com -
flow m u st be in tegral to brain fu n ct ion .2 Th e path ophysiological pat ible w ith life is gen erally qu ite brief, an d th e deficits su st ain ed
processes of cerebral isch em ia are com plex an d m u ltim odal; du ring an oxic brain injur y after cardiac arrest are often severe.
n on eth eless, an u n derstan ding of th e un derlying processes h elps Focal isch em ia is m ost often th rom boem bolic in n at u re bu t also
to guide fut ure research an d im prove outcom es in th is popula- resu lt s from su barach n oid h em or rh age, in t racerebral h em or-
t ion of pat ien t s. rh age, an d t raum a. In gen eral, focal isch em ia produces less se-
Th e h u m an body h as im p ressive in n ate protect ion again st vere an d m ore focal d eficit s t h an global isch em ia. Th e volu m e
st roke an d brain inju r y from vascu lar isch em ia. Th e circle of Wil- of in farct is defin ed n ot on ly by th e vu ln erabilit y of in dividu al
lis en sures th at th ere is sign ifican t collateral circu lat ion , w h ich pop u lat ion s of cells, but also th e variabilit y an d com p eten ce of
protects th e brain from in farct ion du e to proxim al vessel occlu - collateral blood flow to th e affected area.
sion . With m ore distal blockage, h ow ever, in farct ion is th e ru le
rath er t h an th e except ion . Th e size of in farct ion depen ds directly
on th e availabilit y an d size of pial–pial collaterals. Collateral flow
is clearly im port an t , as m any p at ien t s w ith sym ptom at ic st roke ■ Vascular Biology
h ave evid en ce of p reviou s in farct ion t h at rem ain ed sm all an d
Aside from cases of isch em ia secon dar y to th rom boem bolism
asym ptom at ic due to th e presen ce of collateral flow. Isch em ic
from m ore p roxim al sou rces su ch as th e h ear t , cerebral isch em ia
inju r y occu rs un der m any differen t circu m st an ces, m ost com -
begin s in th e vascu lar en doth elium of th e carot id or ver tebral
m on ly th rom boem bolism or ath erosclerot ic disease. Th ere are
ar teries or th e sm aller vessels supplying th e brain . Popular belief
m any ot h er cau ses, in clu d in g t rau m a, vascu lar in flam m ator y
in recen t years h as focused on th e role of diet an d hyp erch oles-
diseases, hem orrhage, hypercoagulable states, and venous th rom -
terolem ia in the pathogenesis of vascular atherosclerosis, but th is
bosis. In con t rast to oth er t issues, th e brain is subject to several
m odel far oversim plifies th e u n derlying path ophysiology.
proper t ies, su ch as its st rict relian ce on glu cose an d oxygen as
Th e over w h elm in g body of evid en ce suggest s t h at at h ero -
en ergy su bst rate, au toregu lat ion of blood flow, an d p resen ce of
sclerosis is t h e resu lt of th e in flam m ator y dam age to en d ot h e-
t h e blood–brain bar r ier, t h at m ake isch em ia a ver y h eteroge-
lial cells an d th eir result an t dysfun ct ion .4 Mu lt iple act ivators of
n eou s an d m u lt ifactor ial p rocess. Th is ch apter review s t h e p ro-
th is in flam m ator y p rocess, in clu d in g elevated low -d en sit y lip o -
cesses involved in cerebral isch em ia an d h igh ligh t s p ossible
p rotein (LDL) levels in t h e circu lat ing blood , free rad icals from
aven u es for in ter ven t ion an d research .
cigaret te sm oke or ot h er sou rces, hyp er ten sion , d iabetes, ot h er
m et abolic d eran gem en t s, an d even in fect iou s organ ism s h ave
been p rop osed . Regard less of th e in it iat ing factor, en d ot h elial
dam age cau sed by in flam m ator y cascad es, if left u n ch ecked ,
■ Definitions w ill resu lt in t h e for m at ion of a com p lex at h erosclerot ic lesion .
Th e term s st roke an d cerebrovascular accident are gen erally syn - Bran ch ing poin ts or bifurcat ion s of vessels are part icularly sus-
onym ous; th ey en tail an acute n eurologic deficit of a vascular cept ible to th is process because of th e in creased w all sh ear st ress
et iology caused by isch em ia or h em orrh age. Th e brain m eet s its an d t urbulen ce.5
m et abolic dem an ds solely by u t ilizing glu cose an d oxygen . Th ese En dot h elial vascu lar inju r y st im u lates th e en doth elial cells
m ust be con t in uously delivered as th e brain h as virt ually n o en - to exp ress cell su r face m olecu les t h at lead to t h e ad h eren ce,
ergy reser ve. Isch em ia occu rs w h en deliver y of eith er glucose or m igrat ion , an d accu m u lat ion of m on ocytes an d T-cells in t h e
oxygen fails to m eet th e m et abolic dem an d of t h e t issu e. Hypoxia vascu lar w all.4 As m on ocytes accu m u late in th e vessel w all,
refers to d ecreases in th e p ar t ial p ressu re of oxygen , w h ereas p rod u ct ion of cytokin es an d ot h er in flam m ator y m ed iators re-
an oxia suggest s t h e com p lete absen ce of oxygen in blood flow in forces th e p rocess by fu r th er in flam m ator y cell recr u it m en t .

203

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204 III Ischemic Stroke and Vascular Insufficiency

Th e in it ial in flam m ator y respon se st im u lates th e recr u it m en t p rofile sim ilar to th at in n eop last ic con dit ion s.6 In ou r labora-
an d p roliferat ion of sm oot h m u scle cells resu lt ing in t h icken in g tor y, w e m easu red t h e d en sit y of n eovascu lar izat ion w it h in t h e
of t h e ar terial w all. Alt h ough t h is sm ooth m u scle hyp er p lasia fibrou s cap of th e p laqu e an d fou n d th e den sit y of n ew vessels
occu rs tow ard t h e extern al su r face of t h e vessel, as t h e st iffn ess to be sign ifican t ly h igh er in sym ptom at ic p at ien t s t h an in as-
of t h e w all in creases, t h e lu m en is n arrow ed . In terest ingly, w e ym ptom at ic pat ien t s.7 We hypot h esize th at th is n eovascu lari-
h ave fou n d a d ifferen ce in t h e m olecu lar gen et ics of sym ptom - zat ion con t ribu tes st rongly to in st abilit y of th e plaqu e leading
at ic an d asym ptom at ic carot id p laqu es, suggest in g th at plaqu es to r u pt u re an d d ist al em bolizat ion .8 Fu rth er u n derst an ding of
th at becom e sym ptom at ic begin to t ake on a gen e exp ression t h e m ech an ism s by w h ich an giogen esis an d sm oot h m u scle

a b c

Fig. 16.1a–j Restoration of cerebral perfusion. This patient presented with


left arm transient ischem ic at tack. Magnetic resonance perfusion im ages
show relatively m aintained cerebral blood volum e (a), mildly decreased blood
flow (b), and m arkedly increased m ean transit tim e (c) in the right m iddle
cerebral artery (MCA) territory. Diffusion-weighted im aging shows several d
sm all areas of infarction in the border zone (d, arrow).

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16 Pathophysiology of Cerebral Ischem ia 205

p roliferat ion escap e n orm al gen et ic con t rols m ay h elp to iden - w all an d drive sm ooth m uscle cell apoptosis.9 Th u s, it is th ough t
t ify p at ien t s w ith h igh er risk profiles for st roke an d en able early that the T-cell–m ediated im m une reaction also plays a prom inen t
in ter ven t ion . role in p laqu e in st abilit y. Plaqu e u lcerat ion or r upt ure th en ex-
Several oth er factors w ith in th e ath erosclerot ic plaqu e it self poses th e bloodst ream to n on -en doth elial cells, w h ich are h igh ly
m ay con t ribute to a h igh er risk of st roke. As th e in flam m ator y t h rom bogen ic. Th e ad h eren ce of p latelet s an d for m at ion of a
react ion con t in u es, T-lym p h ocytes an d ot h er in flam m ator y fibrin clot predisposes to dist al em bolizat ion (Fig. 16.1). Th is
cells in duce m acroph ages to secrete m at rix m et alloprotein ases form s th e basis of m edical prophylaxis in patien ts w ith ath ero-
th at break dow n th e fibrou s con n ect ive t issu e w ith in th e vessel sclerot ic carot id disease w ith platelet-in h ibit ing agen ts.

e f g

h i j

Fig. 16.1a–j (continued ) Right com mon carotid angiogram s in antero- ber of the vessel. Magnetic resonance im aging 4 m onths after intervention
posterior (e) and lateral (f) projections dem onstrate high-grade stenosis shows near norm alization of cerebral blood volum e (h), cerebral blood flow
with ulcerated plaque dist al to the internal carotid artery bifurcation. (i), and mean transit time (j). The patient did not develop any further symp-
(g) Postangioplast y and stenting angiography shows restoration of the cali- tom s after treatm ent.

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206 III Ischemic Stroke and Vascular Insufficiency

CO2 is on e of t h e m ost p oten t cerebral vasodilators in h u m an s


■ Cerebral Blood Flow an d in h alat ion of 5% to 7% CO2 is associated w ith an in crease in
Th e path op hysiological m ech an ism s govern ing cerebral blood CBF of 50 to 100%.16 It is gen erally th ough t th at CO2 acts by de-
flow (CBF) are in t im ately t ied to th ose of cerebral isch em ia an d creasing t h e p H of local p er ivascu lar flu id (an d ext racellu lar
in farct ion . Th e brain is su p p lied by fou r m ajor ar ter ies. Th ese m at rix), th ereby leading to K+ efflu x an d hyperpolarizat ion of
ar teries an astom ose at th e skull base to provide redun dan cy in vascular sm ooth m uscle cells, an d decreased cytosolic Ca 2+ con -
flow an d su pply. Several in terdepen den t m ech an ism s regu lat ing cen t rat ion s leading to relaxat ion .17 Th e effect s of CO2 on CBF are
CBF h ave been iden t ified th at fun ct ion in a m an n er dist in ct from gen erally m it igated after 3 to 5 h ou rs. Oxygen is th ough t to be
th ose in th e rest of th e body. Th ese m ech an ism s in clude n euro- an oth er im por tan t regulator of CBF an d m ay act th rough sim ilar
vascular coupling, cerebral autoregulation, and neuronal control. m ech an ism s (albeit w ith th e opposite respon se) to CO2 . In addi-
Met abolic or n eu rovascu lar cou p ling is t h e resp on se of CBF to t ion , hypoxia m ay st im u late n eu ron s in th e rost ral ven trolateral
m et abolic byproduct s in th e ext racellular space, an d h as been m edulla th at affect CBF via th e n eurogen ic m ech an ism described
st udied for over a cen t u r y. More recen tly, th is coupling h as been above.18,19
observed in real-tim e w ith blood-oxygen-level–dependent (BOLD)
fu n ct ion al m agn et ic reson an ce im aging (fMRI) sequ en ces.10 Pro-
ton s, potassium , n it rou s oxide, aden osin e, eicosan oids, en doth e-
lin s, an d oth er m olecu les h ave all been im plicated in th e process
of m etabolic cou p ling. Im p or tan tly, by th is m ech an ism , blood
■ The Ischemic Penumbra
flow ch anges ap pear m ore resp on sive to th e ext racellular m ilieu Th e iden t ificat ion an d p reser vat ion of th e isch em ic p en u m bra
th an to th e rate of n eu ron al firing.11 h as been th e cen t ral focus of st roke research for several decades.
Cerebral au toregu lat ion refers to th e p h en om en on w h ereby Th is is based on th e idea th at th ere are differen t CBF th resh old s
n ear-con st an t CBF is m ain tain ed over a w ide range of cerebral th at ren der cells eith er in act ive or dead. Cells, w h ich are in act ive
perfu sion p ressu res (50–150 m m Hg). Th e m ech an ism of au to- bu t n ot yet d ead , are t h eoret ically cap able of salvage if blood
regu lat ion involves vasocon st rict ion of cerebral resistan ce ves- flow can be restored or secon dar y dam age can be m it igated (Fig.
sels (precapillar y ar terioles) in respon se to in creased t ran sm u ral 16.2).
pressu re. Au toregu lat ion is kn ow n to be im p aired or abolish ed in In th eir 1974 paper, Sun dt et al20 establish ed th at du ring u n i-
con dit ion s of ch ron ic isch em ia, su barach n oid h em orrh age, t rau - lateral carot id occlu sion for en dar terectom y, d ecreases in CBF
m at ic brain injur y, cer t ain m etabolic derangem en t s, an d vessels below 18 m L/100 g/m in un iform ly resulted in depression of th e
in t h e bed of an ar ter ioven ou s m alfor m at ion .12 Alt h ough t h e elect roen cep h alogram (EEG) t racing on t h e ip silateral sid e. It
exact m ech an ism of cerebral au toregu lat ion is u n kn ow n , several w as n oted t h at after p lacem en t of a sh u n t , som et im es after a
hypoth eses h ave been pu t for th to explain th e obser ved clin ical p eriod of m ore th an 10 m in utes, EEG fun ct ion ret urn ed an d
fin dings. In th e m yogen ic hyp oth esis, th e sm ooth m u scle cells of n on e of th e pat ien ts h ad postoperative in farct ion . Flow below 6
th e ar terial w all are able to respon d directly to ch anges in pres- to 8 m L/100 g/m in for sh or t periods of t im e h as been sh ow n to
su re via som e in h eren t m ech an oreceptor m ech an ism w ith th e lead to aden osin e t riph osph ate (ATP) dep let ion an d in creases in
in flu en ce of calciu m .13 Th e en doth elial hypoth esis suggest s th at ext racellu lar K+ con cen t rat ion s, in dicat ing m em bran e dysfun c-
autoregu lat ion m ay be con t rolled by th e en doth elial release of t ion .21 Th e viabilit y of th e cell is related n ot on ly to th e absolu te
n it ric oxide in respon se to ch anges in w all st ress.14 Fin ally, th e levels of p erfusion but also to th e d urat ion for w h ich th e cell is
n eu rogen ic hyp ot h esis at t r ibu tes au toregu lat ion to t h e release su bjected to altered flow.22 It is suggested th at flow levels below
of n eu rot ran sm it ters from p er ivascu lar n er ve fibers.15 An atom - 6 to 8 m L/100 g/m in m ay be tolerated for u p to 1 h our w ith out
ically, t h ere is som e cred en ce to t h is last hyp ot h esis based on perm an en t n ecrosis or t issue dam age.23 In an oth er st udy of sur-
t h e in n er vat ion of th e cerebral vessels th em selves. Vessels at th e vival of cort ical n eu ron s, cells did n ot recover th eir spon t an eous
su rface of th e brain an d in th e Virch ow -Robin sp aces receive in - activit y after experiencing flow reduction below 5 m L/100 g/m in
n er vat ion from th e t rigem in al (sen sor y), superior cer vical (sym - for 20 m in utes, below 8 m L/100 g/m in for m ore th an 30 m in u tes,
path et ic), an d sp h en op alat in e (p arasym path et ic) ganglia. On ce below 12 m L/100 g/m in for m ore th an 50 m in utes, or below 15
th e vessels dive w ith in th e brain paren chym a, th ey receive local m L/100 g/m in for m ore th an 80 m in u tes.24 Th is st u dy suggested
in n er vat ion from th e n u cleu s basalis, th e locu s coeruleu s, an d th at isch em ia below 18 m L/100 g/m in m ain t ain ed in defin itely
th e dorsal rap h e n u clei.11 It is clear t h at th ese p at tern s of in n er- w ould cau se perm an en t cell dam age (Table 16.1).
vat ion h ave com plex in terplay in both n orm al an d path ological Alth ough cerebral isch em ic dam age is directly related to de-
st ates. liver y of en ergy su bst rate via blood flow , ch anges in cell m e-
Any discussion of CBF w ould be in com plete w ith out discus- t abolism in itiated by isch em ia m ay con t in ue un abated even after
sion of th e role of carbon dioxid e (CO2 ). It h as been kn ow n for restoration of substrate.25 This suggests that although restoration
m any years th at hyp er ven t ilat ion is a u sefu l sh or t-term t reat- of CBF is clearly necessar y to restore function and prevent further
m en t for elevated in t racran ial p ressu re. Hyp er ven t ilat ion act s by dam age, it m ay n ot be en ough in an d of it self. Th e sp ecific m ech -
decreasin g CO2 (an d t h u s H + ion con cen t rat ion s) in t h e brain . an ism s by w h ich th is occurs are described in th e n ext sect ion .

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16 Pathophysiology of Cerebral Ischem ia 207

a b

c d

Fig. 16.2a–h Cerebral blood flow and m echanical throm bolysis. Com - lobe. This pat tern is indicative of severe deficit in blood flow and MTT, with
puted tom ography (CT) perfusion m ap showing decreased blood flow (a), preservation of substrate delivery via collaterals (cerebral blood flow). (d) CT
increased m ean transit tim e (MTT) (b), and preserved cerebral blood vol- angiogram shows right MCA occlusion (arrow). (continued on page 208)
um e (c) in the m iddle cerebral artery (MCA) distribution of the right frontal

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208 III Ischemic Stroke and Vascular Insufficiency

e f

g h

Fig. 16.2a–h (continued ) (e) Right internal carotid artery (ICA) angio- MCA flow in-phase with the ACA. (h) Non-infused CT at 2-weeks shows
gram anteroposterior (AP) view shows MCA occlusion (arrow) with dense only a sm all area of hyperem ia and infarct in the right insular cortex (arrow),
anterior cerebral artery (ACA)–MCA pial–pial collaterals (f, arrows). (g) Right which is much sm aller than the original perfusion defect.
ICA angiogram AP view post–m echanical thrombolysis showing antegrade

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16 Pathophysiology of Cerebral Ischem ia 209

Table 16.1 The Phases of Cerebral Ischemia

Rate of Cerebral
Blood Flow
Phase (mL/100 g/min) Neurologic Deficit Biomechanical Events

Norm al 50–60 No deficit No change, blood flow sufficient for delivery of oxygen and glucose
Hemodynamic 20–50 Mild or none, reversible Blood volum e increases due to dilatation of collaterals to keep
substrate delivery relatively constant. Once arterioles are m aximally
dilated, oxygen and glucose extraction fractions increase to
maintain metabolism. Cellular damage is minimal. No reperfusion
injury if intervention at this stage. Mild acidosis m ay occur at this
stage.
Penumbra 10–20 Severe, reversible (if only Electrical failure on electroencephalogram. Oxidative metabolism
for a short time) reduced, failure of membrane ion pumps. Relatively m ild increases
in extracellular potassium and intracellular calcium. Increases in
extracellular glutamate causing excitotoxicit y. May suffer reperfusion
injury due to accumulation of reactive oxygen species. Results in
production of inflam matory m ediators and recruitment of
inflammatory cells.
Infarct < 10 Severe, irreversible Complete failure of ion homeostasis and plasm a membrane leads to
(infarction) cellular death. Massive influx of calcium and efflux of potassium
from the cell. Inflam matory response is marked and can induce
damage in adjacent tissue. Cerebral edema from ion pump and
metabolic failure. Reperfusion m ay result in hemorrhage from
breakdown of blood–brain barrier.

■ Modes of Neuronal Death m ach in er y, resu lt in g in ATP d ep let ion an d m em bran e inju r y.
As op posed to cell sh rin kage an d p h agocytosis, th e n ecrot ic cell
from Ischemia sw ells u n t il th e m em bran e is even t u ally lysed, spilling th e cel-
Apoptosis an d n ecrosis are th e m ost com m on ly discussed pat- lular con ten t s in to th e ext racellu lar space. Th is often result s in
tern s of cell death in cerebral isch em ia. Apoptosis is essen t ially dam age to su rrou n ding cells an d an in ten se in flam m ator y re-
“cell su icid e” as t h e fu n ct ion al u n it s of t h e cell sh u t d ow n in sponse, w h ich is lacking after apoptosis.26 Event ually, th e n ecrotic
respon se to cer tain death sign als. Th e cell sh rin ks in to sm all cy- m aterial is rem oved by m acroph ages and oth er im m un e cells
toplasm ic, m em bran e-boun d vesicles th at con t ain th e rem n an ts an d rep laced by gliot ic scar t issu e (Fig. 16.3).
of organ elles an d n uclear bodies.26 Th ese “apoptot ic bodies” are Th e m icroscop ic app earan ce of th e core of an in farct is p re-
then rem oved from the t issue by im m un e-directed phagocytosis. dom in an tly ch aracterized by n ecrosis. Th e m ost isch em ic t issu e
Th ere is m in im al in flam m ator y react ion of th e su rrou n ding t is- is often fatally injured an d n ot capable of recover y. On e t arget for
sue and little, if any, evidence that the cell ever existed. Apoptosis fu t u re t reat m en t of st roke involves m odulat ion of th e in flam m a-
is a con t rolled form of cell death and is involved in p ath ological tor y respon se aroun d th e in farct core. Un ch ecked, th is respon se
processes as w ell as n orm al t issu e t u rn over an d m ain ten an ce. often leads to fu rth er t issue dam age and death . On th e oth er
Variat ion s of t h is p rocess are an essen t ial p ar t of fet al d evelop - h an d, apoptosis m ay p lay a role in delayed cell death in th e isch -
m en t w h ere th e brain is “sculpted” in to fun ct ion al n eural n et- em ic p en u m bra (see below ) w h ere th e isch em ic cell is p reser ved
w orks from a m ass of d isorgan ized cells. for h ours to days after th e in it ial in farct .27 If th e ap optot ic sign als
In con t rast , n ecrosis is an u n con t rolled an d violen t cell death . can be preven ted or m it igated in th e ap propriate t im e w in dow,
Th is p rocess is often in it iated by th e lack of fu el for th e cellu lar t issue in th e pen u m bra m ay be preser ved.
(text cont inues on page 212)

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210 III Ischemic Stroke and Vascular Insufficiency

a b

c d e

Fig. 16.3a–k The evolution of an infarct. This patient presented with left- giogram (b) shows right middle cerebral artery (MCA) occlusion (arrow). CT
sided weakness. Non-infused computed tom ography (CT) of the head (a) perfusion imaging shows decreased blood volume (c), decreased blood flow
shows mild cortical edem a (arrow) but no obvious infarct, whereas CT an- (d), and increased m ean transit time (e) in the right MCA distribution.

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16 Pathophysiology of Cerebral Ischem ia 211

f g h

i j k

Fig. 16.3a–k (continued ) Magnetic resonance im age shows gyriform T2 and there is gyriform contrast enhancem ent (j) due to breakdown of the
hyperintensit y (f) and diffusion restriction (g) in the right MCA distribu- blood–brain barrier. (k) At 6 m onths, the infarcted brain has undergone
tion. (h) By day 3, the right MCA infarct is quite obvious on CT (a craniec- necrotic transform ation.
tomy has been perform ed). At 2 weeks, the T2 hyperintensit y rem ains (i)

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212 III Ischemic Stroke and Vascular Insufficiency

Fig. 16.4 The apoptotic pathway. In the intrinsic pathway, ischem ia in- is com m on to both m odes of apoptosis. This results in DNA dam age and
duces the calcium -dependent alteration in the m itochondrial transition activation of proteases, which break down the cell m em brane and lead di-
pore (MTP). This leads to efflux of cytochrom e c from the m itochondria, rectly to the form ation of apoptotic bodies and cell death. It should be
which form s the apoptosom e and ultim ately activates caspase-3. The ex- noted that these pathways are also activated by reactive oxygen species,
trinsic pathway is m ediated by certain death ligands (FasL) that bind to which are produced with reperfusion of ischem ic tissue. Abbreviations:
cell-surface receptors leading to caspase-3 activation directly or through NMDA, N-m ethyl-D-aspartate. (Courtesy of Barrow Neurological Institute.)
the alteration of the MTP. Caspase-3 begins the execution pathway, which

Apoptosis occurs by both an in t rin sic an d ext rin sic path w ay ch an n els, an d variou s oth er cytoskelet al com p on en t s. In ter ven -
in th e brain (Fig. 16.4). Th e en d resu lt of both path w ays is th e t ion in th is fin al com m on path w ay m ay p rovide an op por t u n it y
release of cytoch rom e c in to th e cytosol th rough th e ou ter m ito- to block apoptosis regardless of th e origin al in it iat ing factor.
ch on d r ial m em bran e. In t h e in t r in sic p at h w ay, t h is occu rs by
d irect m itoch on drial dam age or ch anges in perm eabilit y of th e
outer m em bran e in a process depen den t on th e act ion of Bcl-2
protein s.28 Th e ext rin sic path w ay is ch aracterized by st im u lat ion ■ Biochemical and Metabolic
of plasm a m em bran e “death dom ain s” by th e bin ding of th e Fas
ligan d to its receptor. It w as origin ally th ough t th at th e ext rin sic
Derangements in Ischemic Brain
path w ay played m ore of a role in n orm al t issu e m ain ten an ce Th ere are en t ire cascad es of ch anges th at occur in brain cells de-
th an in acute isch em ia, bu t Fas an d FasL im m u n oreact ivit y h as void of m et abolic subst rate. Broadly, th ese can be classified in to
been sh ow n to be elevated in p en u m bral n eu ron s in h u m an ch anges in cell sign aling an d t ran sdu ct ion , in m et abolism , an d in
brain s.29 Th is suggest s t h at p en u m bral n eu ron s m ay be receiv- gen e regulat ion an d expression .25 Pract ically, isch em ia result s in
in g a “self-dest r uct” sign al from n eigh boring t issues dam aged by disru pt ion of cellu lar en ergy su bst rate, disru pt ion of ion h om eo-
isch em ia. Th ese fin d ings p rovide an opp ort u n it y for in ter ven - st asis, an d failure of cellu lar st ruct ural in tegrit y.31
t ion in this p rocess, p reser ving th e pen u m bra. By m ass, t h e brain h as t h e h igh est en ergy requ irem en t s of
In th e fin al com m on path w ay for apoptosis, cytoch rom e c any t issu e w ith in th e body. Th e brain receives 25% of th e cardiac
from th e m itoch ondria bin ds several protein s in the cytosol form - output at rest an d con sum es 20% of th e body’s total en ergy
ing th e apoptosom e. Th e apoptosom e leads to th e act ivat ion of stores.32 The prim ary function of blood flow to the brain is to de-
several cellu lar casp ases, in par t icu lar caspase-3, w h ich carr y liver glucose an d oxygen for m itoch on drial oxidat ive ph osph or y-
out th e fin al t asks of apoptosis.30 Caspase-3 is kn ow n to cleave lat ion an d p rod u ct ion of ATP. ATP is vit al as t h e m ain cerebral
poly–adenosine diphosphate (ADP), poly (ADP-ribose) polym erase en ergy t ran sfer m olecu le, w h ich is involved in ion h om eost asis
(PARP) (a DNA repair en zym e), various plasm a m em bran e ion an d act ion p oten t ial con d u ct an ce (via t h e Na +/K+–ad en osin e

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16 Pathophysiology of Cerebral Ischem ia 213

t r iph osp h at ase [ATPase]), n eu rot ran sm it ter reu pt ake, an d syn - ch on dria becom e m ore dysfu n ct ion al, th ey release Ca 2+ back in to
th esis of cellu lar m olecu les an d protein s. Th e absolu te cellu lar th e cytosol creat ing a p osit ive feedback loop for cellular inju r y
effect s of isch em ia largely dep en d on th e available reser ve stores an d breakdow n . Alth ough acidosis m ay m it igate th e effects of
of glu cose or th e am ou n t of glu cose an d oxygen sup plied by col- glut am ate-in duced Ca 2+ in flu x, it gen erally leads to m ore cellular
lateral circulat ion . dam age th rough th e gen erat ion of free radicals.40
Main ten an ce of rest in g n eu ron al m em bran e p oten t ials is
h igh ly depen den t on sodiu m an d potassium exch ange via th e
Na +/K+-ATPase, w h ich requ ires th e hydrolysis of ATP. For secon ds
to m inutes after th e on set of isch em ia, ATP levels can be kept ■ Inflammatory Mediators in
near baseline by creating m ore ATP from short-term storage m ol-
ecules such as ph osph ocreat in e.33 Ast rocytes also con tain th eir
Cerebral Ischemia
ow n supply of glycogen , an d th is can be used for ATP syn th esis Cerebral t issu e can n ot p rogress from isch em ia to in farct ion
even u n der hypoxic con dit ion s via an aerobic glycolysis.34 During w ith out th e presen ce an d act ion of in flam m ator y cells an d m e-
th is p eriod, cellu lar processes con t in u e as n orm al an d th ey fu r- diators. It is w rong, h ow ever, to assu m e th at in flam m at ion h as
th er dep lete ATP stores. As ATP levels fall an d th e Na +/K+-ATPase on ly n egat ive con sequen ces in th e brain in th e set t ing of isch -
ceases it s fun ct ion , th e m em bran e becom es “leaky.” Th is leads to em ia or inju r y. Th e p rod u ct ion of in flam m ator y m ed iators by
th e gradu al efflu x of K+ an d, in t u rn , a gradual rise in th e rest ing isch em ic t issu e is a fin al “call for h elp ” t h at m ay resu lt in som e
m em bran e poten t ial.35 As th e m em bran e poten t ial rises, voltage- p rotect ive m ech an ism s being act ivated w h ile also p rop agat ing
gated ion ch an n els open , leading to fur th er efflu x of potassium an in flam m ator y resp on se t h at creates secon dar y dam age an d
an d in flu x of Na +, Ca 2+, an d Cl– . Th e failu re of rest ing m em bran e u lt im ately larger in farct volu m e. Ult im ately, t h e leu kocyte is
ion ic gradien t s leads to cytotoxic edem a as w ater flow s in to th e t h e cell resp on sible for th e progression of cerebral isch em ia to
cell w ith Na + an d Cl– . Movem en t of w ater h as th e poten t ial to in farct ion .41
lead to fu r th er secon dar y isch em ic dam age via redu ct ion s in CBF In flam m ator y gen es for factors su ch as in terleukin -1 (IL-1),
to th e affected areas because of local or global in creases in in t ra- IL-6, t u m or n ecrosis factor-α (TNF-α), an d t ran sfor m ing grow t h
cran ial pressure. Th is con cept h as led to som e prom ise for early factor-β (TGF-β) are overexpressed in ischem ic tissue resulting in
su rgical decom pressive cran iectom y to m it igate th e effect s of produ ct ion of th ese in flam m ator y cytokin es.42 Th is is st im u lated
in creased in t racran ial p ressure an d preser ve blood flow in th e largely by th e isch em ia it self, as w ell as th e in flu x of calciu m an d
absen ce of sufficien t ATP. Given n o m ean s to reest ablish th e ion react ive oxygen sp ecies. Th ese in flam m ator y cytokin es lead to
gradien ts n ecessar y for n orm al n eu rologic fu n ct ion , th e term i- th e u p regu lat ion of cell adh esion m olecu les su ch as E-select in ,
n ally depolarized n eu ron s becom e elect rically silen t .36 in tercellu lar ad h esion m olecu le-1 (ICAM-1), ICAM-2, an d vas-
Th e term in al dep olarizat ion of n eu ron s is also th ough t to play cu lar cell adh esion m olecu le-1 (VCAM-1) in th e en doth elial cells
a role in secon dar y brain dam age via excitotoxicit y.37 ATP deple- of th e cerebral m icrovascu lat ure.41 Th ese adh esion m olecules, in
t ion leads to in creased ext racellu lar levels of glu t am ate (an excit- t urn , bin d n eut roph ils an d assist in th eir t ran slocat ion in to th e
ator y am ino acid) both via increased release from the depolarized cerebral paren chym a. Som e auth ors h ave th eorized th at m icro-
n eu ron s an d decreased reupt ake (an ATP-depen dent process). vessel plugging by n eut roph ils, platelets, an d red blood cells fur-
Alth ough n eu ron s in th e isch em ic pen um bra tech nically h ave t h er in h ibit s th e p er fu sion of t h ese brain region s (n o -reflow
en ough su bst rate deliver y to su st ain cellu lar processes, th eir ATP ph en om en on ).43 Th is react ion can also be p erp et u ated w h en th e
stores can be depleted by repetitive depolarization/repolarization t issu e is revascu larized , resu lting in th e deliver y of m ore in flam -
m ed iated by glu t am ate excit at ion of N-m et hyl-D-asp ar t ate m ator y cells, but is also act ive in th e pen um bra an d surrou n ding
(NMDA) or α -am in o-3-hydroxy-5-m ethyl-4-isoxazoleproprion ic t issu e becau se of th e local an d region al act ion of th e cytokin es.
acid (AMPA) receptors. Th is can lead to th eir term inal depolar- Prod u ct ion of react ive oxygen species by in flam m ator y cells is
ization.38 This glutam ate-m ediated depolarization leads to further on e of th e key factors in rep erfusion inju r y.
cytosolic Ca 2+ overload, w h ich in t u rn leads to fu r th er st r u ct ural In addit ion to recr uited leukocytes from th e bloodst ream , m i-
cellular dam age. Th is is th ough t to be on e of th e un derlying rea- croglia in th e cerebral t issue are act ivated w ith in a few m in utes
son s th at restorat ion of CBF m ay n ot en t irely p reser ve th e p en - of th e isch em ic in su lt .44 Like so m any of th e factors in develop -
um bral t issue. m en t an d progression of st roke, th e in flam m ator y act ivat ion of
An oth er factor th at con t ributes to secon dar y injur y in th e m icroglia app ears to be a “dou ble-edged sw ord.” Th e in flam m a-
isch em ic pen um bra is acidosis. Dep en d ing on th e balan ce be- tor y m ediators an d cells con t ribu te to a prolonged respon se to
t w een oxidat ive p h osp h or ylat ion an d an aerobic glycolysis oc- injur y, result ing in injur y to th e pen u m bra, cerebral edem a, an d
cu r rin g in t h e isch em ic p en u m bra, t h e ext racellu lar p H falls breakdow n of th e blood–brain barrier. Leukocytes release factors
secon dar y to th e product ion of lact ate an d proton s. It h as been t h at act ivate t h e m at r ix m et allop rotein ases in th e vascu lar en -
dem on st rated th at p reisch em ic hyp erglycem ia aggravates cere- d oth elium , w h ich cleave protein s in th e ext racellular m at rix an d
bral isch em ic dam age an d leads to a larger (an d earlier) n ecrot ic plasm a m em bran e.45 Th e in flam m ator y react ion also in du ces
in farct volu m e. It is th ough t th at hyp erglycem ia con t ribu tes to act ivat ion of th e con tract ile com pon en t of th e en doth elial cell
acidosis via increased lactate product ion in an aerobic glycoly- con t ribu t ing to th e form at ion of larger gap ju n ct ion s.46 As th e
sis.39 Th ere is also a com p lex in teract ion bet w een acidosis an d blood–brain barrier fur th er degrades, th e paren chym a is flooded
in t racellular Ca 2+ con cen t rat ion s. Mitoch on drial sequest rat ion is w ith m ore in flam m ator y cells com pou n ding th e process, as w ell
on e of t h e p r im ar y cellu lar con t rols of cytosolic Ca 2+; h ow ever, as album in an d oth er osm ot ic com poun ds con t ribut ing to th e
as par t ially hypoxic m itoch on dria t ake up Ca 2+ from th e cytosol, vasogen ic edem a seen in st roke. Th is fur th er con t ributes to sec-
th eir abilit y to p rodu ce ATP is fu r th er redu ced .31 As th e m ito- on dar y isch em ia an d fu r th er risk to th e isch em ic pen um bra.

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214 III Ischemic Stroke and Vascular Insufficiency

At th e sam e t im e, act ivated m icroglia appear to assist in th e release of in t racellu lar calciu m (fur th er poten t iat ing th e effect ),
m ain ten an ce of bystan der cells by secret ing cytokin es an d ch e- an d dam age to cellu lar st r u ct ure.53
m okin es.44 Alt h ough it h as been gen erally accepted t h at t h e Th e produ ct ion of free radicals resu lt s in secon dar y en ergy
h u m an brain h as lim ited cap acit y for regen erat ion an d rep air, failure of th e recovering cell via in act ivat ion of th e t ricarboxylic
th e in flam m ator y resp on se m ay act u ally in du ce th e p rolifera- acid cycle en zym es an d dissipat ion of th e m itoch on drial m em -
t ion an d m igrat ion of n eu ral p rogen itor cells to th e inju red t is- brane potential leading to dysfunction in the electron transp or t
su e.47 We h ave fou n d th at expression of osteop on t in , galect in -3, ch ain .54 Th is is fu r t h er p rop agated by t h e act ivat ion of PARP-1
an d m on ocyte ch em oat t ract an t p rotein -1 st im u late an giogen - by DNA dam age an d react ive oxygen sp ecies lead ing to d ep le-
esis in th e su bven t ricu lar zon e an d in du ce th e p roliferat ion of t ion of th e oxid ized for m of n icot in am id e ad en in e d in u cleot id e
n eu ral p rogen itor cells an d t h eir m igrat ion to t h e isch em ic (NAD+). Becau se th e produ ct ion of NAD+ is ATP-depen den t , th is
area.48–50 By h arn essing th ese m ediators an d lim it ing th eir det ri- con t in u es th e viciou s cycle of en ergy dep let ion , m et abolic fail-
m en t al effects, w e m ay be able to m ake progress tow ard restora- u re, an d n ecrot ic cell death .55
t ion of fun ct ion after st roke.

■ Conclusion
■ Reperfusion and Brain Damage Th e vit al fu n ct ion s of th e brain are directly depen den t on con -
If direct isch em ic cellu lar injur y is n ot en ough , th e t reat m en t of t in u ou s blood flow for d eliver y of m et abolic su bst rates. Th e
isch em ic st roke is fu r th er com pou n ded by th e secon dar y inju r y brain , u n like ot h er body organ s, h as m in im al en ergy reser ves
created th rough reperfusion . Reperfusion is th e r ule in isch em ic an d lit tle capacit y for repair on ce dam aged. Cerebral isch em ic
disease an d m ay occu r by su ccessfu l m edical in ter ven t ion versu s even ts are a m ajor cau se of m orbidit y an d m or talit y. Th rough
autolysis of clot or im proved supply of ar terial collaterals. For a greater u n derst an ding of th e m u lt ifactorial p rocess by w h ich
sh or t t im e after an acu te isch em ic even t , t issu es h ave bet ter ac- isch em ia causes brain inju r y, it is h oped th at p at ien ts at risk for
cess to oxygen th an to m etabolic subst rate. Th is leads to th e pro- st roke can be iden t ified early an d ap propriately t reated. In th is
du ct ion of react ive oxygen sp ecies in th e m itoch on dria, w h ich ch apter, w e h ave ou tlin ed t h e m ajor regu lator y com p on en t s of
leads to protein oxidation/nitrosylation/nitration, lipid peroxida- CBF an d th e m ajor path ophysiological even ts t aking place in th e
tion an d DNA dam age, leading to cell d eath despite th e resu m p - isch em ic brain . In ter ven t ion m ay com e in th e form of preven t ion
tion of norm al oxygen and substrate deliver y.51 Th is phenom en on of ath eroem bolic disease, or in th e form of cerebral protect ion .
m ay play a role in th e failure of som e reperfusion th erapies to Th e fu t u re of st roke research is brigh t w ith th e p oten t ial for
im prove ou tcom es. m ajor advan ces. As th e et iology an d gen et ic factors involved in
Alth ough brain t issue is isch em ic, th e con su m pt ion of any re- ath erosclerosis are fu r th er defin ed, w e w ill d iscover n ew m eth -
ser ve ATP resu lts in th e form at ion of several pu rin e m et abolites ods of preven t ion an d th erapy. Iden t ificat ion of th e “u n st able”
su ch as xan t h in e an d hyp oxan t h in e. After rep er fu sion , t h ese plaqu e m ay en able earlier in ter ven t ion an d t reat m en t in at-risk
m etabolites are oxidat ively broken dow n , form ing peroxide an d pat ien ts. Un derstan ding of th e path op hysiological m ech an ism s
su p eroxide radicals. High levels of cytosolic calciu m du ring isch - of cerebral in farct ion w ill en able ou r t reat m en t m odalit ies to
em ia are also kn ow n to con t ribu te to th e produ ct ion of react ive lim it prim ar y an d secon dar y brain inju r y. As reperfusion tech -
oxygen species th at can dam age th e cell. In terest ingly, alth ough n ology im proves, w e n ot on ly w ill focus on reperfusion of th e
som e of th ese m et abolites are bu ilding u p du ring isch em ia, th ey at-risk t issu e, bu t also w ill lim it any dam age cau sed by react ive
often do n ot cause cellular dam age u n t il th e t issue is reperfused oxygen species an d th e im m un e respon se to reperfu sion . Fin ally,
an d th e cell is resu pplied w ith oxygen .52 Th ese react ive oxygen alth ough w e m ay n ot be able to preven t in farct ion in ever y case,
species th en result in lipid peroxidat ion, protein den at urat ion , w e m ay be able to h arn ess th e in flam m ator y “call for h elp” th at
in act ivat ion of n ecessar y cellu lar en zym es, DNA dam age, fu rth er occurs to assist in rem odeling an d regen erat ion of brain t issue.

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17 Medical Management of Cardiogenic
Cerebral Embolism
Yazan J. Alderazi and Sean I. Savitz

Deter m in in g t h e et iology of isch em ic st roke is cen t ral to sec- ated from other m uch less frequent causes of proxim al em bolism ,
on dar y preven t ion because specific eviden ce-based t reat m en t su ch as aor t ic arch ath erom a an d parad oxical em bolism . Th ese
dep en ds on th e st roke su bt yp e. Cardiogen ic em bolism , along sources m ay create sim ilar pat tern s of in farct ion .
w ith sm all vessel disease, ext racran ial ath erosclerosis, an d in t ra- Th e m ajorit y of cardioem boli origin ate in th e left-sided h ear t
cran ial ath erosclerosis, accoun t for m ost cases of isch em ic st roke. ch am bers, in p ar t icu lar t h e left at riu m an d left at rial ap p en dage
Oth er less com m on cau ses in clu de ar terial dissect ion an d, rarely, in cases of at rial fibrillat ion . Th e left ven t ricle an d th e m it ral an d
vascu lit is. Th ere are also som e con ten t ious causes such as para- aor t ic valves are oth er locat ion s of cardiogen ic em bolism as in
d oxical em bolism w it h a p aten t foram en ovale. Fu r t h er m ore, m ural th rom bus, m ech an ical valve disease, an d rh eum at ic h ear t
patients often have several com peting m echanism s of stroke pre- disease. Th e righ t h ear t circu lat ion is effect ively separated from
d isp osing t h em to recu rren t st roke risk. Th erefore, a t h orough th e left h ear t circulat ion by th e pulm on ar y cap illar y system an d
evalu at ion for each of t h e m ajor cau ses is n ecessar y for each an in t act in t ra-at rial sept u m in m ost pat ien ts. Tricuspid disease
pat ien t . an d pulm on ar y ar ter y disease are n ot con sidered direct an a-
Although the m anagem ent of atrial fibrillation , th e m ost com - tom ic su bst rates for cerebral em bolism .
m on cau se of cardiogen ic em bolism , is w ell defin ed in term s of
risk factors, p rogn ost ic factors, diagn ost ic m odalit ies, an d pres-
en ce of effect ive t reat m en t , it rem ain s a sign ifican t pu blic h ealth
problem . An aging p op u lat ion in developed cou n t ries, cou p led ■ Pathophysiology and Natural History
w ith in creasing prevalen ce of hyper ten sion w orldw ide, suggests of Cardioembolic Stroke
th at at rial fibrillat ion w ill rem ain a com m on cau se of card io-
em bolic st roke for years to com e. Oth er cau ses of cardioem bolic Th e sou rces of cardioem boli are varied. Th ey m ay be grou ped
stroke are also relatively com m on; som e of them require different u n der com m on p ath op hysiological–an atom ic con siderat ion s.
preven t ive an d th erapeu t ic app roach es, e.g., in fect ive en docardi-
t is an d perip rocedu ral st roke associated w ith cardiac su rger y.
Arrhythmias
At r ial fibrillat ion is th e m ajor cau se of card ioem bolic st roke.
According to dat a from th e Fram ingh am st udy, at rial fibrillat ion
in creases th e risk of st roke 5-fold.1 Hyper ten sion , coron ar y ar-
■ Relevant Anatomy ter y disease, alcohol abuse, valvular heart disease, dilated cardio-
Th e en t ire cerebral circu lat ion is su p p lied by bran ch es of th e m yopathy, hyper t roph ic cardiom yopathy, an d hyper thyroidism
proxim al aor ta. Th e sou rce of em bolism is proxim al in cardio- are iden t ified risk factors for developing at rial fibrillat ion .
gen ic em bolism ; th erefore, occlusion m ay involve th e an terior or At rial fibrillat ion m ay be silen t or sym ptom at ic. It is also clas-
posterior circu lat ion . Frequ en tly, both territories are involved. sified as p aroxysm al, p ersisten t , or longst an ding-persisten t de-
Eith er h em isph ere m ay be affected an d is at risk of recurren t pen ding on th e du rat ion of th e arrhyth m ia. A h igh risk of st roke
st roke in th is st roke su bt ype. Occlu sion m ay involve p roxim al is associated w it h bot h p aroxysm al an d p ersisten t at r ial fibr il-
m ajor vessels su ch as th e in tern al carot id ar ter y, w h ich places lat ion .2 Th e risk of cerebral em bolism in pat ien t s w ith at rial fi-
large brain territories at risk. Occlu sion of distal bran ch es can brillat ion is n ot con stan t across pat ien t groups. Several clin ical
cau se localized dam age, as in occlu sion of d ist al m iddle cerebral scores h ave been develop ed to st rat ify th e risk of cardioem bolic
ar ter y (MCA) bran ch es or even t iny in farct s lim ited to th e m icro- st roke in pat ien t s w ith at rial fibrillat ion , for exam ple, th e Con -
circulat ion . Depen ding on th e st at us of th e collateral circulat ion gest ive h ear t failure Hyper ten sion Age Diabetes St roke (CHADS2 )
an d on th e rapidit y of th rom bus dissolut ion , cardiogen ic em bo- score (Table 17.1).3 Th ese scor in g system s are u sefu l for d ecid -
lism m ay lead to in farct ion s rest ricted to territories of p erforator in g th e t im ing of an t icoagu lat ion for p at ien t s w h o h ave n ot h ad
vessels, su ch as t h e len t icu lost r iate vessels or p on t in e p er fora- an isch em ic st roke or t ran sien t isch em ic at tack (TIA), especially
tors. Th is poin t is im por tan t because th e in it ial clin ical presen ta- you n g p at ien t s w it h low CHADS2 scores. How ever, t h e ben efit
t ion an d , in som e cases, even t u al ou tcom e m ay m im ic t h at of of an t icoagulat ion h as clearly been est ablish ed for pat ien ts w h o
sm all vessel d isease. Th e p at ter n of in farct ion in card iogen ic h ave already experien ced an isch em ic st roke or TIA. Th ese pa-
em bolism m ay m im ic th at of border-zon e in farct ion , also kn ow n t ien ts h ave a m uch h igh er risk of stroke.
as w atersh ed in farct ion . Tiny em boli h ave a ten d en cy to lodge Elect rop hysiologically, at rial fibrillat ion is cau sed by abn or-
in th e sm all vessels of th e m icrocircu lat ion th at feed th e border m al sm all an d large re-en t ran t w avelets in th e left at rium . Th ese
zon es of th e brain . Cardiogen ic em bolism sh ou ld be differen t i- currents require a trigger and an abnorm al substrate. The currents

216

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17 Medical Management of Cardiogenic Cerebral Embolism 217
Table 17.1 CHADS2 Score sion th erap ies for m yocardial in farct ion do n ot overcom e th is
Characteristic Points risk.4 Left ven t ricular th rom bus in creases th e risk of cardioem -
bolic st roke five-fold, w ith st roke occurring in 10% of pat ien t s
Recent congestive heart failure 1
w ith left ven t ricu lar th rom bus com pared w ith 2%for m yocardial
Hypertension 1
in farct ion w ith ou t left ven t ricu lar th rom bus.5 How ever, it is un -
Age at least 75 years 1
clear if th e risk is sign ifican tly in creased in pat ien t s w ith hypoki-
Diabetes mellitus 1
n et ic segm en ts w ith out left ven t ricu lar th rom bu s. Of n ote, m ost
Prior stroke or transient ischemic at tack 2
left ven t ricu lar th rom bi develop early, but som e occur after h os-
pit alizat ion ; 50% are detected du ring h osp italizat ion w ith 90%
detected w ith in 3 m on th s.6
are in itiated by pulm on ar y vein t riggers located in m yocardial
m uscular sleeves th at exten d for 1 to 3 cm in to th e four pulm o-
Cardiomyopathy and Left Ventricular Thrombus
n ar y vein s an d by n onpulm on ar y vein t riggers located in th e left
atrium . The five m ajor autonom ic ganglion ic plexuses are located Isch em ic h ear t disease is a prevalen t cause of cardiom yopathy
ep icardially in t h e in terat rial groove an d along th e ligam en t of an d congest ive h ear t failu re (CHF). Alth ough cardiom yopathy is
Marsh all n ear orifices of t h e pu lm on ar y vein s. In syn ergy w ith n ot rest ricted to th e left ven t ricle, dilat ion of th e left ven t ricle in
pu lm on ar y vein t riggers, th ese foci h ave been im plicated in su s- th is con dit ion h as led to in terest in it as a cu lp rit in cardiogen ic
tain ing at rial fibrillat ion . As a subst rate for at rial fibrillat ion , th e em bolism . In som e cases th rom bi h ave been dem on st rated to
t issu e of th e left at riu m u n dergoes rem odeling in resp on se to form w ith in th e left ven t ricle w ith subsequ en t em bolizat ion . In
h igh at rial rates an d in path ological st ates such as coron ar y ar- prosp ect ive st u dies th e rates of cerebral em bolism in pat ien ts
ter y disease an d m it ral sten osis. From an an atom ic perspect ive, w ith left ven t ricular eject ion fract ion < 35% ranged from 1.5 to
th e left at rial ap p en dage is th e site at w h ich m ost th rom bi form 4% per year. W h eth er pat ien t s w ith cardiom yopathy w h o h ave
in th e set t ing of at rial fibrillat ion . Th e im p airm en t of elect rical already h ad a st roke or TIA h ave a sign ifican tly h igh er risk of re-
con d u ct ion w ith in th e at rial w all an d su bsequ en t im paired at rial curren t st roke th an in dividuals w ith n o h istor y of cerebrovascu-
con t ract ion leads to st asis p redisp osing to th rom bosis. Th e left lar isch em ia is u n kn ow n . Congest ive h ear t failu re often coexists
at riu m is frequ en tly dilated in pat ien ts w ith at rial fibrillat ion . w ith at rial fibrillat ion ; th ese pat ien ts h ave a risk of recurren t
At rial flut ter is an oth er arrhyth m ia th at in terrupt s efficien t st roke th at is h igh er th an th at of pat ien t s w ith eith er con dit ion
at rial cont raction and predisposes individuals to cardiogen ic em - alon e.
bolism . Alth ough th e dat a are less robu st to quan t ify th e risk as-
sociated w ith at rial flu t ter, p at ien ts are t reated sim ilarly to th ose
w ith at rial fibrillat ion . Valvular Heart Disease
Th e fin al com m on rhyth m con siderat ion in card iogen ic em - Rheumatic Valve Disease
bolism is sin us n ode dysfun ct ion an d th e use of pacem akers.
Sin u s n ode dysfu n ct ion , or th e sick sin u s syn drom e, h as m any On ce a m ajor cause of cardiovascular disease, rh eu m at ic valve
cau ses beyon d th e scop e of th is ch apter. It s im p or t an ce lies in disease h as becom e rare in th e develop ed w orld. Of rh eu m at ic
th at it m ay lead to th e t achy–brady syn d rom e an d th at it m ay valve disease, m it ral valve disease h as th e st rongest associat ion
requ ire a pacem aker for t reat m en t . In t h is syn drom e episodes of w it h card ioem bolic st roke. Th e rate is 9.6% p er year w it h ou t
su p raven t ricu lar tachycardia, su ch as at rial fibrillat ion an d at rial an t icoagulat ion th erapy.7 Most of th ese pat ien t s also h ave at rial
flu t ter, altern ate w ith periods of bradycardia. Sym ptom at ic bra- fibrillation.8 Throm bi often form in the left atrium , particularly in
dycardia m ay be th e first sym ptom to develop. Th e n ecessar y use the left at rial appendage.9 In the absen ce of atrial fibrillation, the
of pacem akers in th ese pat ien t s often obscures th e abilit y to in - risk of cerebral em bolism associated w ith rh eu m at ic m it ral valve
terpret su bsequen t elect rocardiogram s (ECG) an d to detect at rial disease is u n clear. Th e risk of cardiogen ic em bolism is h igh th e
fibrillat ion or at rial flut ter sh ould th e pat ien t develop isch em ic first year after stroke, and m ost em boli occur w ithin 6 m onths.8
st roke. Th an kfu lly, t h ese p acem akers can be in ter rogated for Other rheum atic valvular lesions are not thought to be associated
at rial arrhyth m ias. w ith such a h igh risk of th rom bus form at ion an d em bolizat ion .

Mitral Valve Prolapse, Mitral Annular Calcification, and


Left Ventricular Thrombus, Acute Myocardial
Aortic Sclerosis
Infarction, and Cardiomyopathy
W h et h er m it ral valve p rolap se, m it ral an n u lar calcificat ion , or
Acute Myocardial Infarction and Left aor t ic sclerosis resu lt s in st roke is u n cer t ain . Of t h ese lesion s,
Ventricular Thrombus aor t ic sclerosis h as n o dem on st rated excess risk of st roke.10,11
Myocardial in farct ion is associated w ith subsequen t isch em ic Mit ral an n u lar calcificat ion h as th e st rongest associat ion ; h ow -
st roke. Ap ar t from t h e p revalen ce of sim ilar risk factors in both ever, it is u n cer tain if it is a m ere m arker of st roke risk.12
grou p s of p at ien t s, n am ely, advan ced age, hyp er ten sion , hyp er-
lip id em ia, an d d iabetes, ot h er u n iqu e sit u at ion s are w or t h
Prosthetic Heart Valves
m en t ion ing. Myocardial in farct ion often lead s to hyp okin et ic
segm en t s of th e left ven t ricle. A th ird of pat ien ts w ith an terior Th e risk of card iogen ic em bolism w ith p rosth et ic h ear t valves
m yocardial in farct ion w h o do n ot u n dergo reperfu sion th erapy dep en ds on w h ich valve is rep laced (m it ral versu s aor t ic), th e
develop left ven t ricu lar th rom bu s in th e first 2 w eeks. Reperfu - t yp e of valve (biop rost h et ic versu s m ech an ical), an d op erat ive

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218 III Ischemic Stroke and Vascular Insufficiency

tech n ique (open versus en dovascu lar). Bioprosth et ic valves in Paradoxical Embolism
p at ien t s w it h sin u s rhyth m are associated w it h on ly a m ild in -
creased risk of st roke, esp ecially in p at ien t s on an t ip latelet s. Paradoxical em bolism refers to em bolizat ion of m aterial from
Bioprost h et ic m it ral valves are associated w ith a sligh tly h igh er th e ven ou s, righ t -sided circu lat ion , to th e ar terial, left-sided cir-
risk of st roke th an aort ic valves du ring th e first 3 m on th s after culat ion . Th ese righ t-to-left sh un ts m ay occu r from abn orm al
replacem ent. This association led to a recom m endation for short- con n ect ion s w ith in th e h ear t , m ost com m on ly, a paten t foram en
ter m an t icoagu lat ion t h erapy. Pat ien t s w it h m ech an ical p ros- ovale or, rarely, ext racardiac sh u n t , as in pulm on ar y ar teriove-
th et ic valves are at in creased risk of st roke. Th e st roke risk w ith n ous m alform at ion s. Paradoxical em bolism h as been invoked as
obsolete caged-ball m ech an ical valves is h igh er th an w ith n ew er a cau se of st roke in pat ien ts w h o w ould oth er w ise be classified
gen erat ion t ilt ing-disk m ech an ical valves or bileaflet m ech an ical as h avin g cr yptogen ic st roke. Paten t foram en ovale, a rem n an t
valves. Pat ien t s w ith prosth et ic h ear t valves are at risk of at rial of t h e fet al circu lat ion , is m ore p revalen t in p at ien t s w it h cr yp -
fibrillat ion an d in fect ive en docardit is, both of w h ich m odify risk togen ic st roke (45%) th an in th ose w ith a d eterm in ed cau se of
of st roke an d t reat m en t recom m en dat ion s. st roke (23%).13 Fu r th erm ore, m ediu m -to-large p aten t foram en
ovales are m ore com m on in cr yptogen ic st roke pat ien t s (26%)
com p ared w ith sm aller paten t foram en ovale (6%) an d are asso-
Infective Endocarditis
ciated w ith em bolic p at tern s on MRI.13
In fect ive en docardit is is an un com m on but im por tan t cau se of Non eth eless, paten t foram en ovale is ver y com m on (15 to
card iogen ic em bolism . Th e sou rce of em bolism is veget at ion s, 38%) in pat ien t s w h o n ever h ave an isch em ic st roke.14,15 Both in
con sist in g of bacter ia, p olym or p h on u clear cells, p latelet s, an d st roke p at ien t s an d n orm al pop u lat ion s, th e in ciden ce of p aten t
fibrin th at form on th e h ear t valves (n at ive or prosth et ic). In th e foram en ovale decreases w ith age.14 Oth er risk factors, such as
era before an t ibiot ics, em bolic rates of 70 to 97% w ere com m on . hyper ten sion , ath erosclerosis, an d at rial fibrillat ion , in crease be-
In fect ive en docardit is of th e left h ear t valves predisposes a pa- yon d th e age of 55 years, w hich is th e usual cutoff for stroke in the
t ien t to cerebral em bolizat ion , th e m ost frequ en t site of em boli- you ng. Th ese factors accou n t for m ost recu rren t st rokes associ-
zat ion . Prosth et ic valve en docard it is h as an even h igh er em bolic ated w ith advan cing age. Th erefore, m any cases of patent foram en
poten t ial. Th ese sept ic em boli frequ en tly cau se sp on tan eou s ovale th at are detected on rout in e evaluat ion of st roke pat ien t s
h em orrh agic t ran sform at ion of cerebral in farcts as w ell as m y- are likely in ciden tal. Oth er st u dies show ed th at m ediu m to large
cot ic an eu r ysm s in th e cerebral circu lat ion in som e cases. Th e paten t foram en ovales are m ore com m on in cr yptogen ic st roke.
in it ial in farct s m ay be sym ptom at ic or asym ptom at ic. Th e m ag- Th e Paten t Foram en Ovale At r ial Sept al An eu r ysm (PFO-ASA)
netic resonance im aging (MRI) pattern ranges from single lesion s st u dy fou n d th at p aten t foram en ovale sh u n t size w as n ot p re-
to n um erous lesion s of any size, w h ich m ean s th at in farct s due to dict ive of recu rren t st roke risk.16 For t un ately, th e risk of recu r-
in fect ive en docardit is can m im ic oth er causes of em bolic st roke ren t st roke is low for in dividu als on aspirin : 2% in 4 years.15–17
(Fig. 17.1). Pat ien ts in th e PFO-ASA st udy w ere you nger th an 55 years of
age. Oth er st u dies h ave sh ow n th at st roke in p at ien ts w ith paten t
foram en ovale w h o h ave a recurren t st roke h ave a differen t cause
Nonbacterial Thrombotic Endocarditis and
in a th ird of cases.18 It is im por t an t to search th orough ly for oth er
Libman-Sacks Endocarditis
cau ses of st roke before th e sou rce of em bolism is at t ribu ted to
Tw o form s of noninfective endocarditis w arrant m ention. In both paten t foram en ovale in p at ien ts w ith cr yptogen ic st roke. In p ar-
con d it ion s sterile veget at ion s form on th e leaflet s of th e cardiac t icu lar, p aroxysm al at rial fibrillat ion , sm all vessel disease, in t ra-
valves—th e aor t ic or m it ral valve in n on bacterial th rom bot ic en - cranial stenosis, and arterial dissection are other m ore established
docardit is or th e m it ral valve in Libm an -Sacks. In n on bacterial cau ses th at can easily be m issed. In pat ien t s w ith cr yptogen ic
th rom bot ic en docardit is, also kn ow n as m aran t ic en docardit is, st roke w h o h ave a paten t foram en ovale, cau ses of ven ou s th rom -
th e veget at ion s con t ain p latelet s an d fibrin w ith ou t an in flam - bosis besides ar terial th rom bosis m ay be relevan t , for exam ple,
m ator y in filt rate. Non bacterial th rom bot ic en docardit is prim ar- acquired an d in h erited hypercoagu lable states, as listed below.19
ily occu rs in p at ien ts w ith can cer, bu t it also can occur in pat ien t s
w ith dissem in ated in t ravascular coagulat ion in sepsis. In Lib -
Other Considerations in Patients w ith
m an -Sacks en docardit is, w h ich occurs in pat ien ts w ith system ic
Paradoxical Embolism
lu pu s er yth em atosu s or th ose w ith an t iph osp h olip id syn drom e,
th e veget at ion s con t ain m on on u clear in flam m ator y cells an d An oth er an atom ic con siderat ion is th e presen ce of an at rial sep -
im m u n e com plexes in add it ion to p latelets an d fibrin . tal an eur ysm associated w ith a paten t foram en ovale, w h ich oc-
In both con dit ion s th e size of th e vegetat ion s var y an d m any curs in 4 to 9% of st roke pat ien t s w ith paten t foram en ovale.16,17
are less t h an 3 m m . Tran sesop h ageal ech ocard iograp hy (TEE) is Again , p rosp ect ive coh or t st u dies h ave dem on st rated con flict ing
a bet ter ch oice th an t ran sth oracic ech ocardiography (TTE) for resu lt s regarding risk of recurren t st roke. Th e PFO-ASA st udy
diagn osis of th ese lesion s. Non bacterial th rom bot ic en docardit is suggested an in creased risk of 15% over a p eriod of 6 years in
(NBTE) is th ough t of as a hypercoagu lable st ate. Alm ost invari- pat ien ts w ith septal defect s, w h ereas th e Paten t Foram en Ovale
ably in NBTE, t h ere is a p at ter n of m u lt ip le cerebral in farct ion s in Cr yptogen ic St roke St udy (PICSS), w h ich in cluded older pa-
of various sizes on MRI: sm all (< 10 m m ) an d large (> 30 m m ). t ien ts, did n ot .20,21
Patients often present w ith em bolic encephalopathy before m ajor In su m m ar y, for th e in dividual st roke pat ien t , th e p resen ce of
focal even ts. Rarely, in pat ien ts w ith Libm an -Sacks en docardit is, paten t foram en ovale on test ing is in su fficien t to at t ribu te cau sa-
su p erim p osed bacterial en docardit is h as been rep or ted in th ose t ion to it . St roke du e to PFO m ay be con sidered in p at ien t s <55
w h o h ave un dergon e im m u n osu p p ressive th erapy. years old, w ith m ediu m -large PFO size, w ith an em bolic pat tern

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17 Medical Management of Cardiogenic Cerebral Embolism 219

a b

Fig. 17.1a–c Magnetic resonance im aging of the brain in a patient with


bacterial endocarditis. Axial im ages show num erous infarcts in multiple
vascular territories in both hem ispheres (a,b) and tiny hem orrhagic areas
within the infarcts (c). c

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220 III Ischemic Stroke and Vascular Insufficiency

a b

Fig. 17.2a,b Im aging of 44-year-old patient with patent foram en ovale salva maneuver. (b) Magnetic resonance im age dem onstrating t ypical pat-
and embolic strokes. (a) Transcranial Doppler ultrasonogram of the m iddle tern of infarction.
cerebral arteries shows m ultiple high-intensit y transient signals after a Val-

of in farct ion on MRI, after com pet ing causes h ave been th or- involving th e an terior an d posterior circu lat ion . Th e first ep isode
ough ly ruled ou t (Fig. 17.2). of card iogen ic em bolism m ay be clin ically ap p aren t or silen t ,
d ep en ding on th e involvem en t of eloquen t st ru ct ures.
Th e clin ical feat u res of each st roke syn drom e are determ in ed
Cardiac Procedures by th e st ruct ures supplied by th e occluded vessel. Th e size of car-
Several cardiac procedu res can be classified as cau ses of card io- dioem bolic m aterial, th rom bi, or vegetat ion s varies. Th erefore,
gen ic em bolism . Th e risk of st roke varies w ith th e procedure an d any blood vessel in th e cerebral circulat ion m ay be affected w ith
w ith evolu t ion of th e tech n ique. Th e perioperat ive risk associ- th e resultan t w ide variet y of presen tat ion . Accordingly, clin ical
ated w ith coron ar y cath eterization is low for diagn ostic (0.03–3%) feat ures alon e are in sufficien t to dist inguish bet w een cardio-
an d for coron ar y (0.3–0.4%) in ter ven t ion s. Th e risk is h igh er for em bolic an d n on cardioem bolic cau ses of st roke. Pat ien t s m ay
coron ar y ar ter y byp ass graft (CABG, 1.6%) an d h igh est for val- presen t w ith focal d eficit s at t ribu table to cor t ical lesion s, su ch as
vu lar su rger y. Th e r isk is 2.1% for su rgical rep lacem en t , 3.8% isolated aph asia or h an d w eakn ess (“cort ical h an d”) associated
for t ran scath eter aor t ic valve replacem en t , an d 8% for m ultiple w ith bran ch vessel occlu sion . Mult iple cor t ical an d subcor t ical
valve su rger y.22–25 Many of th ese even ts are th ough t to be due to deficits m ay result from hem ispheric involvem ent from occlusion
m an ipulat ion of aort ic arch ath erom a. In aort ic sten osis, calcific of th e MCA or basilar ar ter y. A com atose state or cran ial n er ve
em boli are an oth er im p or t an t m ech an ism . Th e clin ical m an ifes- deficit s often resu lt from brain stem involvem en t w h en occlu sion
tat ion s, in clu ding cogn it ive deficit s, en ceph alop athy, an d focal of th e basilar ar ter y occu rs due to a cardioem bolic st roke.
deficit s, are p rotean , as discu ssed below. Pat ien ts m ay h ave focal deficit s w ith out cor t ical sign s th at
m ay be in d ist in gu ish able from st rokes related to sm all vessel
d isease, d ep en d in g on t h e st at u s of t h e collateral circu lat ion
Cardiac Tumors an d rapidit y of spon t an eous th rom bolysis. Pat ien ts often pres-
en t w it h asym ptom at ic st rokes id en t ified on im agin g. Closer
Cardiac t u m ors are an exceedingly rare cau se of st roke. At rial
in sp ect ion m ay reveal su bt le cogn it ive d eficit s. Pat ien t s w it h
m yxom a is a n ot able cau se.
m ult iple em bolic st rokes m ay h ave so-called em bolic en ceph a-
lopathy such as after a cardiac bypass or in p at ien t s w ith st rokes
or n on bacterial th rom bot ic en docardit is. Fin ally, spin al cord in -
farct ion m ay be a rare m an ifest at ion of cardioem bolic st roke, as
■ Clinical Presentation in th e case of valvu lar cardiac su rger y. How ever, in m ost of th ese
Th e cardin al m an ifest at ion of cardiogen ic em bolism is th e su d- cases, th e act u al sou rce m ay be t h e aor t a. Alt h ough t h e h all-
den on set of focal n eu rologic deficits related to recu rren t st roke m ark feat u res of recu rren t st roke in m u lt iple vascu lar dist ribu -
in m ult ip le vascular dist ribu t ion s involving both h em isph eres or t ion s suggest cardioem bolic st roke, a cardiac sou rce of em bolism

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17 Medical Management of Cardiogenic Cerebral Embolism 221

sh ou ld be con sidered in ever y pat ien t being evalu ated for isch - or con t rast m edia. TEE is superior to TTE in detect ing left at rial
em ic st roke. th rom bu s (93–100% vs 39–73%), valve veget at ion s (82–100% vs
58–62%), aor t ic arch ath erom a, an d paten t foram en ovale (89–
100%vs 50%respect ively). TEE is com parable to TTE for detect ing
Evaluation of Cardioembolic Stroke
left ven t ricu lar path ology.28 Alth ough TEE is safe, it is n ot u n iver-
Th e evalu at ion of card ioem bolic st roke h as several p u r p oses: sally available an d it requires sedation , w hich m ay be problem atic
con fir m at ion of isch em ic st roke, d ocu m en t at ion of a card iac in som e st roke p at ien t s. TTE can be p erform ed safely w ith ou t
sou rce of em bolism , diagn osis of com pet ing st roke et iologies, hem odynam ic consequences in stroke patients and is less expen -
an d diagn osis of com orbid con dit ion s. Pat ien ts w ith cardioem - sive, easier to perform , an d m ore w idely available th an TEE.
bolic st roke ben efit from st ru ct ural brain im aging w ith MRI or Alth ough it does n ot allow st r uct u ral cardiac im aging, t ran -
com p u ted tom ograp hy (CT) to diagn ose isch em ic st roke, an d im - scran ial Dopp ler (TCD) u lt rason ography is a safe an d reliable
aging of ext racran ial an d in t racran ial vessels by CT angiograp hy, m eth od for evaluat ing righ t-to-left sh un ts. Com pared w ith TEE
MR angiography, or ult rasonography to diagn ose cerebrovascular as th e gold stan dard, TCD has a sen sit ivit y of 91.3% an d a speci-
path ology such as ath erosclerosis or dissection. These tests should ficit y of 93.8%. It s overall accuracy is 92.8%. Th e advan tages of
be in corporated in to th e rout in e evalu at ion of isch em ic st roke TCD for sh un t detect ion are low cost , pat ien t com fort , an d ease
even w h en a cardioem bolic source is su spected because fin dings of perform an ce both in acutely ill pat ien t s an d in th e am bu lator y
often alter m an agem en t . set t ing (Fig. 17.2).32
Decision s on w h ich test to p erform depen d on t h e level of
Detection of Arrhythmia su spicion for each of th e u n d erlying con dit ion s, th e p resen ce of
oth er et iologies, an d available resources. W h en th ere is a h igh
Tw elve -Lead Electrocardiography level of susp icion for en docardit is (in fect ive, n on bacterial th rom -
Elect rocardiogram s detect at rial fibrillat ion in as m any as 25%of bot ic en docardit is or Libm an -Sacks) or at rial th rom bus, it m ay
isch em ic st roke p at ien t s.26 An in it ial ECG id en t ifies th e n ew be m ore efficien t to proceed directly to TEE. In cases suspiciou s
on set of at rial fibrillat ion in 10% of st roke pat ien t s.27,28 At rial fi- for paradoxical em bolism , TEE or a com bin at ion of TTE w ith TCD
brillat ion h as sign ifican t im plicat ion s for m an agem en t an d prog- is an acceptable first-line choice. In other cases, particularly w hen
n osis; t h erefore, ECG sh ou ld be obt ain ed rou t in ely in isch em ic oth er et iologies h ave been foun d, TTE is su fficien t .28
st roke p at ien t s. As m en t ion ed earlier, im p lan t at ion of card iac
pacem akers lim its th e in terp retat ion of ECG. In su ch pat ien ts Magnetic Resonance Imaging of the Brain
fu r t h er in ter rogat ion of rhyt h m is n ecessar y. Th e ST segm en t ,
Magn et ic reson an ce im aging of th e brain is th e best diagn ost ic
Q-w aves, an d left ven t ricu lar hyp er t rophy on ECG are often a
test for cerebral in farct ion . Alth ough MRI is in sufficien t to diag-
sign of acu te or ch ron ic com orbid coron ar y ar ter y disease or car-
n ose cardiogen ic em bolism , th e pat tern of in farct ion h elps sug-
d iom yop at hy. Th ese fin d ings m ay raise t h e in d ex of su sp icion
gest th e cause, raising th e in dex for fur th er test ing in in dividual
for m yocardial in farct ion , m ural th rom bus, or cardiom yopathy as
cases. Cardiogen ic em bolism t yp ically p rodu ces on e of several
th e cause of st roke.
pat tern s: (1) a single large in farct du e to occlu sion of a m ajor
cerebral blood vessel, w ith or w ith out spon t an eous recan aliza-
Inpatient Cardiac Telemetry, Holter Monitoring, and t ion ; (2) m u lt ip le in farct s dist ribu ted bet w een th e cerebru m an d
Long -Term Event Monitoring cerebellum ; an d (3) m ult iple in farct s dist ributed in both h em i-
A m in im um of 24 h ou rs of telem et r y or Holter m on itoring during sph eres (Figs. 17.1, 17.2, 17.3).29 How ever, even pat ien ts w ith
h ospitalizat ion h as been advocated for isch em ic st roke pat ien ts oth er in farct p at tern s on MRI st ill require basic cardiac evalua-
to address th e risk of failing to diagn ose paroxysm al at rial fibril- t ion because a cardiac source is often foun d .29
lat ion . Th e d iagn ost ic yield of th is pract ice h as been reported to
be bet w een 4% an d 8%.29 Holter m on itoring is used in h ospitals Blood Tests
that are not equipped w ith telem etr y in th eir stroke unit and also
m ay be used on an ou t patien t basis. An oth er opt ion for h ospitals Basic blood tests such as a com plete blood pan el, basic ch em ist r y
w ith m in im al resou rces is fou r daily serial ECGs.27 pan el, lip id p rofile, an d screen ing for diabetes by fast ing glu cose
For a selected grou p of p at ien ts, for exam p le, th ose w ith cr yp - or h em oglobin A1c are ap prop riate for all card ioem bolic st roke
togen ic st roke an d especially th ose w ith a cardioem bolic pat tern pat ien ts to search for th e presen ce of com orbidit ies an d risk fac-
on MRI or a d ilated left at r iu m , longer m on itor ing m ay be ap - tors. W h en in fect ive en docardit is is a con cern , obtain ing blood
p rop r iate. Th e n ew er gen erat ion of even t m on itors can d etect cult ures occasion ally h elps con firm th e diagn osis. Th e er yth ro-
arrhyth m ias over longer periods (7 days). Th ese m on itors yield cyte sedim en t at ion rate is often elevated in pat ien ts w ith en do-
an addit ion al 6 to 15% of cases th at w ou ld n ot h ave been de- cardit is, bu t th is test is n on sp ecific. In you ng p at ien t s in w h om
tected by ECG plu s 24-h ou r Holter m on itoring.30,31 a righ t-to-left sh unt is con firm ed, test ing for in h erited an d ac-
qu ired hyp ercoagu labilit y m ay be app ropriate.

Echocardiography
Mandatory Tests in Patients w ith
The m ain conditions identified by echocardiography are left atrial
Paradoxical Embolism
th rom bu s, m u ral th rom bu s, valve veget at ion s, p aten t foram en
ovale, card iom yop athy, an d sign ifican t m it ral valve sten osis. Th e A thorough hypercoagulabilit y work up, including the tests below,
detect ion of p aten t foram en ovale requ ires u se of agitated salin e is m an dator y in all st roke pat ien ts.

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222 III Ischemic Stroke and Vascular Insufficiency

■ Treatment of Cardioembolic Stroke


Th ere are several eviden ce-based m easu res th at im p rove ou t-
com es for pat ien t s w ith acu te isch em ic st roke. Th ese m easu res
also apply to pat ien t s w ith cardioem bolic st roke. Alth ough th is
topic is beyon d th e scope of th is ch apter, possible in ter ven t ion s
in clude th rom bolysis, risk factor m odificat ion , p reven t ion an d
t reat m en t of com p licat ion s, care in a st roke u n it , early reh abili-
tat ion , an d organ izat ion of care in st roke cen ters (Table 17.2).
Th e reader is directed to app ropriate ch apters in th is text .

Treatment of Stroke Due to Atrial Fibrillation


An t icoagulat ion th erapy is th e m ain t reat m en t proven to safely
red u ce t h e r isk of recu r ren t st roke in p at ien t s w ith at r ial fibr il-
lat ion (Tables 17.3 an d 17.4). Th e ben efit s of an t icoagu lat ion
out w eigh th ose of aspirin or com bin at ion an t iplatelet th erapy
in pat ien t s w ith at rial fibrillat ion . Th e risk of m ajor bleeding
is sim ilar w ith w arfarin as w ith th e com bin at ion of aspirin an d
clop idogrel. Th e n ew er oral an t icoagu lan ts—dabigat ran , rivarox-
aban , an d apixaban —h ave been dem on st rated to be n on in ferior
to w arfarin for th e preven t ion of st roke in at rial fibrillat ion . Th e
ch oice am ong differen t an t icoagu lan t s is in dividu alized based on
pat ien t p referen ces, com orbidit ies, an d resou rces. Th is sect ion
review s th e applicat ion of an d eviden ce for th e variou s t h erapies
to reduce th e risk of st roke in at rial fibrillat ion .

Fig. 17.3 Magnetic resonance im age of the brain in a patient with atrial Warfarin
fibrillation demonstrates a pat tern suggestive of cardioembolic stroke. Note
War far in t h erapy to red u ce st roke in p at ien t s w it h at r ial fibr il-
involvement of multiple vascular territories in both hemispheres, acute right
middle cerebral artery infarct, and clinically asymptomatic chronic posterior lat ion began in t h e 1940s. War far in , a vit am in K an t agon ist , is a
cerebral artery infarcts bilaterally. vit am in K ep oxid e red u ct ase in h ibitor t h at im p airs t h e avail-
abilit y of redu ced vit am in K, w h ich is n ecessar y for th e carbox-
ylat ion of several clot t ing factors: p roth rom bin (factor II) an d
• Protein C an t igen an d act ivit y factors VII, IX, an d X (Table 17.4). Th e developm en t of th e in ter-
• Protein S an t igen an d act ivit y n at ion al n orm alized rat io (INR) en abled m ore reliable m easure-
• An t ith rom bin III an t igen an d act ivit y m en t of t h e an t icoagu lan t effect . Th e t arget INR of 2.5 (ran ge 2
• Factor V Leiden m u tat ion to 3) h as been est ablish ed for w arfarin th erapy in pat ien ts w ith
• Proth rom bin gen e m u tat ion atrial fibrillation.33 Patients w ith an INR of less than 2 are at a m uch
• Act ivated protein C resist an ce h igh er risk of isch em ic st roke; pat ien ts w ith an INR of greater

Table 17.2 Acute Care Setting Interventions and Risk-Factor Modification in Cardioembolic Stroke

Blood pressure (BP) Hyperacute set ting: goal of < 220/120 mm Hg (or < 185/110 mm Hg for patients receiving thrombolytics), avoid
hypotension, BP < 100 m m Hg systolic, or mean arterial pressure (MAP) < 70
After 24 hours: gradual BP reduction
Long-term BP goal of < 135/85 m m Hg or close to normal: 120/80 mm Hg
Cholesterol Target: < 70 mg/dL or at least 50% reduction in low-densit y lipoprotein
Statins are the preferred agents
Smoking Smoking cessation interventions should begin during the hospitalization
Interventions: counseling, consider nicotine replacement or pharmacological interventions to aid smoking cessation
Physical inactivit y Goal: safe return to physical activit y and regular exercise
Interventions: tailored initial (and subsequent) exercise regimen based on physical rehabilitation planning
Acute care set ting Care in a dedicated stroke unit (or by a stroke team and trained nurses if a stroke unit is not feasible)
Regional organized care in stroke centers
Early mobilization
Deep venous thrombosis prophylaxis, pharmacological management using heparin subcutaneously or low-
molecular-weight heparin, or nonpharmacological managem ent
Physical rehabilitation planning beginning on the first day after stroke
Assessment of risk of aspiration prior to oral feeding
At tention to skin care

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17 Medical Management of Cardiogenic Cerebral Embolism 223

Table 17.3 Summary Recommendations for Secondary Prevention of Cardioembolic Stroke

Cardiogenic Embolism Subgroup Recommended Therapy Comment

Arrhythmia
Atrial fibrillation Anticoagulation (warfarin international normalized ratio Well-quantified risk of recurrent stroke;
Atrial flut ter [INR] 2–3, dabigatran, rivaroxaban, apixaban) therapy supported by high-qualit y
Sick sinus syndrom e evidence
Left ventricular disease
Myocardial infarction Antiplatelet therapy if no thrombus is present Well-quantified risk of stroke
Left ventricular thrombus Anticoagulation (warfarin INR 2–3) for at least 3 months Well-quantified risk of stroke; therapy
supported by good evidence
Cardiomyopathy without Patients with stroke: Unclear stroke risk in patients with stroke
ventricular thrombus Anticoagulation (warfarin INR 2–3) for at least and cardiomyopathy
3 months Or antiplatelet therapy
Patients without stroke (i.e., primary prevention):
Antiplatelet therapy
Valvular disease
Rheumatic valve disease Stroke with severe mitral disease: Frequent association bet ween mitral
Anticoagulation (warfarin INR 2–3) lesions and atrial fibrillation; therapeutic
Other rheumatic lesions: recomm endation based on observational
Antiplatelet therapy studies and expert opinion
Prosthetic heart valves Metallic valves:
Anticoagulation (warfarin INR 2.5–3.5)
Bioprosthetic valves:
Antiplatelet therapy, consider anticoagulation in
patients failing antiplatelet therapy
Infective endocarditis Antibiotic therapy; avoid anticoagulation; avoid High risk of hemorrhagic transformation
thrombolysis
Nonbacterial throm botic Treatment of the underlying disorder and Thrombosis in this condition thought to be
endocarditis (NBTE) anticoagulation with heparin independent from vitamin K activation
Libman-Sacks endocarditis Treatment of underlying disease (e.g., systemic lupus Superimposed infective endocarditis also
erythem atosus [SLE]) must be considered
Anticoagulation
Mitral valve prolapse, mitral Antiplatelet therapy Uncertain if these are independent risk
annular calcification factors for stroke; no high-qualit y
evidence for secondary prevention
Cardiac procedures
Cardiac catheterization Antiplatelet therapy Thorough investigation of other causes is
Coronary artery bypass grafts necessary
(CABG)
Valvular surgery
Cardiac tumors
Myxoma Treatment of myxoma
Paradoxical embolism
Patent foramen ovale (PFO) Anticoagulation (warfarin INR 2–3) Association only applies in patients < 55
or single-agent antiplatelet therapy years old after thorough investigation of
PFO closure only in set ting of clinical trials until benefit other causes of stroke
is demonstrated

th an 3 are at a h igh er risk of in t racran ial h em orrh age.33 Experi- reduct ion for recurren t isch em ic st roke, w ith 1.5% per year in
m en tal eviden ce suggest th at alth ough INR prolongat ion occurs pat ien ts on w arfarin an d 4.5%p er year in p at ien ts on th e placebo
w ith in 2 days of w arfarin adm in ist rat ion , th e an t ith rom bot ic ef- in p rim ar y preven t ion s st u dies an d 4% an d 12% per year in sec-
fect takes 4 m ore days. Th e h alf-life of w arfarin is 36 to 48 h ou rs. on dar y p reven t ion st u d ies.35–37 Overall t h e h em or rh age rate
Due to m et abolism by cytoch rom e P-450 2C9 an d binding to w ith w arfarin is n ot h igh (1.3%) com pared w ith a placebo (1%) or
plasm a protein s, m any dr ugs an d food s in terfere w ith w arfarin aspirin for th e prim ar y preven t ion of st roke. Th e rate in creases
m et abolism . Th e INR m u st be m on itored frequ en tly. Even in con - to 2.8% per year for w arfarin an d 1% per year for aspirin in sec-
tem porar y clin ical t rial set t ings, pat ien ts are con t rolled w ith in on dar y preven t ion st u dies.36,38 Th e risk of at rial fibrillat ion in -
th is range on ly 60 to 65% of th e t im e.34 creases w ith age, as does the risk of recurrent stroke in patients
In ran dom ized con t rolled t rials, w arfarin h as been dem on - w ith atrial fibrillation.39 Given concerns that the risk–benefit ratio
st rated to be su p er ior to a p lacebo, su p er ior to asp ir in , an d su - of w arfarin m ay be different in older patients, the Birm ingham
p erior to aspirin plus clopidogrel, an d th e t reat m en t effect as Atrial Fibrillation Treatm en t of the Aged (BAFTA) st udy w as p er-
m easured again st a placebo is large. Th ere w as a 68%relat ive risk form ed in patients older than 75 years random ized to treat m en t

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224 III Ischemic Stroke and Vascular Insufficiency

Table 17.4 Comparison of Anticoagulants

Onset of
Anticoagulant Action Half-Life Elimination Mechanism of Action Dosing Monitoring

Warfarin Days 20–60 hours Liver by Vitamin K antagonist Daily to maintain INR 2–3 for INR
cytochrome (vitamin K epoxide most indications
P-450 reductase inhibitor)
Dabigatran 0.5–2 hours 12–17 hours 80% renal Dabigatran etexilate 150 mg b.i.d. or 110 mg b.i.d.; None required; a
prodrug is 75 mg b.i.d. if CrCl 15–30 mL/ normal PTT
converted to min suggests very lit tle
dabigatran, a direct dabigatran effect;
thrombin inhibitor normal TT excludes
dabigatran effect;
ECT has best test
characteristics
Rivaroxaban 2–4 hours 5–9 hours 66% renal; 28% Direct factor Xa 20 mg daily; None required,
hepatic/fecal inhibitor 15 mg daily if CrCl 15–49 mL/ however, consider
min anti-factor Xa
activit y when
testing is needed
Apixaban 3–4 hours 12 hours Combined Direct factor Xa 5 mg t wice daily for most None required,
hepatic inhibitor patients. The does should however, consider
CYP3A4 and be adjusted to 2.5 mg t wice anti-factor Xa
renal daily in patients with at least activit y when
t wo of the following: age testing is needed
>80 years, body weight
<60kg, serum creatinine
level >1.5 mg/dL (133
µm ol/L)
Abbreviations: INR, international norm alized ratio; b.i.d., t wice daily; CrCl, creatinine clearance; PTT, partial throm boplastin tim e; TT, thrombin tim e; ECT, ecarin clot ting
tim e; CYP, cytochrom e P-450.

w ith w arfarin or aspirin .38 Even th ough m ost p at ien t s w ere older An t icoagu lat ion Th erapy (RE-LY) t rial exam in ed t w o dosing regi-
th an 80 years, th e st u dy dem on st rated ben efit s of w arfarin in m ens of dabigatran against w arfarin.34 The 110 m g t w ice daily
th e preven t ion of isch em ic st roke w ith ou t an excessive h em or- d ose w as n on in fer ior to w arfar in t h erapy for p reven t ing recu r-
rh age rate (1.4%p er year w ith w arfarin versu s 1.6%per year w ith ren t isch em ic st roke. How ever, a dose of 150 m g t w ice daily w as
aspirin ).38 superior to w arfarin . At th is dose, dabigat ran h ad a rate of m ajor
Som e p at ien t s st ill h ave an isch em ic st roke w h ile on w arfarin h em orrh age th at w as sim ilar to th at of w arfarin . War far in -
w ith a th erapeut ic INR. In th ese pat ien t s it is especially pruden t t reated p at ien t s in RE-LY h ad a t h erap eu t ic INR 64% of th e t im e,
to look for oth er causes of st roke, such as carot id ar ter y sten osis. w h ich is t ypical for clin ical t rial set t ings. How ever, t h ere w ere
In creasing th e t arget INR to greater th an 3 is associated w ith a m ore in t racran ial h em orrh ages in p at ien t s on w arfarin an d m ore
h igh er rate of m ajor h em orrh age in th e absen ce of dat a sh ow ing gast roin test in al h em or rh ages in p at ien t s w ith dabigat ran .
in creased efficacy. Fu r th erm ore, th e eviden ce does n ot supp or t Th ere are cer t ain clin ical scen arios in w h ich assessing dabiga-
the com bin ation of w arfarin an d aspirin for th e treatm ent of atrial tran anticoagulation is im portant: pat ients un dergoing em ergen t
fibrillat ion , even in pat ien t s w ith con com it an t stable coron ar y su rger y or vict im s of t rau m a. In th ese sit u at ion s th e proth rom -
ar ter y disease. Th e risk of h em orrh age associated w ith th e com - bin t im e (PT) an d INR are n ot useful. Th e par t ial th rom boplast in
binat ion is h igh er (3.9%) th an th e risk caused by at rial fibrillat ion t im e (PTT) is sen sit ive, bu t it h as a n on lin ear resp on se to dabiga-
(2.3%).40 Th erefore, u n less t h ere are oth er com pelling in dicat ion s t ran . If t h e PTT is com p letely n or m al, t h e p at ien t likely h as n o
su ch as acu te coron ar y syn drom es or sit u at ion s involving m e- or ver y lit tle an t icoagu lan t effect . How ever, pat ien t s w ith even
ch an ic h ear t valves or sten t s, th e com bin at ion of w arfarin p lu s m ildly elevated PTT m ay have a considerable effect of dabigatran.
asp irin sh ou ld be avoided. Th e th rom bin t im e (TT) is also p rolonged in pat ien t s on dabiga-
tran an d is a m ore reliable test than PTT; a norm al TT excludes th e
effect of dabigat ran . Th e ecarin clot t ing t im e (ECT), w h ich is n ot
Dabigatran
yet available clin ically, h as a lin ear relat ion sh ip w ith dabigat ran
An t icoagulat ion th erapy u sing dabigat ran , a direct th rom bin in - an d m ay be a bet ter test . An effect ive reversal agen t does n ot yet
h ibitor, is a proven altern at ive to w arfarin in pat ien ts w ith at rial exist for dabigat ran . Du e to it s low p rotein bin ding, dabigat ran is
fibrillation. Dabigatran etexilate, the prodrug, is converted to dabi- exp ected to be dialyzable. Fin ally, for pat ien ts w ith sign ifican t
gat ran , w h ich h as a rapid on set of an t icoagulat ion (0.5–2 h ours) renal im pairm ent (creatinine clearance of 15 to 30 m L per m inute)
an d a h alf-life of 12 to 17 h ou rs, an d requires n o laborator y m on i- w h o ch oose to use dabigat ran , th e U.S. Food an d Drug Adm in is-
toring (Table 17.4). The Random ized Evaluation of Long-Term t rat ion (FDA) h as recom m en ded dabigat ran 75 m g t w ice daily.

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17 Medical Management of Cardiogenic Cerebral Embolism 225

Rivaroxaban pirin offset any ben efit over asp irin alon e in pat ien ts w ith at rial
fibr illat ion . Toget h er, p rolon ged com bin at ion clop id ogrel p lu s
Rivaroxaban is a direct factor Xa in h ibitor w ith ou t an t ith rom bin
aspirin sh ou ld be avoided in pat ien ts w ith at rial fibrillat ion un -
III m ediat ion . Rivaroxaban h as an on set of act ion of 3 h ours an d
less a clear in dicat ion is dem on st rated.
a h alf-life of 5 to 9 h ours, an d does n ot require m on itoring for
dosing (Table 17.4). Th e effect iven ess of rivaroxaban w as exam -
in ed again st w ar far in in a ran d om ized con t rolled t r ial in n on - Endovascular and Surgical Interventions
valvular at rial fibrillat ion : Rivaroxaban On ce-daily Oral Direct
Factor Xa In h ibit ion Com p ared w ith Vit am in K An t agon ism for En dovascu lar an d su rgical in ter ven t ion s in at rial fibrillat ion are
Preven t ion of St roke an d Em bolism Tr ial in At r ial Fibr illat ion targeted at exclu ding th e left at rial appen dage from th e circula-
(ROCKET-AF).41 Rivaroxaban 20 m g daily w as sh ow n to be n on - t ion an d th erap ies aim ed at rhyth m con t rol.
in ferior to w arfarin w ith regard to recurren t st roke preven t ion Th e Watch m an device w as design ed to exclu de th e left at rial
an d did n ot lead to an excess of m ajor h em orrh ages. Warfarin - appen dage from th e circulat ion . It w as st udied in th e Watch m an
t reated pat ien ts in ROCKET-AF h ad a th erap eu t ic INR 55% of th e Left At rial Appen dage System for Em bolic Protect ion in Pat ien ts
t im e. As in th e case of dabigat ran , PT an d INR are u n reliable m ea- w ith At rial Fibrillat ion (PROTECT AF) st udy, w h ich en tailed per-
su res w ith rivaroxaban . An t i–factor Xa assay (factor Xa act ivit y) cutan eous closure of th e left at rial appen dage versu s w arfarin
is prom ising as a m easu re of rivaroxaban effect . Th e dose of riva- th erapy for preven t ion of st roke in p at ien t s w ith at rial fibrilla-
roxaban is 15 m g daily in patients w ith renal im pairm ent and cre- t ion . Th is st u dy fou n d th at th e even t rate for recu rren t st roke in
at in in e clearan ce of 30 to 49 m L p er m in u te. High p lasm a p rotein th e device grou p w as com p arable to th at in th e w arfarin -t reated
bin ding m akes it u n likely th at rivaroxaban w ou ld be dialyzable. pat ien ts. How ever, th ere w ere m ore p rocedu ral com p licat ion s,
som e of w h ich w ere seriou s. Use of th e device in th e t rial also
required a com plex antithrom botic regim en: warfarin for 45 days,
Apixaban
follow ed by aspirin plu s clopidogrel, follow ed by aspirin m on o-
Apixaban is a factor Xa in h ibitor w ith out an t ith rom bin III m edia- t h erapy. Fu r t h er m ore, su ccessfu l d evice im p lan t at ion en abled
t ion . Apixaban h as an on set of act ion of 3 to 4 h ou rs, a h alf-life of w arfarin to be discon t in u ed w ith in 45 days in 86% of pat ien ts.
12 h ou rs, an d does n ot require m on itoring for dosing (Table Follow -u p in th is st u dy w as on ly 18 m on th s. Th erefore, alth ough
17.4). The effectiveness of apixaban for prevention of cardiogenic occlusion of the left atrial appendage is a prom ising target for future
em bolism in at rial fibrillat ion w as exam in ed again st w arfarin research , it is n ot yet ready to rep lace an t icoagu lat ion th erapy.
an d again st aspirin in th e Apixaban for Reduct ion in St roke an d
Oth er Th rom boem bolic Even ts in At rial Fibrillat ion (ARISTOTLE)
and Apixaban Versus Acet ylsalicylic Acid (ASA) to Prevent Strokes Rhythm Control
(AVERROES) st u dies, resp ect ively.42,43 Ap ixaban 5 m g t w ice daily Th e Atrial Fibrillation Follow -up Invest igation of Rhythm Manage-
w as sh ow n to be n on in ferior to w ar farin in term s of recu rren t m en t (AFFIRM) st udy dem on st rated th at a st rategy of rate con -
st roke p reven t ion . How ever, ap ixaban - t reated p at ien t s h ad a t rol im p roved m or talit y w h en com pared w ith st rategy of rhyth m
low er m or talit y an d m ajor h em orrh age rate th an p at ien ts t reated con t rol in p at ien t s w ith at rial fibrillat ion .46 How ever, AFFIRM
w ith w arfarin . Warfarin -t reated patien ts in ARISTOTLE h ad a u sed m edicat ion s for rhyth m con t rol. Th e develop m en t of m ore
th erap eu t ic INR 62% of th e t im e. W h en com pared w ith aspirin effect ive cath eter-based pulm on ar y vein isolat ion an d oth er ab -
for th e t reat m en t of at rial fibrillat ion, apixaban w as m ore effec- lat ion p rocedu res h as rekin dled in terest in rhyth m con t rol for
t ive in preven t ing cardioem bolism w ith ou t an excessive h em or- at rial fibrillat ion . Th ese th erap ies su ccessfu lly con t rol at rial flu t-
rh age rate.42 An t i–factor Xa act ivit y m ay be con sidered w h en th e ter an d, less so, at rial fibrillat ion . It rem ain s to be determ in ed if
apixaban effect m u st be m easured. Th e dose of apixaban sh ould th e risk of recu rren t st roke after ablat ion of at rial fibrillat ion can
be adjusted to 2.5 m g t w ice daily in p at ien ts w ith at least t w o of be reduced to levels com p arable to th ose w ith an t icoagulat ion .
the follow ing factors: age > 80 years; body w eight < 60 kg; a serum
creat in in e level > 1.5 m g/dL (133 µm ol/L).
Treatment of Stroke Due to Left
Antiplatelet Agents Ventricular Thrombus
An t icoagu lan ts are m uch m ore effect ive th an an t iplatelet agen ts Based on resu lt s for t h ree sm all ran d om ized con t rolled t r ials
in p reven t ing recu rren t st roke in pat ien t s w ith at rial fibrillat ion . an d obser vat ion al st udies, an t icoagulat ion th erapy is ben eficial
Before n ovel oral an t icoagu lan t agen t s w ere d evelop ed , an t i- in pat ien t s w ith left ven t ricular th rom bus for th e preven t ion of
p latelet t h erapy w as reser ved for p at ien t s w it h con t rain dica- ischem ic stroke.47–49 The durat ion of therapy is unclear but should
t ion s to w ar far in . Asp ir in (325 m g) h as a sm all bu t m easu rable span at least 3 m on th s after a m yocardial in farct ion becau se th is
effect on reducing recurren t st roke rate, based on th e St roke Pre- is th e period w h en th rom bi are m ost likely to form an d em boli-
ven t ion in At rial Fibrillat ion (SPAF) t rial.35 Th e At rial fibrillat ion zat ion to occu r.6,50 Warfarin ad m in istered w ith an INR goal of 2.5
Clopidogrel Trial w ith Irbesartan for prevention of Vascular Events (range 2 to 3) is recom m en ded. Oth er an t icoagulan t s h ave n ot
(ACTIVE) W an d A st udies exam in ed th e com bin at ion of clopido- been st udied in th is con dit ion (Table 17.3).
grel plu s aspirin versu s w arfarin an d versus asp irin , respect ively,
in pat ien t s w ith at rial fibrillat ion . Warfarin w as su perior to th e
com bin at ion of clop id ogrel p lu s asp ir in in ter m s of red u cin g re-
Treatment of Stroke Due to Cardiomyopathy
cu r ren t card ioem bolic st roke. Th e st u d ies also d em on st rated Obser vational studies suggest that the stroke rate in patients w ith
th at clop idogrel p lu s aspirin w as associated w ith a sim ilar m ajor cardiom yopathy is 1.5 to 4%. The Warfarin Versus Aspirin in Re-
h em orrh age rate to w arfarin .44,45 Th e risks of clop idogrel p lu s as- duced Cardiac Eject ion Fract ion (WARCEF) t rial of ant icoagu lat ion

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226 III Ischemic Stroke and Vascular Insufficiency

in pat ient s w ith eject ion fract ion less th an 35% failed to sh ow a sequ en t even t s.53 An t icoagu lat ion in t h e p resen ce of in fect ive
ben efit of an t icoagulat ion th erapy in reducing th e rate of m or tal- en d ocard it is lead s to a h igh r isk of in t racran ial h em or rh age in
it y or st roke.51 How ever, in th is st u dy on ly a m in orit y of pat ien t s th e absen ce of st ud ies dem on st rat ing a ben efit from an t icoagu -
h ad a st roke before en rollm en t . Th e st u dy design is m ore sim ilar lat ion th erapy. Th e likely path op hysiological explan at ion is th at
to th at in prim ar y preven t ion rath er th an in secon dar y preven - an t icoagulat ion does n ot in fluen ce sept ic em boli. Fur th erm ore, a
t ion of st roke. It determ in ed w h ich th erapy w ou ld red u ce th e ran dom ized t rial of aspirin sh ow ed n o eviden ce reducing cardio-
st roke an d m or t alit y rates of p at ien t s w ith a low eject ion frac- gen ic em bolism in th is con dit ion .54 Th erefore, an t ibiot ics rem ain
t ion . Most of th e even t s w ere n on –st roke-related death s.51 th e m ain st ay th erapy for st roke associated w ith in fect ive en do-
Th ere is a gap in th e eviden ce an d th e presen ce of clin ical equ i- card it is. An t icoagu lat ion t h erapy sh ou ld be avoid ed d u e to it s
poise in pat ien ts w ith a low eject ion fract ion w h o h ave experi- r isks. Th is rem ain s t r u e for early an t icoagu lat ion in p rost h et ic
en ced isch em ic st roke. Accept able regim en s in clu de an t icoagu - valve en d ocardit is. On ce t h e n eu rologic con d it ion st abilizes,
lat ion w ith w arfarin w ith a target INR of 2.5 (range 2 to 3) or an t icoagulat ion m ay resum e based on th e usual care of pat ien t s
in it iat ing an t iplatelet th erapy w ith a single an t ip latelet: asp irin , w ith m ech an ical prosth et ic valves (Table 17.3).
clop idogrel, or asp irin -dipyridam ole (Table 17.3).

Treatment of Stroke w ith Suspected


Treatment of Stroke Due to Native Paradoxical Embolism
Valvular Disease
In young pat ien ts w ith cr yptogen ic st roke w ith paten t foram en
Obser vat ion al st udies from th e 1940s onw ard suggest a ben efit ovale, eith er an t iplatelet th erapy or an t icoagulat ion is reason -
from an t icoagu lat ion t h erapy in p at ien t s w it h rh eu m at ic d is- able becau se th e paten t foram en ovale is often in ciden tal an d th e
ease in t h e for m of red u ced recu r ren t card ioem bolic st roke recu rren ce rate is low. In p at ien t s w ith paten t foram en ovale an d
an d, in m ost cases, t h e sp on t an eou s resolu t ion of in t raar ter ial deep ven ou s th rom bosis or th rom boph ilia, th e t reat m en t is an t i-
th rom bi.7,8,52 Th ese st u dies h ave led to th e recom m en dat ion of coagulat ion . Curren tly, th ere is n o eviden ce to sup por t paten t
anticoagulation w ith w arfarin for secondar y prevention of stroke foram en ovale closure. Th e Closure or Medical Th erapy for Cr yp -
in p at ien t s w it h a card iogen ic em bolism related to rh eu m at ic togen ic St roke w it h Paten t Foram en Ovale (CLOSURE 1) t r ial
m it ral valve sten osis. Th e target INR is 2 to 3. in clu ded pat ien ts w ith cr yptogen ic st roke or TIA w h o w ere ran -
Th ere are no ran dom ized cont rolled trials of pat ients w ith non - dom ized to p aten t foram en ovale closu re w ith th e STARFlex
rheum atic valve disease, m itral annular calcification, m itral valve device (NMT Med ical In c, Boston , MA) or m edical th erapy w ith
prolapse, or aor t ic sclerosis. For th ese pat ien ts th e recom m en da- aspirin or w arfarin .55 Th is t rial sh ow ed n o ben efit from paten t
t ion s of an t iplatelet th erapy w ith asp irin , aspirin -dipyridam ole, foram en ovale closure. St roke rates w ere 2.9%an d 3.1%at 2 years,
or clopidogrel are appropriate for th e secon dar y preven t ion of respect ively. Th ere w as n o differen ce w h en th e coexisten ce of an
st roke. No an t iplatelet th erapy is in dicated for p rim ar y p reven - at rial septal an eu r ysm w as con sidered (35% of each grou p ), n or
t ion of st roke in th is pat ien t grou p ap ar t from th e u su al st rat ifi- w as th ere a relat ion sh ip w ith th e degree of sh un t ing.55
cat ion of vascular risk factors (Table 17.3). Un t il furth er st udies sh ow ben efit of paten t foram en ovale
closu re, th is p ract ice sh ou ld be rest ricted to clin ical t rials. Th e
Random ized Evalu at ion of recu rren t St roke com paring PFO [Pat-
Treatment of Stroke Due to Prosthetic en t Foram en Ovale] closu re to Est ablish ed Cu rren t st an dard of
Heart Valves care Treat m en t (RESPECT) t r ial is on e of t h ese st u d ies. It is eval-
An t icoagulat ion th erapies are recom m en ded to preven t valve u at ing th e efficacy an d safet y of paten t foram en ovale closu re
th rom bosis as w ell as for th e p rim ar y an d secon dar y preven t ion w ith th e Am plat zer PFO occluder (AGA Medical Corp, Plym outh ,
of st roke. After st roke, pat ien ts w ith m ech an ical prosth et ic h eart MN) com pared w ith m edical th erapy w ith an t iplatelet s or an t i-
valves sh ould con t in ue or resum e an t icoagulat ion th erapy w ith coagu lan t s in pat ien t s w ith cr yptogen ic st roke associated w ith
w arfarin for a target INR of 2.5 to 3.5. If th e p at ien t w as already paten t foram en ovale. In con t rast to th e CLOSURE t rial, RESPECT
adequately an t icoagulated, th e addit ion of aspirin m ay be con - exclu d ed p at ien t s w it h TIA. Th e p rotocol in RESPECT also m ore
sidered . Th e sam e is n ot t ru e for p at ien t s w ith at rial fibrillat ion t h orough ly exclu d ed p at ien t s w it h ad d it ion al st roke et iologies,
w ith out m ech an ical h ear t valves. In pat ien ts w ith eith er in fec- esp ecially in t racran ial at h erosclerosis an d lacu n ar in farct s in
t ive en docardit is or a large area of in farct ion , in terru pt ing an t i- part icu lar. Th e ou tcom e ch osen in RESPECT w as st roke or death ,
coagu lat ion th erapy is advised in t h e in it ial p h ase u n t il th e risk w ith ou t in clu d ing TIAs as an ou tcom e m easu re. RESPECT w ill
of in t racerebral h em orrh age subsides. Th e durat ion is in dividu- in clude ~ 900 pat ien ts, an d th us its size w ill be sim ilar to th at of
alized for each pat ien t . In pat ien ts w ith bioprosth et ic valves w h o th e CLOSURE t rial.56
h ave a st roke w h ile on an t iplatelets, w e con sider an t icoagulat ion
w ith w arfarin w ith an INR of 2.0 to 3.0 if th eir bleeding risk is
low (Table 17.3).
■ Patient Outcomes
Treatment of Stroke Due to Cardioem bolic st roke, in p ar t icu lar w h en related to at rial fibril-
lat ion , is associated w ith an in creased 30-day case fatalit y rate
Infective Endocarditis (17 to 32%) an d m or talit y (30 to 60%) w ith in th e first year in th e
An t ibiot ic th erapy is effect ive in redu cing th e risk of fur th er em - p re–t issu e p lasm in ogen act ivator an d h em icran iectom y era.26
boli from in fect ive en d ocard it is w it h a rap id red u ct ion in su b - Th e excessive m or t alit y rem ain s even after con t rolling for age in

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17 Medical Management of Cardiogenic Cerebral Embolism 227

obser vat ion al st udies. Th e risk of m or t alit y an d disabilit y associ- in farcts w ith ou t edem a or h em orrh agic t ran sform at ion , w e st art
ated w ith cardiogen ic em bolism is h igh er th an w ith oth er st roke an t icoagulat ion soon er after st roke. It is im por tan t to con sider
su bt yp es. Sligh tly m ore th an 20% of pat ien ts are u n able to w alk st ar t ing an t icoagu lat ion th erapy before h ospit al d isch arge to en -
or at ten d to th eir bodily n eeds (m odified Ran kin scale 4-5) at sure com plian ce.
h ospital disch arge. Mort alit y from cardioem bolic st roke is also
sligh tly greater th an 20% at h osp ital disch arge.57 Most of th e
death s are related to st roke rath er th an to cardiac cau ses. For Choice of Anticoagulation Agent in
su r vivors, th e h igh rate of recu rren t isch em ic st roke of 15%h igh - Atrial Fibrillation
ligh t s th e n eed for adequ ate secon dar y preven t ion in ever y pa- Th e ch oice of w arfarin , dabigat ran , rivaroxaban , or apixaban for
t ien t . In p at ien t s w ith isch em ic st roke, t h e r isk of m yocard ial an t icoagulat ion is in dividu alized. It depen ds on pat ien t com or-
in farct ion is 1 to 2% in th e early ph ase an d persists for as long as bidit ies, pat ien t preferen ces, pat ien t com plian ce w ith th erapy,
1 year after st roke.58 Th e long-term risk of m yocardial in farct ion , an d available resources. Th e n ovel agen ts w ere com pared w ith
h ow ever, is h igh —10 to 20% over 5 to 10 years. Cardiac causes w arfarin . Th e t im e w ith a th erapeu t ic INR for w arfarin w as dif-
accou n t for a larger p rop or t ion of long-term m or t alit y.58 Th is feren t in each t rial, an d each t rial h ad sligh tly differen t de-
fin ding fur th er em ph asizes th e n eed to address risk factors in sign .34,43 Th ese differen ces lim it th e abilit y to d eterm in e w h ich
th ese pat ien t s. of t h e d r ugs is t h e m ost efficaciou s. War far in th erapy is reason -
able for p at ien t s w h o can reliably ach ieve an d m ain t ain INR
w it h in th e d esired range. In p at ien t s w h o p refer to avoid fre-
qu en t INR test ing or in t h ose w ith difficu lt y m ain t ain ing INR
■ Alternative Therapy Solution in w ith in the desired range, on e of th e n ovel agen ts sh ou ld be used
Atrial Fibrillation in stead. From an efficacy st an dpoin t , dabigat ran an d apixaban
are good ch oices given th eir superiorit y over w arfarin , w ith an
Several p oin ts an d clin ical scen arios are w or th fu r th er con sider-
INR w ithin th e th erapeut ic range—64% an d 62% of th e t im e, re-
at ion w h en select ing altern at ive th erap ies to t reat pat ien ts w ith
sp ect ively.34,43 Apixaban is also safer th an w arfarin in term s of
at rial fibrillat ion .
m ajor h em orrhage.43 Th e advan t age of rivaroxaban is on ce-daily
dosing.41
Timing of Anticoagulation After Cardioembolic
Stroke in Atrial Fibrillation Patients w ith Atrial Fibrillation Who Have
Th is clin ical sit u at ion is ver y com m on . An t icoagu lat ion w ith ei- Contraindications to Warfarin
th er w arfarin or n ovel an t icoagu lan ts is of dem on st rated ben efit
In p at ien ts w ith absolu te con t rain dicat ion s to w arfarin th erapy,
for th e secon dar y preven t ion of st roke in pat ien t s w ith at rial fi-
th e p reviou s ch oice w as aspirin or n o t reat m en t . How ever, n ow
brillat ion .38 Most of th e st udies en rolled pat ien ts at least 14 days
th ere are oth er opt ion s. Apixaban is safer th an w arfarin , h as sim -
after st roke. It is u n clear w h at t im e poin t bet w een th e st roke an d
ilar risks as aspirin , an d is m ore effect ive t h an w arfarin at least
14 days after th e st roke is th e opt im al t im e to com m en ce an t ico-
according to on e st udy. An oth er altern at ive is dabigat ran at 110
agu lat ion . Th e con cern w ith an t icoagu lat ion is balan cing th e risk
m g t w ice daily. Con siderat ion of p ercutan eou s closu re of th e left
of h em orrhagic conversion of st roke w ith early an t icoagulat ion
at rial ap p en dage in com bin at ion w ith an t iplatelet th erapy is
again st th e risk of recu rren t st roke w ith delayed an t icoagu lat ion .
m erited in selected cases. How ever, it is n ot free from th e risk of
Th e Heparin in Acu te Em bolic St roke Trial (HAEST) evalu ated pa-
h em orrh age because an t iplatelet th erapy is st ill n ecessar y w ith
t ien t s w ith acu te isch em ic st roke related to at rial fibrillat ion .
th e Watch m an device. Th is ap proach is esp ecially con ten t iou s
Pat ien t s w ere ran d om ized to asp ir in or d altep ar in , a low -
because th e n ovel an t icoagu lan ts h ave excellen t safet y profiles.
m olecular-weight h eparin, w ithin 30 hours of ischem ic st roke.
Th e safet y p rofile of apixaban is sim ilar to th at of aspirin accord-
Based on HAEST, th e risk of recu rren t st roke du ring th e first 14
ing to at least on e st udy. Fin ally, at th is stage, ablat ive th erapy is
days after st roke is 7.5% in p at ien t s receiving asp irin . Treat m en t
a prom ising u nproven poten t ial th erapy for th e preven t ion of
w ith dalteparin , w h ich w as associated w ith a rate of 8.5% recur-
cardioem bolism in p at ien t s w ith at rial fibrillat ion , bu t it can n ot
ren t st rokes, did n ot red u ce th is risk.59
yet be recom m en ded as a rou t in e altern at ive to an t icoagu lat ion
Furth er obser vat ion al st udies an d m eta-an alysis revealed th at
th erapy.
an ticoagulat ion w ith th erapeut ic doses of h eparin or en oxaparin
is associated w ith risks of h em orrh age th at ou t w eigh th e ben e-
fits of redu ced cardiogen ic em bolism .60,61 How ever, deep ven ou s
th rom bosis p rop hylaxis doses of th ese agen t s are safe.62 In th e
absen ce of clear eviden ce, it is reason able to at tem pt to st rat ify
■ Conclusion
p at ien t r isk of h em or rh age to d ecid e w h en to st ar t an t icoagu - Cardiogen ic em bolism rem ain s a m ajor cau se of isch em ic st roke
lat ion t h erapy. In clin ical p ract ice, large in farct size, p resen ce in t h e Un ited St ates an d w orldw id e. Med ical t reat m en t of ar-
of ongoing rath er th an resolving cerebral edem a, an d presen ce of rhyt h m ia h as led to im p rovem en t s in ou tcom es of p at ien t s.
h em orrh agic t ran sform at ion are often used as m arkers of a h igh Treat m en t an d w orku p of st roke sh ou ld alw ays in clu de a th or-
risk of bleeding. In su ch p at ien t s w e delay an t icoagu lat ion u n t il ough cardiac h istor y an d exam in at ion to address th e h ear t as a
later in th e 0- to 14-day postst roke p eriod. In p at ien t s w ith sm all source for st roke.

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228 III Ischemic Stroke and Vascular Insufficiency

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13. Stein er MM, Di Tu llio MR, Ru n dek T, et al. Paten t foram en ovale size an d effect ive in tensit y of prophylact ic an t icoagulat ion for pat ien t s w ith n on -
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St roke 1998;29:944–948 34. Con n olly SJ, Ezekow it z MD, Yu suf S, et al; RE-LY Steering Com m it tee an d
14. Hagen PT, Sch olz DG, Edw ards W D. In ciden ce an d size of paten t foram en Invest igators. Dabigat ran versu s w arfarin in p at ien t s w ith at rial fibrilla-
ovale during th e first 10 decades of life: an autopsy st u dy of 965 n orm al t ion . N Engl J Med 2009;361:1139–1151
heart s. Mayo Clin Proc 1984;59:17–20 35. St roke Preven t ion in At rial Fibrillat ion St udy. Fin al result s. Circulat ion
15. Di Tu llio MR, Sacco RL, Sciacca RR, Jin Z, Hom m a S. Paten t foram en ovale 1991;84:527–539
an d th e risk of isch em ic st roke in a m u lt ieth n ic p op u lat ion . J Am Coll Car- 36. EAFT (European At rial Fibrillat ion Trial) St udy Group. Secon dar y preven -
diol 2007;49:797–802 t ion in n on -rh eum at ic at rial fibrillat ion after t ran sien t isch aem ic at t ack
16. Mas JL, Arquizan C, Lam y C, et al; Paten t Foram en Ovale an d At rial Sept al or m in or st roke. Lan cet 1993;342:1255–1262
Aneur ysm St udy Group. Recurrent cerebrovascular events associated w ith 37. Har t RG, Pearce LA, Aguilar MI. Met a-an alysis: an t ith rom bot ic th erapy to
paten t foram en ovale, at rial sept al an eu r ysm , or both . N Engl J Med 2001; preven t st roke in pat ien t s w h o h ave n onvalvular at rial fibrillat ion . Ann
345:1740–1746 In tern Med 2007;146:857–867
17. Meissn er I, Kh an dh eria BK, Heit JA, et al. Paten t foram en ovale: inn ocen t 38. Man t J, Hobbs FD, Fletch er K, et al; BAFTA invest igators; Midlan d Research
or guilt y? Eviden ce from a prospect ive populat ion -based st udy. J Am Coll Pract ices Net w ork (MidReC). Warfarin versus aspirin for st roke preven -
Cardiol 2006;47:440–445 t ion in an elderly com m u n it y populat ion w ith at rial fibrillat ion (th e Bir-
18. Mon o ML, Geister L, Galim an is A, et al. Paten t foram en ovale m ay be m ingh am At rial Fibrillat ion Treat m en t of the Aged St udy, BAFTA): a ran -
causal for th e first st roke but un related to su bsequen t isch em ic even t s. dom ised con t rolled t rial. Lan cet 2007;370:493–503
St roke 2011;42:2891–2895 39. Gage BF, van Walraven C, Pearce L, et al. Select ing pat ient s w ith at rial fi-
19. Pezzin i A, Del Zot to E, Magon i M, et al. In h erited th rom boph ilic disorders brillat ion for an t icoagulat ion : st roke risk st rat ificat ion in pat ien t s t aking
in young adult s w ith isch em ic st roke an d paten t foram en ovale. St roke aspirin . Circulat ion 2004;110:2287–2292
2003;34:28–33 40. Den t ali F, Douket is JD, Lim W, Crow th er M. Com bin ed aspirin -oral an t ico-
20. Overell JR, Bon e I, Lees KR. Interat rial sept al abn orm alit ies an d st roke: a agulan t therapy com pared w ith oral ant icoagulant th erapy alone am ong
m et a-analysis of case-con t rol st udies. Neurology 2000;55:1172–1179 pat ien t s at risk for cardiovascular disease: a m et a-an alysis of ran dom ized
21. Hom m a S, Sacco RL, Di Tullio MR, Sciacca RR, Mohr JP; PFO in Cr yptogenic t rials. Arch In tern Med 2007;167:117–124
St roke St udy (PICSS) Invest igators. Effect of m edical t reat m en t in st roke 41. Patel MR, Mah affey KW, Garg J, et al; ROCKET AF Invest igators. Rivaroxa-
pat ien t s w ith paten t foram en ovale: paten t foram en ovale in Cr yptogen ic ban versus w arfarin in n onvalvular at rial fibrillat ion . N Engl J Med 2011;
St roke St u dy. Circulat ion 2002;105:2625–2631 365:883–891

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17 Medical Management of Cardiogenic Cerebral Embolism 229

42. Con n olly SJ, Eikelboom J, Joyn er C, et al; AVERROES Steering Com m it tee of left at rial th rom bi am ong can didates for percu t an eous t ran sven ous m i-
an d Invest igators. Ap ixaban in p at ien t s w ith at rial fibrillat ion . N Engl J t ral com m issurotom y. J Am Coll Cardiol 2002;39:886–891
Med 2011;364:806–817 53. Pasch alis C, Pugsley W, Joh n R, Harrison MJ. Rate of cerebral em bolic
43. Granger CB, Alexan der JH, McMurray JJ, et al; ARISTOTLE Com m it tees an d even t s in relat ion to an t ibiot ic an d an t icoagulan t th erapy in pat ient s w ith
Invest igators. Apixaban versus w arfarin in pat ien t s w ith at rial fibrillat ion . bacterial en docardit is. Eur Neurol 1990;30:87–89
N Engl J Med 2011;365:981–992 54. Ch an KL, Dum esn il JG, Cujec B, et al; Invest igators of th e Mult icen ter As-
44. Con n olly S, Pogue J, Har t R, et al; ACTIVE Writ ing Group of th e ACTIVE pirin St u dy in In fect ive En d ocardit is. A ran d om ized t rial of asp irin on th e
Invest igators. Clopidogrel plus aspirin versus oral an t icoagulat ion for risk of em bolic even t s in pat ien t s w ith in fect ive endocardit is. J Am Coll
at rial fibrillat ion in th e At rial fibrillat ion Clop idogrel Trial w ith Irbesar t an Cardiol 2003;42:775–780
for preven t ion of Vascu lar Even t s (ACTIVE W): a ran dom ised con t rolled 55. Furlan AJ, Reism an M, Massaro J, et al; CLOSURE I Invest igators. Closure or
t rial. Lan cet 2006;367:1903–1912 m edical th erapy for cr yptogen ic st roke w ith paten t foram en ovale. N Engl
45. Con n olly SJ, Pogu e J, Har t RG, et al; ACTIVE Invest igators. Effect of clopido- J Med 2012;366:991–999
grel ad ded to asp irin in p at ien t s w ith at rial fibrillat ion . N Engl J Med 56. Ran dom ized Evaluat ion of Recurren t St roke Com paring PFO Closure to
2009;360:2066–2078 Est ablish Curren t St an dard of Care Treat m en t . Plym outh, MN: AGA Medi-
46. Wyse DG, Waldo AL, DiMarco JP, et al; At rial Fibrillat ion Follow -up Inves- cal Corp.; 2012
t igat ion of Rhyth m Man agem en t (AFFIRM) Invest igators. A com parison of 57. Grau AJ, Weim ar C, Buggle F, et al. Risk factors, outcom e, an d t reat m en t in
rate con t rol an d rhythm cont rol in pat ien t s w ith at rial fibrillat ion . N Engl subt ypes of isch em ic st roke: th e Germ an st roke dat a ban k. St roke 2001;
J Med 2002;347:1825–1833 32(11):2559–2566
47. Nordreh aug JE, Joh an n essen KA, von der Lippe G. Usefuln ess of high -dose 58. Vickrey BG, Rector TS, Wickst rom SL, et al. Occurren ce of secon dar y isch -
an t icoagu lan t s in preven t ing left ven t ricu lar th rom bu s in acu te m yocar- em ic even t s am ong person s w ith ath erosclerot ic vascular disease. St roke
dial in farct ion . Am J Cardiol 1985;55(13 Pt 1):1491–1493 2002;33:901–906
48. Davis MJ, Irelan d MA. Effect of early an t icoagulat ion on th e frequen cy of 59. Berge E, Abdelnoor M, Nakst ad PH, San dset PM. Low m olecular-w eigh t
left ven t ricular th rom bi after an terior w all acute m yocardial infarct ion. h eparin versus aspirin in pat ien t s w ith acute isch aem ic st roke an d at rial
Am J Cardiol 1986;57:1244–1247 fibrillat ion : a double-blin d ran dom ised st udy. HAEST St udy Group. Hepa-
49. Gueret P, Dubourg O, Ferrier A, Farcot JC, Rigaud M, Bourdarias JP. Effect s rin in Acute Em bolic St roke Trial. Lan cet 2000;355:1205–1210
of full-dose h eparin an t icoagulat ion on th e developm en t of left ven t ricu- 60. Paciaron i M, Agn elli G, Mich eli S, Caso V. Efficacy and safet y of an t icoagu-
lar throm bosis in acu te t ran sm ural m yocardial in farct ion . J Am Coll Car- lan t t reat m en t in acute cardioem bolic st roke: a m et a-an alysis of random -
diol 1986;8:419–426 ized con t rolled t rials. St roke 2007;38:423–430
50. Lapeyre AC III, Steele PM, Kazm ier FJ, Ch esebro JH, Vliet st ra RE, Fuster V. 61. Hallevi H, Albrigh t KC, Mar t in -Sch ild S, et al. An t icoagu lat ion after cardio-
System ic em bolism in ch ronic left vent ricular an eur ysm : in ciden ce and em bolic st roke: to bridge or n ot to bridge? Arch Neurol 2008;65:1169–
th e role of an t icoagu lat ion . J Am Coll Cardiol 1985;6:534–538 1173
51. Hom m a S, Th om pson JL, Pu llicin o PM, et al; WARCEF Invest igators. War- 62. Sh erm an DG, Albers GW, Bladin C, et al; PREVAIL Invest igators. Th e effi-
farin and aspirin in pat ien t s w ith h eart failu re and sin u s rhyth m . N Engl J cacy and safet y of enoxaparin versus unfractionated heparin for the preven-
Med 2012;366:1859–1869 t ion of ven ou s throm boem bolism after acute isch aem ic st roke (PREVAIL
52. Silaruks S, Thinkham rop B, Tantikosum W, Wongvipaporn C, Tatsanavivat P, St udy): an open -label ran dom ised com parison . Lan cet 2007;369:1347–
Klungboon krong V. A progn ost ic m odel for predict ing th e disappearan ce 1355

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18 Diagnosis of Brain Infarction
Moham ed Teleb, Paul Singh, and Maarten Lansberg

Tradit ion ally, brain in farct ion h as been a clin ical diagn osis. An Diagnostic History
early n eurologist an d leader in th e field of st roke, C. Miller Fish er
Obtain ing a relevan t , qu ick, an d accurate h istor y for acute brain
of Massach uset ts Gen eral Hospital, st ated, “Neurology is learn ed
in farct ion facilit ates good clin ical care of pat ien t s (Table 18.1). It
on e st roke at a t im e.” Fish er described m any of th e st roke syn -
is im port an t to est ablish th e t im e of sym ptom on set an d to de-
d rom es w e t ake for gran ted today in ad d it ion to d iscover ing
term in e if th e pat ien t is a can didate for acute t reat m en ts such as
m any cau ses of st roke in clu d in g carot id ar ter y sten osis, card io -
in t raven ous t issu e-t yp e plasm in ogen act ivator (t-PA) or en d o-
em bolic st rokes from at r ial fibr illat ion , an d lacu n ar in farct s.
vascu lar t reat m en t , w h ich m ust be adm in istered w ith in h ours of
Even t h e grad in g scale for an eu r ysm al su barach n oid h em or-
sym ptom on set . It is also im por t an t to determ in e if th e progres-
rh age carries Fish er’s n am e.1 Today, brain in farct ion is a clin ical
sion of sym ptom s w as su dd en or gradu al. Most vascu lar even ts
diagn osis th at is h igh ly relian t on im aging. Th e evolu t ion of th e
occur su dden ly, alth ough th ere are except ion s, in cluding st ut ter-
m odern defin it ion of brain infarct ion began w ith th e use of com -
ing TIAs or flow sym ptom s related to in t racran ial or ext racran ial
pu ted tom ograp hy (CT) of th e h ead, bu t it did n ot becom e an
sten osis.
accepted defin it ion un t il th e adven t of diffusion -w eigh ted m ag-
Associated sym ptom s are also im por tan t to establish because
n et ic reson an ce im aging (MRI), w h ich w as developed at Stan ford
th ey can dist ingu ish brain in farct ion from st roke m im ics an d
Un iversit y Medical Cen ter an d h as revolut ion ized th e field of
m ay reveal th e cau se of th e brain in farct ion . A person w ith se-
acute st roke.2 Today m any physician s propose th at even t ran -
vere ch est pain as w ell as pain radiat ing to th e n eck m igh t h ave
sien t isch em ic at tacks (TIAs) sh ou ld be defin ed by th e lack of
a m yocardial in farct ion causing cardiac em boli, w h ereas sudden ,
rest ricted diffu sion on im aging. Th is argum en t h as been d ebated
severe ch est an d back pain cou ld represen t an aor t ic dissect ion
in m u lt iple pu blicat ion s, in clu d ing th e New England Journal of
w ith exten sion in to th e carot id or ver tebral ar teries. Th e h istor y
Medicine.3
h elps determ in e n ot on ly th e possible cause but also th e m an -
Because th e diagn osis of st roke requ ires both an accu rate clin -
agem en t an d t reat m en t of th e sym ptom s.
ical exam in at ion an d advan ced im aging, th is ch apter is divided
If th e pat ien t presen ts to th e ED, th e h istor y can be obtain ed
in to t w o sect ion s. Th e first sect ion focu ses on th e clin ical diag-
from anyon e available, in clu ding th e pat ien t , fam ily m em bers,
n osis of brain in farct ion , w h ich in clu d es t h e in it ial evalu at ion
n u rses, oth er doctors involved in th e pat ien t’s care, or th e em er-
an d d iagn ost ic ap p roach , st roke m im ics, an d com m on st roke
gen cy m edical ser vices person n el w h o brough t th e pat ien t to th e
syn d rom es based on bot h t yp e of st roke (lacu n ar, large vessel,
h ospital. In addit ion to th e acute sym ptom s, it is also im por t an t
em bolic) an d vascu lar territor y. Th e secon d sect ion su r veys th e
to determ in e quickly th e accom panying sym ptom s, th e t im e of
differen t im aging m odalit ies th at can h elp diagn ose brain in farc-
on set , an d oth er relevan t factors su ch as a m edical an d surgical
t ion or isch em ia. Eviden ce-based st roke t reat m en t is addressed
h istor y (Table 18.2). Th e h istor y sh ould focus on exclu sion an d
in oth er ch apters of th is book.
inclusion criteria for the adm inistration of intravenous t-PA, w hich
is th e st an dard of care for pat ien t s w h o reach m edical at ten t ion
w ith in 4.5 h ours of th e on set of sym ptom s.4 Fin ally, h istor y th at
■ Clinical Diagnosis of Acute per tain s to st roke m im ics sh ou ld also be obtain ed qu ickly (Table
Brain Infarction 18.3). It can be difficult to diagn ose st roke m im ics during th e
acu te p h ase. Bet w een 3% an d 16% of p at ien t s t reated w it h t -PA
Evaluation h ave a st roke m im ic.5,6 For t u n ately, m u lt ip le st u d ies, in clu d in g
a m et a-an alysis, h ave sh ow n t h at m ost st roke m im ics h ave bet -
Th e in it ial evalu at ion of brain in farct ion varies w ith th e clin ical
ter ou tcom es w ith out an in crease in sym ptom at ic in t racran ial
en cou n ter. A p at ien t p resen t in g to t h e em ergen cy d ep ar t m en t
bleeds.6 Th e except ion is a p at ien t w ith an in t racran ial t u m or,
(ED) w it h n ew focal sym ptom s is evalu ated d ifferen t ly t h an a
but t um ors are usually visualized on CT scan before in t raven ous
postop erat ive p at ien t , alth ough th e in it ial evalu at ion is sim ilar.
t-PA is adm in istered.
An exam ple of th is variabilit y is seen in a pat ien t after carot id
en dar terectom y su rger y. Un like in th e ED, th e h istor y is usu ally
kn ow n , an d qu ickly reading a surger y repor t m igh t be m ore use-
Diagnostic Examination
fu l th an t r ying to con tact fam ily m em bers w h o m igh t h ave last
seen th e pat ien t in a n orm al n eu rologic state. Acu te im aging of As w ith any m edical exam ination, the evaluation of a patient w ith
th e carot id arter y is in dicated. In th e ED, acu te vascu lar im aging an acute isch em ic st roke begin s w ith th e vital sign s, w h ich m ay
is n ot con sidered th e stan dard of care at m ost in st it ut ion s, an d provide clu es to both th e n at u re of th e brain in farct ion (w h eth er
on ly a CT of h ead is t yp ically in dicated for acu te m an agem en t .4 hem orrhagic or ischem ic) and the cause (Table 18.4). For exam ple,

230

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18 Diagnosis of Brain Infarction 231

Table 18.1 Diagnostic Approach by Time Line Table 18.2 Pertinent History

Time Action History of present Tim e of onset, accompanying symptom s


illness (headache, seizures), evolution of symptoms
0–10 minutes Check vital signs
(sudden, gradual), chest pain
Get history: symptoms, tim e of onset, recent
Medical history Prior intracerebral hemorrhage, head trauma,
surgeries
myocardial infarction, atrial fibrillation
Draw laboratories: glucose, INR/PTT, BMP, CBC
Surgical history Any recent or major surgeries, arterial punctures
10–20 minutes Review vital signs again
in noncompressible sites
Conduct neurologic exam with NIHSS exam and
Allergies Especially to contrast
other pertinent exam s
Medications Especially anticoagulants
20–40 minutes Acute im aging—noncontrast CT, CT
angiography, CT perfusion, or MR imaging
40–50 minutes Decide treatment plan
Abbreviations: INR, international norm alized ratio; PTT, partial throm boplastin
tim e; BMP, basic m etabolic panel; CBC, complete blood count; NIHSS, National
Institutes of Health Stroke Scale; CT, computed tom ography; MR, magnetic
resonance.

Table 18.3 Stroke Mimics and Their Features

Stroke Mimic Comment/ Feature

Seizure Usually postictal Todd’s paralysis or generalized tonic-clonic thought to be basilar stroke
Migraine headache Headaches can come after onset of symptoms
Syncope Usually isolated from hypotension or cardiac arrhythmia; other brainstem findings can help with
possible vertebral basilar insufficiency
Hypoglycemia Can present with focal weakness; history of diabetes mellitus should raise concern; always get glucose
level stat
Metabolic encephalopathy Can present with confusion, slurred speech, or aphasia.
Drug overdose Nonresponsiveness confused for posterior circulation stroke or large catastrophic bleed; exam and
vitals can be helpful
Herpes encephalitis Affects the temporal lobes so confusion, aphasia, and visual field cut are possible but fever or other
signs of central nervous system infection should help
Subdural hematom a Especially in the elderly with minor trauma; im aging rules it out
Peripheral nerve compression Usually not sudden in onset unless patient slept on arm and awoke with it; weakness or numbness are
in a particular peripheral nerve distribution
Bell’s palsy Always check eye closure and forehead (lower CN VII features), although can appear slowly in some
Bell’s palsy patients; lower CN VII features can occur with pontine strokes but other CNs usually
involved, especially CN VI
Benign paroxysm al positional vertigo Vertigo, nausea, vom iting, and a sense of im balance, usually with turning of the head in one direction;
look for other CN findings for stroke
Conversion disorder Ask about psychiatric history especially in young if drug abuse is negative; assum e symptoms are real
and treat according to symptoms
Reactivation of old stroke Can occur with fatigue or any metabolic derangement
Abbreviation: CN, cranial nerve.

Table 18.4 Clinical Features of Ischemic and Hemorrhagic Strokes

Feature Ischemic Strokes Hemorrhagic Strokes

Onset Sudden or stut tering Sudden


Resolution Can resolve (i.e., TIA) Never resolves
Blood pressure Varies but usually elevated; symptoms with low blood Elevated for hypertensive IPH and aSAH; varies in CAA,
pressure indicate possible flow-lim iting stenosis AVM, CAVMAL, venous thrombosis, and tum ors
Level of consciousness Usually awake except in posterior circulation basilar Can be obtunded due to m ass effect of bleed,
strokes hydrocephalus, or brainstem involvement
Headache Usually none Common
Abbreviations: TIA, transient ischemic at tack; IPH, intraparenchym al hemorrhage; aSAH, aneurysm al subarachnoid hem orrhage; CAA, cerebral amyloid angiopathy;
AVM, arteriovenous m alformation; CAVMAL, cavernous m alform ation.

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232 III Ischemic Stroke and Vascular Insufficiency

a person w h o is t achycardic w ith an irregular h ear tbeat likely n ally design ed by Brot t et al7 in 1989 to m easu re clin ical differ-
h as a cardioem bolic isch em ic st roke. A pat ien t w h o h as severely en ces in st roke, an d it h as gain ed w ide accept an ce as th e st an -
elevated blood p ressu re an d is obt u n d ed is m ore likely to h ave a dard of care for th e in it ial exam in at ion of an acu te st roke p at ien t .8
h em orrhagic st roke. Th e exam in at ion can be perform ed qu ickly, an d th e scale h elps
On ce t h e vit al sign s are obt ain ed an d t h e p at ien t ’s air w ay, n ot on ly in predict ing sh or t-term an d long-term outcom es, but
breat h ing, an d circu lat ion are st abilized , a qu ick n eu rologic ex- also in iden t ifying a large vessel occlu sion .9,10 Overall, it is reli-
am in at ion using th e Nat ion al In st it utes of Health St roke Scale able an d rep rod u cible, bu t u sing it requ ires t rain ing an d cer t i-
(NIHSS) sh ould be perform ed (Table 18.5). Th is scale w as origi- ficat ion , w h ich can be obt ain ed t h rough t h e Am er ican St roke
Associat ion’s w ebsite (w w w.st rokeassociat ion .org).11,12

Table 18.5 National Institutes of Health Strokes Scale


Signs and Symptoms of Brain Infarction
1a. Level of consciousness 0 = Alert
Th e clin ical diagn osis of brain in farct ion h eavily depen ds on th e
1 = Not alert, arousable
clin ician’s abilit y to recogn ize cer t ain st roke syn drom es. In th e
2 = Not alert, obtunded
an terior circulat ion , st roke sym ptom s are grou ped by th eir blood
3 = Unresponsive
supply. In the posterior circulation, they classically bear the nam e
1b. Questions 0 = Answers both correctly
1 = Answers one correctly of th e n eu rologist w h o described th em . How ever, th is t ren d in
2 = Answers neither correctly th e p osterior circu lat ion h as ch anged . With m ore advan ced im -
1c. Comm ands 0 = Performs both tasks correctly aging, even p osterior circu lat ion syn drom es are being d escribed
1 = Performs one task correctly by th eir blood sup ply. Th is ch apter describes th e m ost com m on
2 = Performs neither task syn drom es, an d Table 18.6 list s th e sign s an d sym ptom s based
2. Gaze 0 = Normal on t h e ar ter y.13–15 Th is is n ot an exh au st ive list; it focu ses on
1 = Partial gaze palsy t h e sign s an d sym ptom s t h at are m ost likely to be id en t ified in
2 = Total gaze palsy p at ien t s.
3. Visual fields 0 = No visual loss Th ere are som e pract ical tools to h elp iden t ify th e locat ion of
1 = Partial hem ianopsia a brain in farct ion . Pat ien ts w h o h ave un dergon e clipping of an
2 = Complete hemianopsia an terior cerebral arter y (ACA) an eur ysm h ave been described to
3 = Bilateral hem ianopsia h ave a recurren t ar ter y of Heu bn er in farct . In such cases, post-
4. Facial palsy 0 = Normal operat ive h em iparesis sh ould prom pt im m ediate im aging (i.e.,
1 = Minor paralysis search ing in th e vicin it y of th e ar teries th at w ere operated u p on
2 = Partial paralysis as a source of brain in farct ion ). Pat ien ts w ith h em iparesis can
3 = Complete paralysis h ave eith er a large vessel or lacun ar in farct , an d search ing for
5a. Left motor arm 0 = No drift cor t ical sign s su ch as aph asia, visu al field cuts, or n eglect versu s
1 = Drift before 10 seconds
isolated u n ilateral weakn ess can h elp w ith localizat ion . Hem ipa-
2 = Falls before 10 seconds
resis from an an terior or posterior circulat ion in farct can be dis-
3 = No effort against gravit y
t ingu ish ed by con sidering oth er feat u res of th e p at ien t’s clin ical
4 = No movem ent
exam ination , such as cran ial nerve deficits, ataxia, nausea, or
5b. Right motor arm Scored in same fashion as left leg
crossed sensor y findings.16 This point is im portant because m any
6a. Left motor leg 0 = No drift
in st it ut ion s use on ly th e clin ical exam in at ion an d a n on -con t rast
1 = Drift before 5 seconds
2 = Falls before 5 seconds CT of th e h ead to determ ine w h eth er pat ien ts are can didates for
3 = No effort against gravit y en d ovascu lar t reat m en t .
4 = No movement
6b. Right m otor leg Scored in same fashion as right arm
7. Ataxia 0 = Absent
1 = One limb ■ Neuroimaging in Acute
2 = Two lim bs Brain Infarction
8. Sensory 0 = Norm al
1 = Mild loss Th e role of acu te st roke th erap ies su ch as t-PA an d m ech an ical
2 = Severe loss em bolectom y is to salvage p oten t ially viable brain t issu e th at h as
9. Language 0 = Norm al n ot un dergon e in farct ion . Using im aging to determ in e w h ich pa-
1 = Mild aphasia t ien ts m ay ben efit from th ese th erap ies is essen t ial to th e m an -
2 = Severe aphasia agem en t of acu te isch em ic st roke. W h en in t raven ou s t-PA w as
3 = Mute or global aphasia first approved by th e Food an d Dr ug Adm in ist rat ion in 1996, th e
10. Dysarthria 0 = Norm al on ly im aging required w as a n on con t rast CT of th e h ead th at
1 = Mild dem on st rated n o in t racran ial h em orrh age.17 Alth ough th e in it ial
2 = Severe Nat ion al In st it u te of Neu rological Disorders an d St roke (NINDS)
11. Extinction/inat tention 0 = Norm al t r ial sh ow ed favorable ou tcom es in p at ien t s w h o received in -
1 = Mild t raven ou s t -PA com p ared w ith a p lacebo w it h in 3 h ou rs of t h e
2 = Severe on set of neurologic sym ptom s, it was evident from several other
Available at www.ninds.nih.gov/doctors/NIH_Stroke_Scale.pdf. studies, such as th e European Cooperat ive Acute St roke St udy III

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18 Diagnosis of Brain Infarction 233

Table 18.6 Common Signs and Symptoms of Ischemic Brain Infarction

Vessel/Type of Stroke Signs and Symptoms

MCA Contralateral loss of strength and sensation in the face, arm, and to a lesser extent leg;
aphasia if dominant hemisphere, neglect if nondominant
ACA Contralateral loss of strength and sensation in the leg and to a lesser extent arm
PCA Contralateral visual field deficit; possibly confusion and aphasia if dominant hem isphere;
left-sided gives alexia without agraphia
Basilar Various combinations of lim b ataxia, dysarthria, dysphagia, facial and limb weakness and
sensory loss (m ay be bilateral), pupillary asymm etry, disconjugate gaze, visual field
loss, decreased responsiveness; also visual hallucinations, dream like behavior, agitated
behavior, and amnesia
SCA Dysarthria and limb ataxia
AICA Gait and limb ataxia, dysfunction of ipsilateral CNs V, VII, and VIII; acute hearing loss with
ataxia
PICA Vertigo, nausea, vomiting, gait ataxia
Vertebral Ipsilateral limb ataxia and Horner syndrome, crossed sensory loss, vertigo, dysphagia,
hoarseness (lateral m edullary/Wallenberg syndrome)
Penetrating arteries (lacunar syndromes)
MCA perferators (internal capsule/corona radiata) Contralateral hemiparesis alone (pure motor stroke) or contralateral hemiparesis + ataxia
out of proportion to weakness (ataxic-hem iparesis)
Basilar perferators (ventral pons) No cortical signs
PCA perferators (thalamus) Contralateral sensory loss alone (pure sensory stroke); no cortical signs
Abbreviations: MCA, m iddle cerebral artery; ACA, anterior cerebral artery; PCA, posterior cerebral artery; SCA, superior cerebellar artery; AICA, anterior inferior
cerebellar artery; PICA, posterior inferior cerebellar artery; CN, cranial nerve.
Sources: Content derived from Barret t et al,13 Jones et al,14 and Uchino et al.15

(ECASS III), t h at p at ien t s w ell beyon d t h is t im e w in d ow also in for m at ion abou t m ajor vessel p aten cy, an d grad ien t -recalled
m igh t ben efit from th rom bolyt ic th erapies.18 Over th e p ast 15 ech o (GRE) im agin g d etect s in t racran ial h em or rh age. Th is sec-
years radiograp h ic im aging h as at tem pted to su p p lan t “t im e” as t ion d iscu sses th e com m on sequ en ces obt ain ed in t h e acu te
an exclu sion criterion for cerebral reperfu sion th erapies. evaluat ion .
Brain isch em ia en com passes var ying levels of hypoperfused
brain t issue exten ding from a region of irreversibly injured cells
in th e isch em ic core to a p oten t ially salvageable region of de-
Diffusion-Weighted Imaging
creased cerebral blood flow com posed of isch em ic t issue at risk, Th e diffu sion -w eigh ted im aging sequ en ce assesses th e rest ricted
or th e isch em ic pen u m bra.19 Th e isch em ic pen um bra is hypo- m ovem ent of w ater m olecules in tissue related to cytotoxic edem a
perfu sed relat ive to n orm al brain t issu e bu t h as n ot u n dergon e from cerebral isch em ia.30 Diffu sion -w eigh ted im aging can detect
com p lete in farct ion . Th erefore, it h as th e p oten t ial to be revived isch em ia w ith in 30 m in utes in h u m an st udies,31 an d th e volu m e
via various reperfusion strategies. Without reperfusion, this pen- of diffusion-w eighted im aging restriction correlates w ell w ith the
um bral tissue becom es part of the ischem ic core and the patient’s irreversible isch em ic core.32 For th is reason , it is m ore sen sit ive
condition w ill deteriorate.20,21 Num erous im aging m odalit ies have for detect ing isch em ic st roke th an a conven t ion al n on con t rast
been invest igated for clin ical use in determ in ing th e pen um bral CT of th e h ead in an acu te set t ing (Fig. 18.1a).28,33 Th is feat u re
volum e, including positron em ission tom ography (PET),22,23 xenon m akes it a u sefu l tool for gauging salvageable t issu e w h en com -
CT (Xe-CT),7 diffusion -w eigh ted an d perfusion -w eighted MRI,24,25 bin ed w ith perfusion im aging.
an d perfusion CT.26 We focu s p rim arily on MRI an d CT, w h ich Beyon d a cer t ain volu m e of in farcted t issue, th e risk of reper-
appear to be th e m ost p ragm at ic an d easily accessible for select- fu sion inju r y ou t w eigh s th e p oten t ial ben efit s of successfu l t is-
ing pat ien ts as can didates for acu te reperfu sion th erapies.27 su e rep erfu sion . Alth ough exact volu m es are debated, Mlyn ash
and colleagues 34 obser ved that a diffusion -w eighted im aging vol-
um e greater th an 80 m L w as con sisten t w ith a poor progn ost ic
Magnetic Resonance Imaging outcom e, also know n as a m align an t profile. Pat ien ts w ith th is
Mu lt im odal MRI offers several im p or t an t advan t ages over CT profile are th erefore n ot good can didates for revascu larizat ion
w ith respect to th e accuracy of diagn osing both acute isch em ic procedu res such as in t ra-ar terial th erapies.
st roke an d h em orrh age.28 In th e era of perfu sion im aging, m u l-
t ip le perfu sion -w eigh ted p aram eters h ave been w ell st u died in
Apparent Diffusion Coefficient Map
assessing cerebral h em odyn am ics.29 Th e m ism atch bet w een th e
isch em ic core rep resen ted by diffu sion -w eigh ted im aging an d Th e app aren t diffu sion coefficien t is a con firm ator y m ap based
the hypoperfused region on perfusion-w eigh ted im aging has been on various degrees of diffusion w eigh t ing. Th is calculated m ap
hypoth esized to represen t an im aging surrogate for th e isch em ic provides a m ore quantitative assessm ent of restricted water m ove-
pen u m bra an d th erefore a tool to gu id e acu te m an agem en t .27 m en t an d yields a low er sign al relat ive to n orm al brain t issue in
Fu r t h er m ore, m agn et ic reson an ce an giograp hy (MRA) p rovid es acute st roke. Th is sign al rem ain s low for as long as 1 w eek after

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234 III Ischemic Stroke and Vascular Insufficiency

Fig . 18.1a,b (a) Four axial slices from a diffusion-


weighted im aging of an acute left m iddle cerebral artery
territory stroke. (b) The corresponding apparent diffu-
sion coefficient slices in the sam e patient.

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18 Diagnosis of Brain Infarction 235

th e on set of isch em ia. It th en becom es isoin ten se an d even t u ally Computed Tomography
hyp er in ten se.30 Based on t h ese ch aracter ist ics, a hyp er in ten se
diffu sion -w eigh ted im aging sign al sh ou ld correspon d to a hypo- Because MRI is n ot readily available at sm aller h ospit als w h ere
in ten se ap p arent diffu sion coefficien t m ap (Fig. 18.1b). p at ien t s m ay in it ially p resen t , t h ere h as been an effor t to in -
vest igate t h e abilit y of CT to ser ve as a reliable su r rogate for
d eter m in ing w h ich p at ien t s m igh t ben efit from in t ra-ar ter ial
Gradient-Recalled Echo rep er fu sion t h erap ies. Alt h ough CT is excellen t for d etect ing
Th e grad ien t -recalled ech o, or T2* sequ en ce, is a T2-w eigh ted h em or rh agic st roke, n on con t rast CT of th e h ead m ay n ot sh ow
sequ en ce u sed to d eter m in e t h e p resen ce of h em or rh age. De- an isch em ic st roke for m ore t h an 6 h ou rs. Th ere are m u lt ip le
oxygen ated blood p rodu cts are p aram agn et ic an d h ave a ch arac- sign s of early in farct ion in clu d in g, bu t n ot lim ited to, a hyp er-
terist ic low sign al in ten sit y. In th e acu te set t ing, soon after th e d en se vessel rep resen t ing an occlu sive t h rom bu s, blu r r ing of
ext ravasat ion of blood, a m ixt u re of oxygen ated an d deoxygen - t h e gray-w h ite ju n ct ion or in su lar ribbon from cerebral isch em ia
ated blood p rodu cts leads to a h eterogen eou s ap pearan ce (Fig. or ed em a, an d asym m et r ic su lcal effacem en t (Fig. 18.3). Un -
18.2). Th is sequen ce is h elpful for evaluat ing n ot on ly prim ar y for t u n ately, CT is st ill n ot as accu rate as d iffu sion -w eigh ted im -
hem orrhage but also h em orrhagic tran sform ation of an infarct.35 aging for d etect ing acu te isch em ic st roke.28,33 Th ere h as been

Fig. 18.2 Four axial cuts of a gradient-recalled echo se-


quence in a patient who sustained a left intraparenchym al
hem orrhage with intraventricular extension. Note the het-
erogeneit y of signal intensit y in the region of hemorrhage
indicative of hyperacute and acute blood products.

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236 III Ischemic Stroke and Vascular Insufficiency

a b

Fig. 18.3a–c (a) A hyperdense left m iddle cerebral artery (MCA) with blurring of
the insular ribbon and sulcal effacem ent of the left temporal lobe. (b) Blurring of
the gray-white junction involving the left caudate, internal capsule, and putam en.
(c) Sulcal effacem ent and blurring of the gray-white junction over the entire left
c MCA territory.

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18 Diagnosis of Brain Infarction 237

Fig. 18.4 ASPECTS delineation. There are 10 regions assessed, as follows: C, caudate; L, lentiform nucleus; IC, internal capsule; I, insula; and M1 to M6,
corresponding regions of the middle cerebral artery territory.

con sid erable literat ure on th e u se of th e Alber ta St roke Program t ract ion angiograp hy. How ever, bot h are relat ively good n on -
Early CT Score (ASPECTS) to im p rove select ion of pat ien t s for a invasive tools in th e physician’s arm am en t arium . Fig. 18.5 gives
n eu roin ter ven t ion al p roced u re. Th is score requ ires assessm en t exam ples of in t racran ial im aging m odalit ies.
of 10 sp ecific region s on a n on con t rast CT; on e p oin t is su b -
t racted for ever y abn orm al area (Fig. 18.4). Yoo an d colleagu es 36
fou n d th at pat ien ts w ith ASPECTS > 7 sh ow ed h igh er rates of a Perfusion-Weighted Magnetic
good ou tcom es as m easured by a m odified Ran kin Scale score Resonance Imaging
of 0–2. Perfusion -w eigh ted MRI is obt ain ed by adm in istering gadolin -
ium , a param agn et ic su bst an ce, an d m easuring th e in ten sit y of
Magnetic Resonance Angiography and a T2* sign al on sequen t ial sequen ces obt ain ed ever y 1 to 2 sec-
on ds. Th e am plit ude of th e sign al in ten sit y plot ted over a t im e
Computed Tomography Angiography cur ve is used to obt ain region al cerebral blood flow m aps, an d
In a st u dy by Bash an d colleagu es 37 from Un iversit y of Californ ia th e in tegral of t h is cu r ve is u sed to obt ain th e region al cerebral
at Los Angeles, th e sen sit ivit y of con t rast-en h an ced MRA w as blood volum e. Bolus arrival t im es in t issue are used to calculate
com p ared w it h CT an giograp hy (CTA) in d eter m in in g sten osis ot h er p er fu sion p aram eters, su ch as m ean t ran sit t im e, t im e
or occlusion of th e in t racran ial vessels. Th e sen sit ivit y of in t ra- to p eak, an d t im e of m a xim al con cen t rat ion (Tm a x ).39,40 Mu lt ip le
cran ial sten osis an d occlu sion on MRA w as 70% an d 87%, re- st u dies h ave been con du cted to d eterm in e h ow to ext rap olate
sp ect ively. Th e corresp on ding sen sit ivit ies on CTA w ere 98% an d t h ese p aram eters to clin ically m ean in gfu l valu es t h at can be
100%, resp ect ively. W h en ext racran ial vascu lat ure su ch as th e u sed to d eter m in e p en u m bral volu m es. If t h ese volu m es are
carot id bifu rcat ion s are assessed via th ese m odalit ies, CTA re- con siderably larger th an th e volu m e of isch em ic core obt ain ed
m ain s sligh tly su perior to con t rast-en h an ced MRA (97% vs 92 to via diffu sion -w eigh ted im aging, th ese pat ien t s could poten t ially
95%, respect ively).38 Neith er st u dy is as sen sit ive as digit al su b - ben efit from in t ra-ar terial reperfu sion th erapies.

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238 III Ischemic Stroke and Vascular Insufficiency

a b

Fig. 18.5a–c (a) Reconstructed axial magnetic resonance


angiography revealing an occlusion of the left internal
carotid artery and left m iddle cerebral artery (MCA).
(b) Com puted tom ography (CT) angiography m axim um -
intensit y projection showing a right MCA occlusion. (c) CT
c reconstructed image of the sam e right MCA occlusion.

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18 Diagnosis of Brain Infarction 239

Fig. 18.6 Soft ware generated m ism atch m ap. The region in pink represents the diffusion-weighted im aging (DWI) volum e (i.e., ischem ic core). The re-
gion in green represents the Tm ax volum e > 6 seconds (i.e., ischem ic penum bra). PWI, perfusion-weighted im age.

Th e Tm ax is on e of th ese w ell-st u died p aram eters in corporat- Tm ax of 6 seconds. Figs. 18.7 and 18.8 show m ultiple perfusion se-
ing th e t im e delay after d elivering a gadolin ium bolus.41 It h as qu en ces of a com p leted left m iddle cerebral ar ter y (MCA) st roke.
been supported by PET studies, w hich have found that a threshold Com pu ted tom ograp hy p erfu sion is slow ly evolving to bet ter
of m ore th an 5.5 secon ds is th e m ost sen sit ive value for pen u m - predict th e isch em ic p en u m bra via th e sam e p aram eters as MR
bral flow.40 Clinical data from th e Diffusion and Perfusion Im aging perfu sion , bu t n o defin it ive m eth od of qu an t ifying isch em ic core
Evaluat ion for Un derstan ding St roke Evolut ion St udy (DEFUSE) is universally accepted, m aking penum bral m ism atch a quandary.
dat aset from th e St an ford St roke Cen ter h as con firm ed th at a It is, h ow ever, prom ising th at a Tm ax of 6 secon ds on CT p erfu sion
Tm ax greater th an 6 secon ds correlates w ell w ith pen um bral t is- correlates w ell w ith a Tm ax of 6 secon ds on MRI based on prelim i-
su e. For th is reason , w e u se it as ou r n u m erator in determ in ing a n ar y dat a from th e DEFUSE 2 st udy. Ongoing st udies, su ch as th e
perfusion /diffu sion m ism atch . We defin e a m ism atch p rofile as a CT perfusion to predict Respon se to recan alizat ion in Isch em ic
perfusion lesion th at is m ore than 120%of the diffusion volum e.42 St roke Project (CRISP) st u dy an d su bgrou p an alyses of DEFUSE
Fig. 18.6 gives an exam p le of a p at ien t th at h as a good m ism atch 2 based at th e Stan ford Stroke Cen ter, are using cerebral blood
profile using a soft ware program that calculates diffusion-weighted flow an d cerebral blood volum e correlates to bet ter delin eate th e
im aging volu m e an d perfu sion -w eigh ted im aging based on th e isch em ic core on CT.

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240 III Ischemic Stroke and Vascular Insufficiency

Fig. 18.7 Axial perfusion im ages of a patient with a completed left m iddle cerebral artery stroke dem onstrating cerebral blood volum e (CBV), cerebral
blood flow (CBF), m ean transit tim e (MTT), and Tm ax. Note the reduction in CBV, delayed CBF, delayed MTT, and delayed Tm ax.

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18 Diagnosis of Brain Infarction 241

Fig. 18.8 Soft ware-generated m ism atch m ap from the sam e patient as the Tm ax volum e > 6 seconds (i.e., ischem ic penum bra). This patient did not
shown in Fig. 18.5a. The region in pink represents the diffusion-weighted have a mism atch ratio am enable to reperfusion therapy.
im aging (DWI) volum e (i.e., ischem ic core). The region in green represents

em ic st roke is an evolving field th at is t ran sit ion ing from a tem -


■ Conclusion poral w in dow to a radiograph ic w in dow to im p rove th e select ion
Th e in it ial bed sid e d iagn osis of st roke begin s w it h clin ical of p at ien t s for rep er fu sion t h erap ies. Given t h e h igh d egree
kn ow ledge based on a solid fou n dat ion of n eu roan atom ic local- of m orbid it y associated w it h brain in farct ion , t h e goal of opt i-
izat ion an d an appreciat ion of th e m u lt it ude of et iologies th at m izing th ese radiograp h ic select ion criteria is to im prove both
can affect a p at ien t ’s t reat m en t p lan . In an era of con st an t ly th e sh or t-term an d long-term clin ical ou tcom es for ou r st roke
im p roving im aging tech n ologies, th e acu te m an agem en t of isch - pat ien ts.

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26. Win term ark M, Flan ders AE, Velth uis B, et al. Perfusion -CT assessm en t of pler ult rason ography, CT angiography an d blood-pool-enh an ced MR an -
in farct core an d pen um bra: receiver operat ing ch aracterist ic cu r ve an aly- giography in assessing carot id stenosis: a com parat ive st udy w ith DSA in
sis in 130 pat ien t s suspected of acute h em isph eric st roke. St roke 2006; 170 pat ien t s. Radiol Med (Torin o) 2012;117:54–71
37:979–985 39. Roldan -Valadez E, Gon zalez- Gut ierrez O, Mar t in ez-Lopez M. Diagn ost ic
27. Grigor yan M, Tu ng CE, Albers GW. Role of diffusion an d perfusion MRI perform an ce of PW I/DW I MRI p aram eters in d iscrim in at ing hyp eracu te
in select ing pat ien t s for reperfusion therapies. Neu roim aging Clin N Am versu s acu te isch aem ic st roke: fin ding th e best th resh olds. Clin Radiol
2011;21:247–257, ix–x 2012;67:250–257
28. Ch alela JA, Kidw ell CS, Nen t w ich LM, et al. Magn et ic reson an ce im aging 40. Zaro-Weber O, Moeller-Har t m an n W, Heiss W D, Sobesky J. Maps of t im e
an d com puted tom ography in em ergen cy assessm en t of pat ien t s w ith to m axim um and t im e to peak for m ism atch defin it ion in clin ical st roke
suspected acu te st roke: a prospect ive com parison . Lan cet 2007;369:293– st udies validated w ith posit ron em ission tom ography. St roke 2010;41:
298 2817–2821
29. Baird AE, Warach S. Magn et ic reson an ce im aging of acu te st roke. J Cereb 41. Olivot JM, Mlyn ash M, Th ijs VN, et al. Opt im al Tm ax th resh old for predict-
Blood Flow Met ab 1998;18:583–609 ing pen um bral t issue in acute st roke. St roke 2009;40:469–475
30. Albers GW. Diffusion -w eigh ted MRI for evalu at ion of acute st roke. Neu- 42. Albers GW, Th ijs VN, Wech sler L, et al; DEFUSE Invest igators. Magn et ic
rology 1998;51(3, Suppl 3):S47–S49 reson an ce im aging profiles predict clin ical respon se to early reperfusion :
31. Sch aefer PW, Gran t PE, Gon zalez RG. Diffusion -w eigh ted MR im aging of th e diffu sion an d p erfu sion im aging evalu at ion for u n d erst an ding st roke
th e brain . Radiology 2000;217:331–345 evolu t ion (DEFUSE) st udy. An n Neurol 2006;60:508–517

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19 Carotid Disease
Nohra Chalouhi, Rohan Chitale, Pascal M. Jabbour, Stavropoula I. Tjoum akaris,
Aaron S. Dum ont, Robert Rosenw asser, and L. Fernando Gonzalez

Desp ite recen t advan ces in diagn osis an d m an agem en t , st roke are all con t ain ed w ith in th e carot id sh eath an d separate th e ICA
rem ain s th e th ird leading cau se of m or t alit y in th e Un ited St ates from t h e IJV. At th e level of th e soft palate, all n er ves bu t CN X
w ith m ore th an 143,579 death s each year.1 Carot id ath eroscle- exit th e carot id sh eath .
rot ic disease is a m ajor cau se of st roke an d h as, th erefore, been
exten sively scru t in ized. Th is ch apter review s an d discu sses im -
p or t an t fin dings regard ing t h e diagn osis an d m an agem en t of Relationships of Carotid Sheath
carot id disease. An terolaterally, th e carot id sh eath is covered by th e stern oclei-
dom astoid. Posterior to th e carot id sh eath lie th e longu s capit is
m uscle and superior cervical sym pathetic ganglion. Anterom edial
to th e carot id sh eath are th e ph ar yngeal m ucosa an d paraph a-
■ Relevant Anatomy r yngeal space. Laterally, below th e level of th e digast ric m uscle,
lie th e hyp oglossal n er ve, p ar t of th e an sa cer vicalis, an d th e lin -
Extracranial Internal Carotid Artery gual an d facial vein s.
Th e com m on carot id ar ter y (CCA), m easu ring ~ 7 m m in diam e-
ter, bifurcates in to th e in tern al an d extern al carot id ar teries. Th e
in tern al carot id ar ter y (ICA), th e larger of th e t w o bran ch es, is a Variations
paired st ru ct u re th at su p p lies th e bilateral cerebral h em isph eres. Alth ough th e CCA t ypically bifurcates at or n ear th e level of th e
Th e cer vical ICA (C1) as classified by Bou th illier et al,2 refers to thyroid car t ilage (C4), bifu rcat ion s can range from C1 to T2. Th e
t h e p or t ion of t h e ICA t h at begin s at t h e level of t h e CCA bifu r- m edial origin of th e ICA from th e CCA bifurcat ion occurs as a
cat ion an d en ds w h ere th e ICA en ters th e carot id can al of th e com m on variant. In addition, tortuosit y m ay exist, particularly in
pet rou s tem poral bon e. you ng ch ildren an d older adu lt s. A rare an om alou s origin of th e
ECA an d ICA from th e aor t ic arch m ay also occur. Un ilateral or
bilateral congen ital absen ce of th e ICA rarely occu rs an d is asso-
Carotid Bulb ciated w ith absen ce of th e bony carot id can al.3 Diffuse ICA n ar-
At th e m ost proxim al aspect of C1 is a focal dilat ion , m easuring row ing m ay be acqu ired from ath erosclerosis, dissect ion , vascu -
7.5 m m in diam eter, kn ow n as th e carot id bulb. Dyn am ic h elical lit is, or fibrom u scu lar dysp lasia. If h em odyn am ically sign ifican t
blood flow pat tern s w ith flow reversal an d stasis are obser ved sten osis is presen t , collateral circu lat ion m ay be p resen t . Du pli-
h ere as a result of th e presen ce of a bran ch poin t , pu lsat ile flow, cat ion or fen est rat ion of th e cer vical ICA m ay also be n oted, an d
and differing resistances in the runoff of the ICA and external ca- m ay com plicate su rgical opt ion s. Alth ough th ere are t ypically n o
rotid artery (ECA). Unidirectional antegrade flow is seen near the n am ed bran ch es from th e cer vical ICA, persistent hypoglossal or
apical divider, providing the m ajorit y of blood volum e to the brain. proatlantal-intersegm ental carotid-basilar anastom oses m ay exist.

Ascending Segment
Dist al to th e bulb, th e ICA n arrow s to a diam eter of ~ 4.7 m m , ■ Pathophysiology and Natural History
m arking th e secon d part of C1 kn ow n as th e ascen ding segm en t . Ext racran ial carot id ath erosclerosis is in t im ately associated w ith
Th e en t ire length of C1 ru n s w ith in th e carot id sh eath , w h ich is ath erosclerosis elsew h ere in th e body.4,5 In fact , 11 to 26% of pa-
a fascial sp ace t h at also con t ain s loose areolar t issu e, th e in ter- t ien ts w ith coron ar y ar ter y disease an d 25 to 49% of th ose w ith
n al jugu lar vein (IJV), ven ous plexus, postganglion ic sym path et ic periph eral ar ter y disease also h ave asym ptom at ic carot id ar ter y
n er ves, an d cran ial n er ves (CNs) IX to XII. stenosis.1 Risk factors for carotid atherosclerosis include older age,
cigaret te sm oking, ar terial hyper ten sion , diabetes, th e m et abolic
syn drom e, p hysical in act ivit y, h istor y of m yocardial in farct ion
Relationships of C1 Within the Carotid Sheath (MI), in creased total ch olesterol, in creased low -den sit y lipopro-
With in th e carot id sh eath , th e vagus n er ve (CN X) an d th e IJV lie tein (LDL) ch olesterol, decreased h igh -den sit y lipoprotein (HDL)
beh in d an d sligh tly lateral to th e ICA. Th e ICA begin s posterolat- ch olesterol, an d in creased t riglycerides.6–8 Th e prevalen ce of ex-
eral to th e ECA an d cou rses m edial to th e m ain ECA t ru n k as it t racran ial carot id sten osis is t w ice as h igh in m ales th an in fe-
ascen ds. In th e u pper n eck, th e glossoph ar yngeal (CN IX), vagus m ales. Hyperhom ocysteinem ia is also highly prevalent in patients
(CN X), spin al accessor y (CN XI), an d hypoglossal n er ves (CN XII) w ith ext racran ial cerebrovascular disease, th ough a relat ion sh ip

243

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244 III Ischemic Stroke and Vascular Insufficiency

w ith ischem ic even t s h as yet to be clearly establish ed.9 Oth er lateral ret in a or cerebral h em isp h ere. Th e m ajorit y of p at ien ts
factors su ch as carot id an atom y an d geom et r y, specifically ICA w ith sym ptom at ic carot id sten osis in it ially presen t w ith t ran -
angle an d ICA radius at bifurcat ion , m ay also en h an ce th e risk of sien t isch em ic at tacks (TIAs). In th ese pat ien ts, th e risk of st roke
stenosis in depen dent of t radit ion al vascular risk factors.10 is exceedingly h igh an d reach es 13% w it h in 90 days an d 30%
Th e ath erosclerot ic carot id plaqu e is com p osed of a core of w it h in 5 years.12 Th e sym ptom s of carot id ar ter y–related TIA
lipid surroun ded by a den se cap of fibrou s t issue an d sm ooth sh ou ld be differen t iated from ver tebrobasilar-related TIA. Motor
m uscle cells. Sym ptom at ic/un st able carot id plaques are part icu - an d sen sor y sym ptom s from carot id disease t ypically involve th e
larly pron e to ru pt u re or u lcerat ion , an d are com p osed of a th in , con t ralateral face an d body, w h ereas posterior circulat ion TIA
fibrous cap th at con t ain s large n um bers of m acroph ages an d T m ay lead to bilateral or crossed deficit s. Sym ptom s of carot id ar-
lym ph ocytes w ith sm all n u m bers of sm ooth m u scle cells. Con - ter y sten osis in clude t ran sien t m on ocular blin dn ess (am au rosis
versely, asym ptom at ic/stable plaqu es h ave a th ick cap w ith less fugax) from ret in al isch em ia, con t ralateral w eakn ess or pares-
in flam m ator y cells bu t a larger n u m ber of sm ooth m uscle cells. th esias, aph asia, dysar th ria, an d visu al field defect s. On th e oth er
Th e m ajorit y of st rokes associated w ith carot id disease app ear to h an d, sym ptom s of ver tebrobasilar TIA in clude at axia, diplopia,
resu lt from em bolizat ion from an ath erosclerot ic plaque or acute dysar th ria, an d bilateral visu al loss.
occlusion of th e carot id ar ter y (from plaque r upt ure) w ith distal
th rom bu s p rop agat ion .11 Som e st rokes cou ld also resu lt from hy-
poperfu sion (sten ot ic plaqu e) or dissect ion .
Ext racran ial carot id sten osis is respon sible for alm ost 30% of
acute strokes. Several predictors of stroke in patients w ith carotid
■ Perioperative Evaluation
stenosis have been identified. First, the risk of stroke is strongly A th orough h istor y an d physical exam in at ion sh ould be th e in i-
correlated to th e degree of sten osis regardless of th e ch aracteris- t ial step s in t h e evalu at ion of a p at ien t w ith p oten t ial carot id
t ics of th e plaqu e. As su ch , th e risk of st roke in sym ptom at ic p a- sten osis. For pat ien ts p resen t ing w ith acu te n eu rologic deficits,
t ien ts is 18.7% over 5 years for ≤ 50% sten osis, 22.2% over 5 years m an agem en t sh ould be directed tow ard pat ien t stabilizat ion ,
for 50 to 70% sten osis, an d 26% over on ly a 2-year period for diagn osis, an d t reat m en t accord ing to th e gu idelin es for st roke
≥ 70% stenosis.12 Paradoxically, despite its st rong correlation w ith care.21 It is also im por t an t to accu rately d eterm in e t h e severit y
th e d egree of sten osis, th e risk of st roke act u ally decreases in of carot id sten osis for risk st rat ificat ion an d proper pat ien t selec-
pat ien ts w h ose sten osis is bet w een 94 an d 99%. Ap ar t from th e t ion for carot id revascularizat ion .
degree of sten osis, th e risk of st roke is also su bstan t ially h igh er Th e sen sit ivit y (55–77%) an d sp ecificit y (52–71%) of carot id
in sym ptom at ic pat ien t s. As su ch , th e an n u al risk of st roke w ith auscultation in the detection of carotid stenosis are suboptim al.22
≥ 50% sten osis is 2.35% in asym ptom at ic p at ien t s versu s 4.4% Fu r t h erm ore, t h ere is n o cor relat ion bet w een t h e lou d n ess of
in sym ptom at ic pat ien ts.13,14 Likew ise, th e detect ion of cerebral bru it an d th e un derlying carot id sten osis. In fact , br uits m ay be
m icroem boli an d silen t cerebral in farct ion s are poten t ial m ark- su bstan t ially lou d w ith m ild sten osis an d com p letely disap pear
ers of h igh er st roke risk in pat ien t s w ith asym ptom at ic carot id w ith critical stenosis, causing m arked flow restriction. Neverthe-
sten osis. Not su rprisingly, patien ts w ith u n con t rolled cardiovas- less, carot id auscult at ion rem ain s an im port an t screen ing test in
cular risk factors (e.g., hyper ten sion , sm oking) are m ore likely to asym ptom at ic pat ien t s.
su ffer a st roke according to several st u dies.15,16 Th e progression Dop p ler u lt rasou n d is t h e m ost com m on ly u sed in it ial test
of carot id sten osis, w h ich occu rs an n ually in 4 to 29%of pat ien ts, to d etect h em odyn am ically sign ifican t carot id sten osis. It is a
is an ot h er factor th at ap pears to p redict th e risk of st roke. A re- n on invasive, radiat ion -free, in exp en sive, an d read ily available
cen t st u dy in 1,469 pat ien ts w ith asym ptom at ic carot id sten osis diagn ost ic tool. How ever, it is h igh ly dep en den t on operator skill
fou n d th at fast rates of progression of carot id lum in al n arrow ing an d exp erien ce, w ith large in terperson al variabilit y. In addit ion ,
w ere sign ifican tly associated w ith ipsilateral n eurologic even ts.17 Dop p ler u lt rasou n d can overest im ate th e degree of sten osis, an d
Pred ictors of sten osis p rogression in clu d e d iabetes, sm okin g, su btot al ar terial occlu sion m ay som et im es be m istaken for tot al
hyper ten sion , con t ralateral disease, an d severe sten osis. Fin ally, occlusion . Th e sen sit ivit y an d specificit y of carot id Doppler for
in t rap laqu e h em or rh age, as d etected by m agn et ic reson an ce detect ing carot id ar ter y sten osis are abou t 86% an d 87%, respec-
im aging (MRI), seem s to predict t h e risk of isch em ic even t s in t ively.23 In dicat ion s for carot id Doppler test ing in clude pat ien t s
pat ien ts w ith carot id sten osis.18 presen ting w ith n eu rologic sym ptom s related to th e left or righ t
Of n ote, th e risk of coron ar y even t s m ay exceed th e risk of ICA territor y; asym ptom at ic pat ien ts w ith carot id bruit on aus-
st roke in pat ien t s w ith carot id sten osis. In fact , w ith carot id ste- cultat ion ; asym ptom at ic pat ien ts w ith sym ptom at ic periph eral
n osis ≤ 75%, th e an n ual rate of st roke is n egligible, w h ereas th e ar terial disease (PAD), coron ar y ar ter y disease, or aor t ic an eu-
com bined risk of coronar y and vascular events is as high as 9.9%.19 r ysm ; an d asym ptom at ic pat ien ts w ith m ult iple cardiovascu lar
Accordingly, the carotid intim a-m edia thickness (IMT), m easured risk factors.
by carot id u lt rasoun d, is a m arker of system ic ath erosclerosis Pat ien t s w ith sign ifican t fin dings on carot id Doppler sh ould
an d h as been con sisten tly fou n d to predict th e risk of MI.20 u n dergo fu r th er w orkup w ith advan ced im aging using m agn et ic
reson an ce angiography (MRA), com p uted tom ography angiogra-
p hy (CTA), or conven t ion al angiograp hy for bet ter d ep ict ion of
an atom y, collateral circu lat ion , an d p laqu e m or p h ology. Th is
w orku p facilit ates evalu at ing th e in t racran ial vascu lat u re to ex-
■ Clinical Presentation clude tandem lesions. MRA and CTA h ave excellent sensit ivit y and
A carot id sten osis is con sidered sym ptom at ic in th e presen ce of specificit y an d h ave gain ed a sign ifican t role as con firm ator y
t ran sien t or perm an en t n eu rologic sym ptom s related to th e ip si- test s in pat ien t s w ith clin ically sign ifican t sten osis on Doppler.

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19 Carotid Disease 245

MRA h as a sen sit ivit y ranging from 92.6 to 98% an d a sp ecificit y resu lt s of th e NASCET w ere publish ed in 1998 an d sh ow ed a sig-
ranging from 90 to 100%.1 Im port an tly, in con t rast to Dopp ler or n ifican t ben efit , th ough less m arked, in pat ien t s w ith 50 to 69%
CTA, MRA h as t h e advan t age of bein g relat ively in sen sit ive to sten osis (risk of ipsilateral st roke w as 15.7% at 5 years w ith CEA
ar terial calcificat ion s, w h ich m akes it th e preferred im aging m o- vs 22.2%w ith m edical t reat m en t).13 Pat ien ts w ith sten osis of less
dalit y in th is set t ing. How ever, MRA m ay overest im ate t h e d e- th an 50%, h ow ever, w ere n ot fou n d to ben efit from CEA. Th ese
gree of sten osis an d m ay be part icu larly p oor at dist inguish ing fin d in gs w ere cor roborated by t h e ECST, w h ich ran d om ized
su btotal from total occlu sion . MRA m ay also n ot be feasible in 2,518 pat ien ts w ith carot id sten osis an d repor ted a sim ilar ben -
m orbidly obese patients, claustrophobic patients, and those w ith efit for sym ptom at ic pat ien t s w ith ≥ 70%sten osis, bu t n o ben efit
m et al im plan t s. CTA is preferred by m any clin ician s given it s for th ose w ith less th an 70% sten osis.26 Overall, CEA provides a
abilit y to provide direct im aging of th e arterial lum en , w ith h igh - m arked ben efit over m edical m an agem en t in term s of st roke
qu alit y im ages an d th ree-dim en sion al ren derings th at facilit ate preven t ion for p at ien t s w ith ≥ 70%sten osis w ith a p ersisten t bu t
assessm en t of th e disease. Its sen sit ivit y an d specificit y are 85% less st riking ben efit in th ose w ith less severe sten osis (50–70%).
an d 93%, respect ively.24 CTA h as m ult iple advan tages over MRA It is curren tly recom m en ded th at sym ptom at ic pat ien t s at aver-
in clu ding faster data acqu isit ion , bet ter toleran ce by claust ro- age or low surgical risk undergo CEA w ithin 6 m onth s of sym ptom
p h obic p at ien t s, an d im p lan t able d evice (p acem akers, d efibr il- on set in th e presen ce of a carot id sten osis of ≥ 70% on n on inva-
lators, etc.) com pat ibilit y. CTA m ay be lim ited by th e p resen ce of sive im aging (class I; level of eviden ce: A) or ≥ 50% on cath eter
ar terial calcificat ion s, the possible overlap w ith bony an d ven ous angiography (class I; level of eviden ce: B) if th e an t icipated rate
st r u ct u res, an d t h e exp osu re to ion izin g rad iat ion . Becau se of of perioperat ive st roke or m or talit y is less th an 6%.12 Because
t h e n eed for iodin ated con t rast agen t s, MRA is u su ally preferred su bgrou p an alysis of th e RCT sh ow ed th at perioperative risks
over CTA for pat ien ts w ith ren al in su fficien cy. Overall, MRA an d w ere n ot in creased in pat ien ts un dergoing early revascu lariza-
CTA are ver y useful an d n on invasive im aging tech n iques th at can t ion , su rger y sh ou ld p referably be perform ed w ith in 2 w eeks of
provide accu rate assessm en t of th e degree an d m orph ological th e in d ex even t (class IIa; level of evid en ce: B). Carot id revascu -
feat ures of carot id sten osis, th us obviat ing th e n eed for cath eter larizat ion is n ot recom m en ded in p at ien t s w ith less th an 50%
angiography in m ost cases. sten osis (class III; level of eviden ce: A), th ose w ith ch ron ic tot al
Conven t ion al angiography rem ain s th e gold st an dard for th e occlusion of th e t argeted ar ter y (class III; level of eviden ce: C),
assessm en t of carot id sten osis. How ever, because of it s costs an d an d th ose w ith severe disabilit y caused by cerebral infarct ion
risks (in clu ding th e risk of st roke), th e p rocedu re is rarely em - (class III; level of eviden ce: C).12
ployed as a diagn ost ic tool an d h as been reser ved for cases in
w h ich n on invasive im aging is in con clusive or n ot feasible. Cath -
eter angiograp hy exp oses t h e p at ien t to sign ifican t r isks bu t
Asymptomatic Carotid Disease
sh ou ld be con sid ered in cases in w h ich th e sten osis cou ld be With th e w idespread availabilit y an d in creasing use of n on inva-
t reated during th e sam e p rocedu re. sive im aging m odalit ies, m ost p at ien t s diagn osed w ith carot id
disease are asym ptom at ic. Th e p oten t ial ben efit of t reat m en t for
pat ients diagn osed w ith an asym ptom at ic carot id stenosis should
alw ays be w eigh ed again st th e n at ural h istor y of th e disease an d
■ Treatment Modalities th e risk of t reat m en t . In fact , pat ien t select ion for carot id revas-
cu lar izat ion sh ou ld t ake in to accou n t t h e p at ien t ’s life exp ec-
Deter m in in g t h e best t reat m en t st rategy for carot id sten osis t an cy, com orbid con d it ion s, an d p referen ces, after a t h orough
h as gen erated an exten sive an d ongoing debate. Th erapeu t ic op - discu ssion of p oten t ial risks an d ben efits of th e p rocedu re. Tw o
t ion s in clu de m edical t reat m en t , carot id en dar terectom y (CEA), large RCTs, t h e Asym ptom at ic Carot id At h erosclerosis St u dy
an d carot id ar ter y sten t ing (CAS). Several ran dom ized con t rolled (ACAS) an d th e Asym ptom at ic Carot id Su rger y Trial (ACST), es-
t rials (RCTs) h ave en h an ced ou r kn ow ledge of th e com parat ive tablish ed a n et ben efit of CEA for asym ptom at ic pat ien ts w ith
outcom es of th ese t reat m en t opt ion s. Th e Am erican St roke As- a sten osis exceeding 60%. In th e ACAS, a total of 1,662 pat ien ts
sociat ion (ASA) an d th e Am erican Hear t Associat ion (AHA) along w ith asym ptom at ic carot id sten osis w ere ran dom ized to eith er
w ith other em inent organizations have recently published an up - m edical m an agem en t alon e or m edical m an agem en t w ith CEA.
dated eviden ce-based gu idelin e on th e m an agem en t of carot id Th e t rial w as stopp ed after 2.7 years w h en a ben efit to CEA be-
disease.12 cam e app aren t for p at ien t s w ith ≥ 60%sten osis (p rojected 5-year
rates of ipsilateral st roke, perioperat ive st roke, an d death w ere
5.1% w ith CEA vs 11% w ith m edical t reat m en t alon e). In terest-
Symptomatic Carotid Disease ingly, sign ifican t ben efit w as fou n d in m en but n ot in w om en . Of
Th e Nor th Am erican Sym ptom at ic Carot id En dar terectom y Trial n ote, th ese results sh ould be in terpreted in ligh t of th e rem ark-
(NASCET) an d th e European Carot id Surger y Trial (ECST) h ave ably low rate of perioperat ive st roke (2.3%) obser ved in th is t rial,
clearly est ablish ed t h e ben efit of CEA over m ed ical m an age- w h ich is due to th e fact th at CEA procedures w ere perform ed
m en t alon e in sym ptom at ic p at ien t s w ith severe carot id sten osis exclu sively by exp erien ced su rgeon s.27 In lin e w ith th e result s of
(≥ 70%). Th e NASCET ran d om ized sym ptom at ic p at ien t s from th e ACAS, th e ACST en rolled 3,120 p at ien t s w ith asym ptom at ic
50 cen ters to CEA an d m edical th erapy versus m edical th erapy carot id sten osis greater th an 60% an d rep or ted a 6.4% rate of
alon e.25 Th e t rial w as stopped after 18 m on th s of follow -up for st roke or death over 5 years in th e early-su rger y grou p versu s
pat ien ts w ith 70 to 99% sten osis becau se of a sign ifican t ben efit 11.7%in the group initially m anaged m edically. Collectively, these
w ith CEA. As such , th e cum ulat ive ipsilateral risk of st roke w as dat a suggest th at it is reason able to perform CEA in asym ptom -
9%at 2 years w ith CEA versu s 26%w ith m edical th erapy. Fu rth er at ic pat ients w ith ≥ 70%sten osis if th e risk of perioperat ive st roke,

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246 III Ischemic Stroke and Vascular Insufficiency

MI, an d death is low (class IIa; level of eviden ce: A).12 Im p or tan tly rot id disease ≥ 60% but w as stopp ed in 2005 because of a h igh er
h ow ever, because th ese t rials predate recen t advan ces in m edical 30-day rate of st roke an d adverse even t s in pat ien ts un dergoing
m an agem en t , it is un kn ow n w h eth er con tem porar y in ten sive CAS.31 Th is st udy w as crit icized for n ot m an dat ing th e u se of an
m edical th erapy cou ld n egate th e relat ive ben efit obser ved w ith EPD in all pat ien t s, for exclu ding MI from th e p rim ar y en d poin t ,
CEA in th ese st u dies. Trials evalu at ing revascu larizat ion versu s an d for th e su bopt im al level of experien ce of en dovascular in ter-
con tem p orar y best m edical th erapy in p at ien t s w ith asym ptom - ven t ion ists, m any of w h om , in fact , w ere st ill in t rain ing.
at ic carot id disease are n eeded to opt im ize th e m an agem en t of Th e In tern at ion al Carot id Sten t ing St u dy (ICSS) is a large m u l-
th is rapidly grow ing pop u lat ion of pat ien ts. t icen ter t rial th at ran dom ized 1,713 p at ien t s w ith sym ptom at ic
carot id sten osis ≥ 50%to CEA an d CAS.32 Recen tly publish ed pre-
lim in ar y resu lts sh ow ed sign ifican tly h igh er adverse even t s, in -
Comparison of Surgical and clu ding th e risk of st roke, in th e CAS arm (th e 120-day com posite
rate of st roke, death , or procedu ral MI w as 8.5% in CAS pat ien t s
Endovascular Options vs 5.2% in CEA p at ien t s, p = 0.006). Th e m ain lim itat ion s of th is
Carot id en dar terectom y is a w ell-est ablish ed t reat m en t m odal- t rial stem from th e fact th at th e u se of an EPD w as n ot m an dated,
it y for carot id sten osis. How ever, desp ite its p roven efficacy, th e th e en rollm en t w as lim ited on ly to sym ptom at ic pat ien t s, an d
procedu re is invasive, u su ally requ ires gen eral an esth esia, an d th e t rain ing for en dovascu lar in ter ven t ion ists w as n ot st an dard-
carries a non -n egligible risk of cardiovascular events, w ound com - ized . Long-ter m follow -u p , sch ed u led at 3 years, is n eed ed to
p licat ion s, an d cran ial n er ve dam age. Recen t ly, CAS h as been con firm th e fin dings of th is in terim safet y an alysis.
proposed as a valid m in im ally invasive altern at ive to CEA w ith Fin ally, th e Carot id Revascu larizat ion En dar terectom y versus
several advan t ages th at in clu de few er cardiovascu lar com p lica- Sten t ing Trial (CREST) is th e largest an d p erh ap s th e m ost rigor-
t ion s, n o risk of cran ial n er ve p alsy, n eed for on ly m ild sedat ion , ously con ducted t rial com paring CEA and CAS in “conven t ion al
feasibilit y in pat ien t s w ith severe cardiac an d pu lm on ar y dis- risk” p at ien t s w ith carot id sten osis.33 Th e st u dy en rolled 2,522
ease, an d suitabilit y for pat ien t s w ith an atom ically ch allenging sym ptom at ic an d asym ptom at ic p at ien t s in th e Un ited States
lesion s or h istor y of n eck radiat ion . Th e m ajor lim itat ion of CAS and Canada an d found no significant difference bet w een CAS and
appears to be th e h igh er risk of p erioperat ive em bolic st rokes as CEA in th e com posite en d poin t of st roke, death , or MI at 30 days
com p ared w ith CEA. Im p or tan tly, th e u se of em bolic protect ion from th e p rocedu re (5.2% w ith CAS vs 4.5% w ith CEA, p = 0.38)
devices (EPDs) ap pears to be a key factor in redu cing th e risk of an d at a m ean follow -up of 2.5 years (7.2%w ith CAS vs 6.8%w ith
perioperat ive st roke as suggested by a recen t m et a-an alysis th at CEA, p = 0.51). How ever, th e risk of periprocedu ral st roke w as
com p ared CAS w it h an EPD (11 t r ials w it h 839 p at ien t s) an d fou n d to be sign ifican tly h igh er w ith CAS com pared w ith CEA
w it h ou t an EPD (26 t r ials w it h 2,357 p at ien t s), an d fou n d t h e (4.1%vs 2.3%, p = 0.01). Conversely, th e risk of MI or cran ial n er ve
r isk of p er iop erat ive st roke an d d eat h to be 5.5% in p at ien t s p alsy w as sign ifican t ly low er w it h CAS t h an w it h CEA (1.1%
t reated w ith ou t em bolic p rotect ion versu s on ly 1.8% in th ose vs 2.3% for MI, 0.3% vs 4.8% for cran ial n er ve palsy, respect ively;
t reated w ith cerebral p rotect ion .28 p < 0.05). A subgroup an alysis foun d th at pat ien t s younger th an
Several t rials h ave com p ared CEA to angioplast y an d sten t ing 70 years of age fared bet ter w ith CAS, w h ereas th ose 70 years or
in pat ien t s w ith carot id sten osis. Th e Sten t ing an d Angioplast y older w ere m ore likely to ben efit from CEA. Th e in clu sion of as-
w ith Protect ion in Pat ien t s at High Risk for En dar terectom y ym ptom at ic MI as a p rim ar y en d poin t in CREST h as been h arsh ly
(SAPPHIRE) t rial is on e of th e few t rials th at com pared CAS (w ith crit icized becau se of th e act ual clin ical relevan ce of a subclin ical
an EPD) w ith CEA.29 The trial included 334 high-risk patients w ith m yocardial en zym e leak an d it s qu est ion able im pact on a p a-
sym ptom at ic sten osis ≥ 50% or asym ptom at ic sten osis ≥ 80%. t ien t’s qu alit y of life as op posed to th e often debilitat ing im pact
High -risk p at ien t s w ere defin ed as th ose h aving at least on e of of a st roke on a pat ien t’s outcom e. In fact , if asym ptom at ic car-
th e follow ing criteria: clin ically sign ifican t card iac disease, se- diac even ts in CREST are exclu ded from th e p rim ar y en d poin t ,
vere p u lm on ar y disease, con t ralateral carot id occlu sion , con t ra- th e outcom es w ould n o longer be sim ilar an d CEA w ould be a
lateral lar yngeal-n er ve palsy, previou s radical n eck surger y or safer procedu re, w ith a low er in ciden ce of perioperat ive st rokes
radiat ion th erapy to th e n eck, recurren t sten osis after en darter- an d death th an CAS.
ectom y, an d age >80 years. Th e invest igators fou n d sim ilar ou t- Accord ing to th e recom m en dat ion s of th e ASA/AHA, CAS is
com es w ith p ossibly a m odest ben efit for CAS at 1 year (prim ar y in dicated as an altern at ive to CEA for sym ptom at ic pat ien t s at
en d p oin t of st roke/death over 1 year w as 12.2% w ith CAS vs average or low r isk of com p licat ion s associated w it h en d ovas-
20.1% w ith CEA, p = 0.004 for n on in feriorit y an d p = 0.053 for cu lar in ter ven t ion in th e presen ce of carot id sten osis ≥ 70% as
su p eriorit y). Longer follow -u p at 3 years sh ow ed th at th e in ci- docu m en ted by n on invasive im aging or ≥ 50%as docu m en ted by
den ce of st roke w as sim ilar in both grou p s (7.1% w ith CAS vs cat h eter angiography if th e an t icipated rate of periprocedu ral
6.7% w ith CEA; p = 0.945). st roke or m ort alit y is less th an 6%(class I; level of eviden ce: B).12
The Stent-Protected Angioplasty versus Carotid Endarterectomy CAS m ay also be con sidered for asym ptom at ic pat ien t s w ith ca-
(SPACE) t r ial in sym ptom at ic p at ien t s, con d u cted in Ger m any, rot id sten osis ≥ 70% (class IIb; level of eviden ce: B). It is reason -
ran d om ly assign ed 1,214 p at ien t s w it h sym ptom at ic sten osis able to ch oose CAS over CEA in pat ien t s w ith un favorable n eck
≥ 50% to CAS or CEA an d fou n d n o sign ifican t d ifferen ce in th e an atom y in cluding ar terial sten osis distal to th e secon d cer vical
rate of ip silateral isch em ic st roke or d eat h bet w een t h e t w o ver tebra or proxim al below th e clavicle (in t rath oracic) ar terial
grou p s after 2 years of follow -u p (9.5% w it h CAS vs 8.8% w it h sten osis, p reviou s ip silateral CEA, con t ralateral vocal cord p aral-
CEA, p = 0.62).30 Th e En dar terectom y Versus Sten t ing in Pat ien t s ysis, open t rach eostom y, con t ralateral carot id occlusion , radical
w ith Sym ptom at ic Severe Carot id Sten osis (EVA-3S) t rial w as su rger y, an d ir rad iat ion (class IIa; level of evid en ce: B).1 2 On
con du cted in Fran ce an d en rolled p at ien t s w ith sym ptom at ic ca- t h e oth er h an d, it is reason able to ch oose CEA over CAS in older

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19 Carotid Disease 247

a b

Fig. 19.1a,b An 82-year-old wom an with a symptom atic 98%stenosis of the left internal carotid artery (a,b). Because of the patient’s age and the heavy
concentric calcification of her lesion, she was referred for carotid endarterectomy.

pat ien ts, esp ecially w h en ar terial an atom y is u n favorable (Fig. p refer to sh u n t ever y p at ien t to m a xim ize cerebral p rotect ion .
19.1) for en dovascular in ter ven t ion (e.g., ar terial tor t uosit y an d Oth ers believe th at perform ing CEA w ith out a sh un t is a bet ter
calcificat ion s). option because shun t insertion can cause arterial dissection . Still,
m any ch oose to sh un t w h en th ere is eviden ce of n eu rologic defi-
cit w ith cross-clam ping, n oted eith er on elect roen ceph alogram
(EEG) m on itoring or by in t raoperat ive physical exam in at ion in
■ Surgical/ Endovascular Technique th e aw ake pat ien t .
Th e p at ien t is p laced in th e su pin e p osit ion w ith th e h ead ex-
Pr ior to p er for m in g eit h er CEA or CAS, t h e su rgeon m u st h ave ten ded an d t urn ed aw ay from th e side of th e operat ion to sit u ate
a com p lete u n d erst an d ing of t h e p at ien t ’s vascu lar an atom y th e ICA lateral to th e ECA for ease of exposu re. W h en th e ICA is
t h rough exam in at ion of all d iagn ost ic im agin g. Th is in clu d es m edial to th e ECA at th e bifurcat ion , m obilizat ion of th e ECA m ay
kn ow ledge of th e paten cy of both ver tebral ar teries an d th e con - be n ecessar y to exp ose th e ICA.
t ralateral carot id ar ter y. Th e p at ien t an d fam ily m ust be aw are Th e in cision is lin ear along th e an terior border of th e stern o-
of risks, ben efits, an d altern at ives of th e p rocedu re. cleidom astoid m u scle, cen tered u p on th e est im ated level of th e
Th ere is a variet y of an esth et ic an d m on itoring con siderat ion s bifurcat ion . A self-ret ain ing ret ractor is p laced, leaving th e jugu-
for eith er procedure. Both procedures can be perform ed w ith th e lar vein on t h e lateral asp ect of t h e exp osu re. Th is m an eu ver
pat ien t eith er u n der gen eral sedat ion w ith m on itoring or aw ake places th e ICA in a m ore su p erficial p osit ion . Care m u st be taken
w ith con scious sedat ion . For a CEA, in t raoperat ive assessm en t of to avoid lar yngeal n er ve injur y m edially an d CN XI an d XII injur y
vascu lar perfu sion can be accom plish ed th rough st um p pressure laterally w ith ret ract ion . Exposure of th e CCA, ECA, an d ICA is
m on itoring, xen on region al cerebral blood flow st u dies, t ran s- perform ed w ith carefu l at ten t ion to vital sign s as th e carot id
cran ial Dopp ler, an d angiograp hy. Cerebral fu n ct ion in both p ro- bulb is m an ipulated. Th e proxim al CCA, dist al ICA, an d distal ECA
cedu res m ay be m on itored w ith elect roen ceph alography an d are dissected in a circum feren t ial 360 degree w h ile th e bifurca-
som atosen sor y evoked p oten t ials. t ion (w h ere th e CEA w ill be perform ed) is left w ith ou t dissect ion
u n dern eath to p reven t t w ist ing of th e ar ter y. After inject ion of
in t raven ous bolu s of 5,000 u n it s of h eparin , th e ICA, CCA, an d
Carotid Endarterectomy ECA are clam p ed in th is specific sequen ce. In adver ten t clam ping
Several opt ion s exist for perform ing a CEA. Th ere is n o con sen su s of t h e vagu s n er ve an d clam p ing of t h e ECA d ist al to it s m ost
regarding t h e n eed for in t raop erat ive sh u n t ing. Som e surgeon s proxim al bran ch es m u st be avoided. Th e m icroscope is brough t

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248 III Ischemic Stroke and Vascular Insufficiency

in to th e field an d th e rest of th e operat ion is perform ed u n der cath eter is p arked p roxim al to th e lesion , th e area of sten osis is
m agn ificat ion an d illu m in at ion . An ar ter iotom y is p er for m ed crossed w ith a distal protect ion device at tach ed to a w ire th at
w ith a No. 11 blade an d fin ish ed w ith Pot ts scissors. Carefu l dis- is su bsequen tly used for th e angioplast y an d sten t ing procedu re
sect ion of th e in t ralu m in al p laqu e is th en p erform ed w ith a Pen - (Fig. 19.2). Th e pract it ion er m ay ch oose eith er to perform predi-
field No. 4 dissector. Th e plaqu e is cut w ith scissors from th e CCA lat ion w ith a balloon in cases w h ere th e sten osis is severe (1 m m
an d th e ICA, an d p u lled an d ever ted from th e ECA. or less ar terial lum en ), or proceed w ith a self-expan ding sten t .
After th e plaque is rem oved, th e ar teriotom y is repaired w ith Predilat ion im p lies crossing t h e sten osis t w ice, w h ich carries th e
6-0 n on absorbable sut ure. First th e superior thyroid ar ter y an d risk of dislodging em bolic fragm en t s from th e p laqu e. Th e size
th e ECA clips are open ed, an d th en th e CCA is open ed briefly. of th e sten t m ust be long en ough to cross th e en t ire plaqu e an d
Th is en ables debris to flow ou t th rough th e ECA. With th e CCA m ust h ave a pre-deploym en t diam eter sim ilar to th e diam eter of
closed again , th e ICA clip is op en ed an d debris flow s backw ard th e CCA. Th e sten t is p osit ion ed to cross th e ECA w ith care to
from ICA to th e bifu rcat ion an d in to th e ECA. Th is is th en fol- avoid an en doleak. After th e sten t is placed, postdilat ion is per-
low ed by ICA clip rep osit ion ing an d fin al CCA clip open ing. Lastly, form ed if residual sten osis is n oted. A fin al angiograph ic r un is
th e ICA clip is rem oved. On ce h em ost asis is ach ieved an d Dop - com pleted to obser ve stent patency, reestablishm ent of flow, and
pler u lt rason ography or, lately, in docyan in e green flu orescen ce eviden ce of dissect ion or oth er th rom boem bolic even t s.
angiograp hy con firm s blood flow, closu re can be com pleted. Of n ote, cerebral protect ion from m icroem bolizat ion can also
be ach ieved using flow reversal tech n iqu es th rough eith er a
t ran scer vical or t ran sfem oral ap p roach . In sh or t , after occlu sion
Stenting of th e ECA an d proxim al CCA, an ar terioven ous sh un t is created
Pat ien t s are p laced on du al an t ip latelet agen ts, gen erally aspirin bet w een th e ICA an d th e IJV, th us in it iat ing flow reversal from
an d clopidogrel, for at least 5 days prior to th e procedure. Th e th e ICA in to th e ven ou s system . Th e m ain advan t age of th is tech -
pat ien t is preop erat ively prep ared w ith a p ercu tan eou s p acer to n ique over an EPD is th at cerebral protect ion is establish ed be-
avoid angioplast y-in duced bradycardia an d hypoten sion . Vascu- fore crossing th e lesion , w h ich is on e of th e m ost em boligen ic
lar access is obtain ed th rough in ser t ion of an 8 Fren ch (F) sh eath m an euvers in CAS. Th e relat ive com plexit y of th e procedu re, th e
in to t h e fem oral ar ter y via th e Seld inger tech n iqu e. Of n ote, in toleran ce to flow reversal in som e cases, an d th e fact th at flow
som e sten t s allow th e u se of a 6F sh eath for access. A con t in u ou s reversal m ay n ot be ach ieved th rough ou t th e en t ire procedu re
h ep ar in flu sh is u sed to m it igate t h e r isk of t h rom boem bolic (as it depen ds on th e ar terioven ou s pressure gradien t) are th e
even t s related to en dovascu lar m an ip u lat ion . On ce t h e gu id e m ain draw backs of th e tech n iqu e.

a b

Fig. 19.2a–f A 59-year-old m an with a 98% symptom atic stenosis of the right internal carotid artery (ICA) (a,b).

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19 Carotid Disease 249

c d

e f

Fig. 19.2a–f (continued ) (c) The stenosis was crossed with a distal em bolic protection device. (d) Balloon angioplast y was perform ed prior to stent de-
ploym ent. (e,f) Post-stent arteriogram s revealed m arked improvem ent in lum en caliber of the ICA.

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250 III Ischemic Stroke and Vascular Insufficiency

cat ion sh ou ld be in it iated in pat ien t s w ith asym ptom at ic an d


■ Patient Outcomes sym ptom at ic (outside th e hyperacute period) carot id sten osis to
Th e risk of perioperat ive adverse even t s ranges from 2.5 to 6% m ain tain blood pressure below 140/90 m m Hg. Becau se sm oking
w ith eith er CEA or CAS. Possible com plicat ion s of CEA in clude sign ifican tly in creases th e risk of st roke, all pat ien ts sh ou ld be
hem orrhage, hypertension , hypotension , acute arterial occlusion, st rongly advised to qu it sm oking. In it iat ion of st at in t h erapy is of
st roke, MI, ven ou s th rom boem bolism , in fect ion , cran ial n er ve param ou n t im p or tan ce to red u ce LDL levels below 100 m g/dL for
palsy, ar terial resten osis, an d death . Com p licat ion s of CAS in - asym ptom at ic pat ien ts an d 70 m g/dL for sym ptom at ic pat ien ts.
volve st roke, access-site com plicat ion s, t arget vessel p erforat ion , Diet , exercise, an d glu cose-low ering drugs can be useful for pa-
extern al carot id ar ter y occlu sion , d evice m alfu n ct ion , resten osis, t ien ts w ith diabetes m ellit u s an d carot id disease. Given th e as-
an d death . As discu ssed above, periprocedural st rokes are m ore sociat ion bet w een carot id ath erosclerosis an d coron ar y even ts,
likely to occu r w ith CAS. How ever, based on th e resu lt s of several aspirin (81 to 325 m g daily) is recom m en ded to preven t cardio-
large t rials, in clu ding SAPPHIRE, SPACE, an d CREST, th e rate of vascu lar even ts. For th ose w h o sustain ed a TIA/st roke, aspirin ,
fu t u re ip silateral isch em ic even ts is sim ilar w ith both m odalit ies clop idogrel, or a com bin at ion of asp irin p lu s exten ded-release
an d ranges ap p roxim ately from 1 to 2% p er year for sym ptom - dipyridam ole is recom m en ded.
at ic pat ien t s 13,26 an d 0.5 to 0.8% p er year for asym ptom at ic pa- For pat ien ts u n d ergoing CAS, du al an t ip latelet th erapy w ith
t ien ts.27,34 Th e risk of h em odyn am ically sign ifican t resten osis is aspirin (81 to 325 m g daily) an d clopidogrel (75 m g daily) sh ould
abou t 5 to 7% in large t r ials an d ap p ears to be h igh er w it h CAS. be in it iated at least 5 days prior to th e procedure an d con t in ued
In th e SPACE t rial, th e 1-year rates of resten osis ≥ 70% w ere 4.6% for a m in im um of 1 m on th th ereafter. For th ose un dergoing CEA,
w ith CEA an d 10.7% w ith CAS as assessed by u lt rasoun d.30 How - aspirin (81 to 325 m g daily) sh ould be st ar ted prior to th e proce-
ever, th e rates depen d largely on th e defin it ion of resten osis, th e du re an d con t in u ed in defin itely p ostoperat ively. Periprocedural
im aging tool (w ith p ossible sten t-gen erated art ifact s), dup lex blood pressure con t rol an d in it iat ion of st at in th erapy are also of
velocit y criteria used, an d durat ion of follow -u p. Fur th erm ore, param ou n t im por tan ce w ith eith er CAS or CEA.
resten osis h as lit t le clin ical relevan ce, w it h t h e vast m ajor it y
being asym ptom at ic an d, w h en in dicated, easily am en able to re-
peat en dovascu lar t reat m en t w ith angiop last y alon e. Non inva-
sive im aging of th e ext racran ial carot id ar teries is recom m en ded ■ Conclusion
at 1 m on th , 6 m on th s, an d an n u ally after CAS or CEA to r ule ou t
Th e m an agem en t of carot id disease h as greatly evolved in recen t
resten osis an d n ew /con t ralateral lesion s.
years, com m en su rate w ith th e advan ces in m edical th erapy an d
en dovascu lar th erapy. CEA rem ain s th e stan dard p rocedu re for
carot id revascu larizat ion , bu t CAS is em erging as a valid an d rea-
Adjunct Therapies son able altern at ive for m any pat ien ts. Fu t u re im provem en ts in
Man agem en t of p at ien t s w it h carot id sten osis sh ou ld also be sten t s, EPDs, tech n iqu e, an d op erator experien ce w ill u n dou bt-
d irected tow ard con t rolling risk factors. An t ihyper ten sive m edi- edly im p rove th e safet y of CAS.

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t ion s w ith cardiovascular risk factors in the ARIC st udy. Am J Epidem iol Am erican Associat ion of Neu rological Surgeon s, Am erican College of Ra-
1991;134:250–256 diology, Am erican Societ y of Neuroradiology, Congress of Neu rological
7. Tat sukaw a M, Saw ayam a Y, Maeda N, et al. Carot id ath erosclerosis an d Surgeon s, Societ y of Ath erosclerosis Im aging an d Preven t ion , Societ y for
cardiovascular risk factors: a com parison of residen t s of a r ural area of Cardiovascular Angiography an d In ter ven t ion s, Societ y of In ter ven t ion al
Okin aw a w ith residen t s of a t ypical suburban area of Fu kuoka, Japan . Ath - Radiology, Societ y of NeuroIn ter ven t ional Su rger y, Societ y for Vascular
erosclerosis 2004;172:337–343 Medicin e, an d Societ y for Vascu lar Su rger y Develop ed in Collaborat ion
8. Ebrahim S, Papacost a O, W hin cup P, et al. Carot id plaque, in t im a m edia With th e Am erican Acad em y of Neu rology an d Societ y of Cardiovascu lar
thickness, cardiovascular risk factors, and prevalent cardiovascular disease Com pu ted Tom ography. J Am Coll Cardiol 2011;57:1002–1044

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19 Carotid Disease 251

13. Barn et t HJ, Taylor DW, Eliasziw M, et al. Ben efit of carot id endar terectom y raphy in carot id ar ter y stenosis: a system at ic review. St roke 2003;34:
in pat ien t s w ith sym ptom at ic m oderate or severe sten osis. North Am eri- 1324–1332
can Sym ptom at ic Carot id En dar terectom y Trial Collaborators. N Engl J 24. Koelem ay MJ, Nederkoorn PJ, Reit sm a JB, Majoie CB. System at ic review of
Med 1998;339:1415–1425 com puted tom ograph ic angiography for assessm en t of carot id ar ter y dis-
14. Hobson RW II, Weiss DG, Fields WS, et al; Th e Veteran s Affairs Coopera- ease. St roke 2004;35:2306–2312
t ive St udy Group. Efficacy of carot id en darterectom y for asym ptom at ic 25. North Am erican Sym ptom atic Carotid Endarterectom y Trial Collaborators.
carot id sten osis. N Engl J Med 1993;328:221–227 Ben eficial effect of carot id en darterectom y in sym ptom at ic pat ien t s w ith
15. Kaw ach i I, Cold it z GA, St am p fer MJ, et al. Sm oking cessat ion an d d e- h igh -grade carot id sten osis. N Engl J Med 1991;325:445–453
creased risk of st roke in w om en. JAMA 1993;269:232–236 26. Ran dom ised t rial of en dar terectom y for recen tly sym ptom at ic carot id
16. MacMah on S, Peto R, Cutler J, et al. Blood pressu re, st roke, and coron ar y sten osis: fin al resu lt s of th e MRC Eu rop ean Carot id Su rger y Trial (ECST).
h ear t disease. Par t 1, Prolonged differen ces in blood pressure: prospect ive Lan cet 1998;351:1379–1387
obser vat ion al st udies corrected for th e regression dilut ion bias. Lan cet 27. Endarterectom y for asym ptom atic carotid arter y stenosis. Executive Com -
1990;335:765–774 m it tee for the Asym ptom at ic Carot id Ath erosclerosis St udy. JAMA 1995;
17. Hir t LS. Progression rate an d ipsilateral n eu rological even t s in asym ptom - 273:1421–1428
at ic carot id sten osis. St roke 2014;45:702–706 28. Kast r up A, Grösch el K, Krapf H, Breh m BR, Dich gans J, Sch ulz JB. Early
18. Alt af N, MacSw een ey ST, Gladm an J, Au er DP. Carot id int raplaque h em or- outcom e of carot id angioplast y an d sten t ing w ith an d w ith out cerebral
rh age predict s recurren t sym ptom s in pat ient s w ith high -grade carot id protect ion devices: a system at ic review of th e literat ure. St roke 2003;34:
sten osis. St roke 2007;38:1633–1635 813–819
19. Norris JW, Zh u CZ, Born stein NM, Ch am bers BR. Vascu lar risks of asym p - 29. Gu r m HS, Yadav JS, Fayad P, et al; SAPPHIRE Invest igators. Long-ter m
tom at ic carot id sten osis. St roke 1991;22:1485–1490 resu lt s of carot id sten t ing versu s en dar terectom y in h igh -risk p at ien t s.
20. Arn old AM, Psat y BM, Ku ller LH, et al. In ciden ce of cardiovascu lar disease N Engl J Med 2008;358:1572–1579
in older Am erican s: th e cardiovascular h ealth st u dy. J Am Geriat r Soc 30. Eckstein HH, Ringleb P, Allen berg JR, et al. Resu lt s of th e Sten t-Protected
2005;53:211–218 Angioplast y versus Carot id En darterectom y (SPACE) st udy to t reat sym p -
21. Adam s HP Jr, del Zoppo G, Alber t s MJ, et al; Am erican Heart Associat ion / tom atic stenoses at 2 years: a m ultinational, prospective, random ised trial.
Am erican St roke Associat ion St roke Coun cil; Am erican Heart Associat ion / Lan cet Neurol 2008;7:893–902
Am erican St roke Associat ion Clin ical Cardiology Coun cil; Am erican Heart 31. Mas JL, Ch atellier G, Beyssen B, et al; EVA-3S Invest igators. Endar terec-
Associat ion /Am erican St roke Associat ion Cardiovascu lar Rad iology an d tom y versu s sten t ing in pat ien t s w ith sym ptom at ic severe carot id sten o-
In ter ven t ion Coun cil; Ath erosclerot ic Periph eral Vascular Disease Work- sis. N Engl J Med 2006;355:1660–1671
ing Group; Qualit y of Care Outcom es in Research In terdisciplin ar y Work- 32. Ederle J, Dobson J, Feath erston e RL, et al; In tern at ion al Carot id Stent ing
ing Group. Guidelin es for th e early m an agem en t of adult s w ith isch em ic St udy invest igators. Carot id arter y sten t ing com pared w ith endarterec-
st roke: a gu id elin e from th e Am erican Hear t Associat ion /Am erican St roke tom y in pat ien t s w ith sym ptom at ic carot id sten osis (In tern at ion al Ca-
Associat ion St roke Cou n cil, Clin ical Cardiology Cou n cil, Card iovascu lar rotid Sten ting St udy): an in terim analysis of a ran dom ised controlled trial.
Radiology an d In ter ven t ion Coun cil, an d th e Atherosclerot ic Periph eral Lan cet 2010;375:985–997
Vascu lar Disease an d Qu alit y of Care Ou tcom es in Research In terd isci- 33. Brot t TG, Hobson RW II, How ard G, et al; CREST Invest igators. Sten t ing
p lin ar y Working Groups: Th e Am erican Academ y of Neu rology affirm s versu s en darterectom y for t reat m en t of carot id-ar ter y sten osis. N Engl J
th e valu e of th is gu idelin e as an edu cat ion al tool for n eu rologist s. Circu la- Med 2010;363:11–23
t ion 2007;115:e478–e534 34. Halliday A, Man sfield A, Marro J, et al; MRC Asym ptom at ic Carot id Sur-
22. Joh an sson EP, Wester P. Carot id br uit s as predictor for carot id sten oses ger y Trial (ACST) Collaborat ive Group. Preven t ion of disabling an d fat al
detected by ult rason ography: an obser vat ion al st u dy. BMC Neu rol 2008; st rokes by su ccessfu l carot id en dar terectom y in pat ien t s w ithou t recen t
8:23 n eurological sym ptom s: ran dom ised con t rolled t rial. Lan cet 2004;363:
23. Nederkoorn PJ, van der Graaf Y, Hun in k MG. Duplex u lt rasoun d an d m ag- 1491–1502
n et ic reson an ce angiography com pared w ith digit al subt ract ion angiog-

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20 Carotid Endarterectomy
Mark us Bookland and Christopher M. Loft us

On ce th e carot id bifu rcat ion h as been iden t ified, dist inguish -


■ Anatomy ing bet w een th e in tern al an d extern al bran ch es is quite easy. Th e
Th e su rgical m an agem en t of any disease requ ires a sou n d kn ow l- posteriorly p laced ICA h as n o ext racran ial bran ch es, w h ereas th e
edge of relevan t an atom ic fu n dam en t als. In carot id en dar terec- extern al carot id ar ter y (ECA; th e an terior fork of th e bifu rcat ion )
tom y (CEA) su rger y, th e m ost com m on site of sten osis lies at th e h as several. Th ese bran ch es, th e first of w h ich is th e su perior
bifurcat ion of th e com m on carot id ar ter y (CCA) in to it s extern al thyroid ar ter y, are u sefu l as an an atom ic referen ce for com p ari-
an d in tern al bran ch es. Th e locat ion of th is bifurcat ion along th e son w ith angiograp h ic im aging to determ in e th e exten t of th e
cau dal-cran ial cou rse of th e n eck m ay var y. Key an atom ic rela- ICA plaqu e. Th e su p erior thyroid n eeds to be con t rolled w ith a
t ion sh ip s as w ell as good an terop osterior (AP) an d lateral angio- su t u re to p reven t backbleeding w h en th e carot id t ree is op en .
graphic (or com puted tom ography angiography [CTA] or m agnetic Th e m ore distal bran ch es are above th e ECA cross-clam p site.
reson an ce angiograp hy [MRA]) im ages of th e relevan t arteries
m ay guide th e surgeon to th e level of th e lesion .
Th e CCA lies w ith in th e carot id sh eath an d t ravels from th e
great vessels at th e th oracic outlet to it s bran ch p oin t in th e n eck
along a cou rse m ed ial an d d eep to t h e ster n ocleid om astoid
■ Pathophysiology
m u scle an d in tern al jugu lar vein (IJV). Dissect ion an d ret ract ion Th e form at ion of a p laqu e at th e carot id bifu rcat ion is th e resu lt
of th e stern ocleidom astoid m uscle’s m edial border is on e of th e of t u rbu len t flow arou n d t h e CCA bran ch p oin t , act ivat ion of
earliest steps in any CEA. Care m ust be t aken n ot to dissect or clot t in g factors, in flam m at ion , an d aber ran t blood vessel w all
pull too aggressively along th is p lan e, as th e accessor y n er ve lies en d oth eliu m . Becau se th ese processes m ay occu r vir t u ally any-
deep to th is m u scle an d m ay be injured. Medially, deep to th e w h ere th rough out th e cardiovascular t ree, pat ien ts w ith carot id
stern ocleidom astoid, is th e IJV. Mu lt ip le bran ch es can be iden t i- ar ter y sten osis sh ou ld alw ays be invest igated for system ic oc-
fied along th e m edial edge of th e IJV (com m on facial v., su perior clu sive vascu lar disease. W h en en doth elial injur y, in flam m at ion ,
thyroid v., m iddle thyroid v.), an d th ey all m ay be safely ligated an d platelet aggregat ion form plaque along th e CCA, it is usually
an d t ran sected as exposure requ ires. Th e facial vein , w h ich is along th e posterior vessel w all w ith in 2 cm of th e bifurcat ion an d
t ypically th e largest vein off of th e in tern al jugu lar, often crosses focu sed w ith in th e ICA, creeping sligh tly in to th e com m on an d
just superficial to th e carot id bifurcat ion . Th is can provide a use- extern al carot id ar teries.
ful an atom ic lan dm ark for th e su rgeon . Even p ar t ial occlu sion of th e ICA via p laqu e form at ion can
Several im p or t an t n er ves also t ravel alon g or across t h e ca- lead to isch em ic sequ elae.1 Ult rasoun d obser vat ion s of th e ICA
rot id bifu rcat ion , an d t h ey m u st be id en t ified an d p rotected an d direct visualizat ion of ret in al ar teries h ave n oted m icroem -
d u r ing th e course of surger y to avoid postoperat ive cran ial n er ve boli proceeding from ICA sten osis. Th ese em boli can pass ceph a-
palsies. Th e t w o m ost com m on ly n oted n er ves du ring CEA su r- lad to ret in al an d cerebral vasculat u re, leading to t ran sien t an d
ger y are th e hypoglossal an d vagus n er ves. Th e vagu s exit s th e p er m an en t isch em ic even t s.2 Th e sever it y of isch em ic even t s
cran ium at th e jugular foram en an d t ravels in th e carot id sh eath varies from pat ien t to pat ien t an d depen ds largely on th e vessel
m edial an d deep to th e jugular vein in parallel w ith th e carot id occluded, durat ion of occlusion, an d degree of collateral flow to
ar ter y. Th e recu rren t lar yngeal n er ve, a bran ch of th e vagu s, is th e affected t issu es. Often , p at ien t s w ith sym ptom at ic vascu lar
also at r isk in th e t rach eoesop h ageal groove, an d can be dam - d isease at th e p roxim al ICA h ave a d egree of im p aired vasoreac-
aged by deep m edially placed retractors, leading to postoperat ive t ivit y w it h in t h e cerebral vascu lat u re, lim it in g t h eir abilit y to
h oarsen ess. We h ave m odified ou r exposure to use on ly blun t com pen sate for acu te em bolic even t s.3
fishhooks, and rarely see lar yngeal ner ve palsies since this change. Left u n t reated, ext racran ial ICA sten osis m ay p rogress to
Th e hyp oglossal n er ve descen d s bet w een th e in tern al jugu lar com p lete occlu sion . If th ere is in adequ ate collateralizat ion at t h e
vein an d th e in tern al carot id ar ter y, u su ally w ell above th e ca- t im e of tot al occlu sion , it m ay lead to severe st roke. Even after
rot id bifu rcat ion , an d crosses th e in tern al carot id arter y (ICA) obliterat ion of a single ICA, th e low -flow state created n ear th e
run n ing m edially to its t arget m uscles. In a low or st an dard ca- occlusion poin t can con t in u e to gen erate th rom bus th at m ay
rot id exposu re, th e hyp oglossal n er ve is n ot an issue, bu t it h as to propagate distally. Th e risk of isch em ic even t s follow ing total ICA
be gen tly m obilized in cases w h ere h igh exposu re of th e dist al occlusion decreases w ith t im e, an d it becom es n egligible 1 year
ICA is n eeded. Alth ough it is n ot a dist in ct n er ve, th e p ericarot id follow ing tot al occlu sion .4
sym path etic ch ain also bears som e m ention, as inadvertent dam - Som e specific p laqu e ch aracterist ics ap pear to p or ten d cere-
age to th is p lexu s du ring su rger y can lead to an ipsilateral p ost- bral isch em ia. Th e percen tage of lum in al occlusion created by a
operat ive Horn er’s syn drom e. plaqu e h as been th e m ost clearly an d th orough ly st u died qu alit y

252

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20 Carotid Endarterectomy 253

of carot id plaques. Based on th e Nor th Am erican Sym ptom at ic


Carot id En dar terectom y Tr ial (NASCET) an d t h e Eu rop ean Ca-
rot id Su rger y Tr ial (ECST), a sym ptom at ic p at ien t w it h rad io -
grap h ic eviden ce of ext racran ial carot id arter y sten osis > 50%
w ill risk an approxim ate 26% t w o-year in ciden ce of st roke. Like-
w ise, based on th e Asym ptom at ic Carot id Ath erosclerosis St udy
(ACAS) an d th e Asym ptom at ic Carot id Surger y Trial (ACST), an
asym ptom at ic pat ien t w ith radiograph ic eviden ce of ext racra-
n ial carot id ar ter y sten osis > 60% h as rough ly an 11% five-year
risk of stroke.5 These data convincingly correlate increasing linear
sten osis an d vessel occlu sion w ith cerebral isch em ia an d h ave
ser ved as th e fou n dat ion for cu rren t recom m en dat ion s regard-
ing su rgical in ter ven t ion . Plaqu e ulcerat ion , rupt u re, an d h em or-
rh age h ave also been p osited as in dicators of an u n st able carot id
ar ter y plaque th at is m ore likely to gen erate th rom bu s an d em -
boli. How ever, to date t h ere are lim ited dat a to con fir m t h at
any of th ese p laqu e qu alit ies reliably p red ict cerebral isch em ia,
an d several st udies h ave n oted com parable in ciden ces of ulcer-
at ion an d h em orrh age in both sym ptom at ic an d asym ptom at ic
pat ien ts.6,7

■ Clinical Presentation and


Perioperative Evaluation
Many pat ien t s w ith carot id ar ter y sten osis are asym ptom at ic,
an d are id en t ified by screen ing st u d ies or t h e p resen ce of a ca-
rot id br u it , w h ich can be au scu lt ated by p lacin g t h e bell of a
steth oscop e over th e lateral n eck bet w een th e angle of th e m an -
dible an d th e su p erior m argin of th e thyroid car t ilage. Th e pres-
en ce of a cer vical br u it d oes n ot con fir m carot id sten osis, as
venous hum s, cardiac m urm urs, thoracic bruits, thyrom egaly, and
u pper ext rem it y arterioven ous fist u las can all m im ic a carot id
bruit .8 Also, th e absen ce of a cer vical bru it does n ot ru le ou t ca-
rot id disease. In tot al, 20 to 35% of p at ien ts w ith h igh -grade ex-
Fig. 20.1 Digital subtraction angiography clearly dem onstrating a left in-
t racran ial carot id ar ter y sten osis h ave n o au scu ltable br u it .9 ternal carotid artery plaque appropriate for surgery with at tendant vascular
In sym ptom at ic patien ts the history often proves the m ost use- and bony anatomy.
fu l. Eviden ce of t ran sien t or en du ring cerebral isch em ic even t s,
su ch as h em ip aresis or h em isen sor y deficits, altered speech , or
vision loss (am au rosis fuga x), can be t h e earliest in d icat ion of h as lim itat ion s relat ive to DSA w h en th e carot id ar ter y h as any
an act ive carot id p laqu e. Th ese sym ptom s com m on ly invoke degree of calcificat ion n ear th e area of in terest . Averaging ar t i-
a st roke w orku p . Lip id p an els, hyp ercoagu labilit y laborator ies, facts n ear th e calcium –plaque or calciu m –blood in terface often
m agn et ic reson an ce im aging (MRI) of th e brain an d carot id im - h ide th e t ru e lum in al diam eter of th e ar ter y. Carot id ar ter y u l-
aging (u lt rasou n d , CTA, MRA, d igit al su bt ract ion angiograp hy t rasou n d h as been a w idely u sed screen ing tool for carot id steno-
[DSA]) are em p loyed to con firm th at an isch em ic even t h as oc- sis. It is, h ow ever, debatable w hether carotid arter y ult rasoun d is
curred an d to localize its source. su fficien t to est ablish th e diagn osis of h igh -grade sten osis in th e
Im aging m odalit ies h ave lim itat ion s. In our experien ce, ult ra- absen ce of con firm ator y tests, such as CTA or DSA. Ult rasou n d
soun d is h igh ly operator d ep en den t an d can be quite in accu rate, evalu at ion s ten d to be h igh ly depen den t on th e skill of th e tech -
MRI is su bst an dard at discern ing bet w een p reocclu sive sten osis n ician ; it h as been suggested th at carot id ult rasoun d sh ould be
in t h e d ist al ICA an d tot al occlu sion , an d CTA u n d erest im ates u sed on ly as a stan d-alon e diagn ost ic tool if it s posit ive predic-
t h e degree of sten osis if th e carot id bifu rcat ion is calcified. DSA t ive valu e for > 50% sten osis exceeds 90% after in st it ut ion al veri-
offers t h e m ost tested an d accu rate assessm en t of t h e carot id ficat ion .10 Carot id u lt rasoun d is a safe an d relat ively in expen sive
bifurcat ion , an d it presen ts th e cerebrovascular surgeon w ith m odalit y for screen ing pat ien t s w ith possible carot id sten osis.
vit al an atom ic referen ces relat ive to th e plaqu e, su ch as th e angle We do not recom m end proceeding to surgery based on ultrasound
of th e m an dible, adjacen t cer vical ver tebrae, an d n earby ECA data alon e.
bran ch es (Fig. 20.1). CTA can p rovide m u ch of th e sam e in form a- Regardless of w h eth er or n ot th e pat ien t presen ts as asym p -
t ion as DSA, in clu ding rem arkable th ree-d im en sion al (3D) an a- tom at ic or suffering from an isch em ic n eurologic even t , a th or-
tom ic details, w ith out the delay or risks of arterial cath eterization ough h istor y is essen t ial. Th e h istor y sh ould iden t ify details of
(Fig. 20.2). How ever, as above, t h e au t h ors h ave n oted t h at CTA t ran sien t or perm an en t focal visual ch anges, langu age difficult y,

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254 III Ischemic Stroke and Vascular Insufficiency

Fig. 20.2 Computed tomography angiography showing


a 3D visualization of a surgical right internal carotid artery
stenosis in relation to the m andible and hyoid.

facial paresis, dysarthria, num bness, or w eakness. These cues can ad m ission to t h e h osp it al an d conversion to h ep ar in w h ile t h eir
h elp lateralize isch em ic inju ries. W h en th ose isch em ic even ts lie INR n or m alizes. A CEA can be safely p er for m ed on a h ep ar in
ipsilateral to im aging-verified carotid stenosis, there is greater ur- drip , an d several ser ies h ave n oted on ly sligh t in creases in p ost -
gency for surgical inter vention. The risk of stroke in untreated ca- op erat ive h em atom as in pat ien t s on h eparin drip s (0.7%).18
rotid artery stenosis for sym ptom atic and asym ptom atic patients
differs m arkedly (26% an d 6.2%, respect ively, over 3 years).11,12
Th e in it ial su rgical evalu at ion sh ou ld also determ in e th e p res-
en ce or absen ce of con cu rren t disease elsew h ere in th e cardio-
vascu lar t ree. Pat ien ts sh ould be coun seled to cease sm oking,
■ Trials and Treatment Modalities
con t rol th eir blood pressu re (< 140/90 m m Hg), m et icu lou sly t i- Our curren t recom m en dat ion s regarding th erapy for carot id ar-
t rate th eir glu cose (if th e p at ien t is diabet ic), an d bring th eir tot al ter y sten osis h ave evolved over th at past 40 years. Early st udies
ch olesterol to h igh -den sit y lip op rotein rat io to < 4, if possible.13 h ad suggested th at m ed ical m an agem en t w it h blood p ressu re
Regardless of w h eth er or n ot a p at ien t w ith carot id ar ter y sten o- con t rol an d an t ip latelet agen t s su rp assed su rgical in ter ven t ion .19
sis fin ally requ ires n eu rosu rgical t reat m en t , th e risk of fu t u re Grat ifying an d un im peach able results from recen t m ult icen ter
m yocardial infarctions, strokes, or peripheral vascular syndrom es t rials, h ow ever, h ave est ablish ed th e su periorit y of su rgical th er-
over 5 years exceeds 20%. Pat ien ts sh ould be coun seled to seek apy over m edical m an agem en t in specific cases of both asym p -
fu t u re cardiovascu lar m on itoring an d care from th eir prim ar y tom at ic an d sym ptom at ic carot id sten osis.12,20,21 Th e NASCET
care physician .13,14 data in dicated th at CEA ben efited all sym ptom at ic pat ien t s w ith
Fin ally, all pat ien ts p resen t ing w ith carot id ar ter y sten osis lesion s cau sing m ore th an a 70% redu ct ion in lum in al diam eter
sh ou ld be p laced on aspirin . Th ere exist s class I eviden ce th at an d for specific su bgrou ps of sym ptom at ic pat ient s w ith m ore
perioperat ive asp irin (81 to 325 m g) redu ces th e risk of st roke th an 50% sten osis. Likew ise, ACAS in dicated th at asym ptom at ic
postop erat ively for u p to 6 m on th s.15,16 We recom m en d th at pat ien ts w ith m ore than 60% stenosis h ad a bet ter outcom e w ith
other antiplatelet agents, such as clopidogrel and ticlopidine, be CEA than w ith m edical m anagem ent. Thanks largely to these well-
stopp ed prior to p erform ing a CEA (ideally 7 to 10 days in ad- designed, ran dom ized con t rolled t rials (RCTs), CEA h as becom e
van ce). An t iplatelet agen t s h ave been associated w ith an elevated th e th erapy of ch oice for select p at ien t s w ith > 50%carot id ar ter y
rate of in t raoperat ive h em orrh age. It can be argu ed t h at clop ido- stenosis. But perioperative m orbidit y and m ortalit y m ust be lim -
grel does add an ext ra layer of p rotect ion again st a cerebrovascu- ited to < 3% an d p at ien t life expectan cy sh ould be > 5 years.22
lar accident perioperatively, but this gain m ust be weighed against Th e NASCET an d ACAS t rials are n ow t w o decades old. Many
its det rim en t al effects on h em ostasis.17 Warfarin sh ould alw ays physician s h ave begu n aggressively t reat ing carot id ar ter y sten o-
be h alted in advan ce of a CEA. Pat ien t s t aking w ar far in n eed sis w ith n ovel an t iplatelet agen ts an d st at in s. Prelim in ar y dat a

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20 Carotid Endarterectomy 255

review ing bot h sym ptom at ic an d asym ptom at ic p at ien t s w it h versus Sten t ing Trial (CREST). Th is m ult icen ter RCT at tem pted to
in t ra- an d ext racran ial carot id ar ter y sten osis h ave suggested address th e n um erous failings of past RCTs com paring CEA an d
th at com bin at ion s of th ese n ew m edicat ion s m ay p rovide st roke CAS. A total of 2,502 pat ien t s (1,262 CEA an d 1,240 CAS) w ere
redu ct ion ben efit s approach ing th at of CEA. A st udy evaluat ing en rolled in CREST. Th e st u dy in clu ded both asym ptom at ic an d
sym ptom at ic carot id ar ter y sten osis, in clu ding in t racran ial dis- sym ptom at ic p at ien ts w ith eith er ≥ 60% or ≥ 50% sten osis of th e
ease, and com bination aspirin/clopidogrel noted a significant re- carot id ar ter y by angiograp hy (oth er radiograp h ic st u dies w ere
du ct ion in t ran scran ial u lt rasou n d-dem on st rated m icroem boli perm it ted for diagn osis, th ough w ith h igh er cu toffs). All su r-
(relat ive risk reduct ion [RRR] 42.4%, p = 0.025). Such radiograph ic geon s an d in ter ven t ion ists h ad to be cer t ified for th eir procedure
redu ct ion s w ou ld presu m ably, but n ot n ecessarily, correlate w ith to par t icipate in th e t rial. For pat ien ts un dergoing CAS, an em -
a redu ced likelih ood of fu t u re isch em ia.23 Test ing th e clin ical va- bolic protect ion device h ad to be em ployed w h erever feasible.
lid it y of clop idogrel adm in ist rat ion for th e p reven t ion of cerebral The st udy’s prim ar y end points w ere periprocedural stroke, m yo-
isch em ic even t s, several RCTs h ave been design ed an d executed cardial in farct ion , an d death , as w ell as any st roke or m yocardial
to com pare aspirin , clopidogrel, an d com bin at ion aspirin /clopi- in farct ion ip silateral to th e diseased arter y up to 4 years after
dogrel t reated p at ien t s. Th e Eu rop ean St roke Preven t ion St u dy-2 t reat m en t .
(ESPS-2) an d th e European /Aust ralasian St roke Preven t ion in Re- In th e fin al an alysis, th e auth ors of CREST n oted n o differen ce
versible Isch aem ia Trial (ESPRIT) both n oted a sign ifican t relat ive in prim ar y en d poin t s bet w een t h e t w o t reat m en t arm s (7.2%
risk redu ct ion for st roke w h en p at ien t s received both asp irin an d CAS vs 6.8% CEA; 95% con fiden ce in ter val [CI], 0.81–1.51; p =
clop idogrel com pared w ith eith er m edicat ion alon e (aspirin an d 0.51). Th ough th ese results h ave been cited as eviden ce of equ i-
clop idogrel: 37%; aspirin : 18%; p = 0.039).24,25 Oth er RCTs h ave poise bet w een CAS an d CEA, th e dat a u n derp in n ing th ese broad
n oted sign ifican tly m ore h em orrh agic com plicat ion s w ith com - con clu sion s lead u s to a d ifferen t in ter p ret at ion . Lookin g at
bin at ion an t iplatelet agen t th erapy w ith out a relat ive reduct ion st roke an d m yocardial in farct ion in depen den tly, th e t w o largest
in cerebral isch em ia.26,27 en d poin t s com p rising CREST’s gen eral en d p oin t , th e st u dy
Th e dat a for stat in u se in carot id sten osis p at ien ts are sligh tly fou n d a sign ifican tly elevated periprocedu ral st roke rate am ong
m ore im pressive. Subgroup an alysis of 1,007 pat ien t s w ith ca- CAS pat ien t s (4.1% CAS vs 2.3%; p = 0.012), on par w ith previous
rotid stenosis and no at tendant coronary disease in the Stroke Pre- st u dies, an d an elevated m yocardial in farct ion rate am ong CEA
vent ion by Aggressive Reduct ion of Ch olesterol Levels (SPARCL) pat ien ts (1.1 CAS vs 2.3%; p = 0.032). Looking at qualit y-of-life
t rial dem on st rated an im p ressive 33% redu ct ion in st roke risk m easu res record ed over t h e st u dy’s 4-year follow -u p (Med ical
am ong th ose pat ien t s ran dom ized to 80 m g of ator vastat in ver- Ou tcom es St u dy 36-Item Sh or t -For m Healt h Su r vey [SF-36]),
sus placebo (p = 0.006).28 Additionally, laborator y data evaluating m yocardial in farct ion s h ad n o dem on st rable effect on pat ien ts’
en doth elial injur y, n it ric-oxide m ediated vasodilat ion , an d p late- qu alit y of life, w h ereas periprocedu ral st rokes did . Fu r th er, th e
let aggregat ion in hydroxyl-m ethyl-glu tar yl–coen zym e A (HMG- rate of m ajor ipsilateral st rokes am ong CAS-t reated pat ien t s, de-
CoA) redu ctase t reated pat ien ts h ave sh ow n th at stat in s in h ibit spite th e use of an em bolic protect ion device, ran n early double
th e early st ages of en doth elial inju r y associated w ith carot id ar- th at of th e CEA pat ien ts (15.2% CAS vs 8.0% CEA).40
ter y ath erosclerot ic ch anges.29 Looking at th e sp ecific CREST data in th is w ay, rath er th an ju st
Alth ough it is un likely th at m edical m an agem en t w ill sup - th e broad su m m ar y st atem en t s, th is latest large t rial leads th e
plan t CEA as th e lead in ter ven t ion for carot id sten osis, th ere h as authors to sim ilar conclusions as w ere seen in previous RCTs com -
been a sh ift in m an agem en t pat tern s for carot id ar ter y sten osis paring CAS and CEA. CREST reaffirm s that CAS bears a m aterially
w ith t h e adven t of carot id ar ter y sten t ing (CAS). Th ere h ave an d st at ist ically h igh er risk of periprocedural st roke com pared
been , to date, 11 RCTs com p ar ing CEA an d CAS.30–37 Th e resu lt s w ith CEA an d th at th is risk is n ot sign ifican tly blu n ted by th e use
h ave failed to validate CAS as a n on in fer ior t reat m en t for ca- of m odern distal em bolic protect ion devices. Th e failure of distal
rot id ar ter y sten osis. More to t h e p oin t , m any st u d ies h ave protect ion devices to lim it CAS-related st roke likely derives from
fou n d CAS to bear a m uch h igh er risk of procedure-related st roke aortic arch disease concurrent w ith carotid stenosis. Such plaques
t h an carot id su rger y. Most n ot able am on g t h ese st u d ies, t h e m ust be t raversed by en dovascu lar in ter ven t ion ist s long before
Leicester an d WALLSTENT t r ials, fou n d a 2- to 4-fold in crease in th ese em bolic protect ion devices can even be deployed.
p er ip roced u re, ip silateral cerebral isch em ic even t s am ong CAS Th u s, alth ough CAS represen t s a rem arkable tech n ological
pat ien ts com p ared w ith CEA p at ien t s.36,38 Th ese resu lt s h ave leap for w ard in th e t reat m en t of carot id ar ter y sten osis an d n o
been cause for m u ch con cern , but suppor ters of CAS h ave re- doubt h as its place in th e m an agem en t of th is disease, th e evi-
spon ded on ly by cit ing a n ascen t un derst an ding of CAS at th e den ce to date con t in u es to favor op en su rgical in ter ven t ion . Nu -
t im e of th ese t rials, an d a lack of exp erien ce w ith th e procedu re m erou s RCTs h ave dem on st rated con sisten t an d reprodu cible
du ring th ese early st u dies. Non eth eless, of th e m ore recen t RCTs, eviden ce for a low er 30-day st roke an d death rate for pat ien ts
th e Sten t-Protected Angiop last y versu s Carot id En dar terectom y ran dom ized to CEA. With out n ovel dat a to suppor t CAS, curren t
(SPACE) t r ial m ild ly favors CEA, t h e En dar terectom y Versu s eviden ce-based m edicin e con t in ues to at test to th e superiorit y
Sten t ing in Pat ien ts w ith Sym ptom at ic Severe Carot id Sten osis of CEA over CAS for the m anagem ent of carotid stenosis patients.
(EVA-3S) defin it ively favors CEA, an d th e interim an alysis dat a
from th e In tern at ion al Carot id Sten t ing St udy-2 (ICSS-2) sh ow
rem arkable su p er ior it y of CEA over p rotected CAS for st roke
preven t ion .32,39
Th e latest an d m ost com preh en sive RCT invest igat ing th e ef-
■ Surgical Techniques and Planning
ficacy an d safet y of CAS an d CEA in th e t reat m en t of carot id ar- On ce a pat ien t h as been recom m en ded for an d coun seled on sur-
ter y sten osis is th e Carot id Revascularizat ion En dar terectom y ger y an d h as con sen ted to it , th e surgeon m ust begin preparing

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256 III Ischemic Stroke and Vascular Insufficiency

th e p at ien t an d th e su rgical team for th e p rocedu re. All p at ien t s Sustained dim inution of the N20-P25 SSEP w ave am plitude > 50%
sh ou ld be st ar ted an d m ain tain ed on aspirin prior to surger y. As h as also been w ell correlated w ith postoperat ive n eurologic defi-
n oted earlier in th is ch apter, if h eparin izat ion w as previously in i- cit .45 As su ch , th e com bin ed u se of th ese t w o in ter ven t ion s offer
t iated, it m ay be con t in u ed th rough th e p rocedu re. Blood p res- th e cerebrovascu lar su rgeon a reliable set of in dicators for re-
su re m edicat ion s sh ou ld be con t in u ed as w ell. Th e pat ien t sh ou ld du ced region al CBF an d at ten dan t im m in en t cerebral isch em ia.
ideally rem ain n orm oten sive leading u p to an d th rough out th e Our detect ion rate is h igh er w ith EEG, but w e add SSEP as a safet y
perioperat ive period.41 m easure for th ose occasion s w h en th e depth of an esth esia, or
Though good argum ents can be m ade w ithin the cerebrovascu- changes after recent stroke, prevents an accurate EEG assessm ent.
lar com m unit y for either local/regional or general anesthesia, the Once th e an esth esiologist h as com pleted th e in t u bat ion , ve-
auth ors recom m en d gen eral an esth esia for CEA. On e advan tage n ous access h as been ach ieved, an ar terial lin e placed, an d fol-
of gen eral an esth esia is th e con t rolled environ m en t it facilitates. low ing th e applicat ion of n eu rom on itoring leads, w e posit ion
Ad dit ion ally, m ost com m on ly em ployed in h alat ion al an esth et ic th e pat ien t su pin e on th e op erat ing room t able w ith t h e arm s
agen t s an d in t raven ou s barbit u rates sign ifican tly redu ce th e ce- t ucked securely at th e side. A sm all bum p of tow els or oth er soft
rebral m etabolic rate of oxygen consum ption,42 giving a presum p - cush ion sh ould be placed bet w een th e sh oulder blades to allow
t ive protect ive effect in in st an ces of dim in ish ed cerebral blood t h e clavicle an d sh ou ld ers to fall aw ay from t h e op erat ive field .
flow. In experien ced h an ds, local an esth esia is safe an d effica- A gentle in clin e in th e back of th e t able an d low ering of th e h ead
cious, bu t for u s it h as several disadvan tages, including th e risk of of t h e bed facilit ates su fficien t exten sion of t h e p at ien t ’s n eck
con t am in at ion , pat ien t m ovem en t du ring th e procedu re, p oten - to p rovide am ple operat ive sp ace. Add it ion ally, th e h ead of th e
tial conversion to general anesthesia under less th an ideal circum - pat ien t is cocked gen tly to th e sid e con t ralateral to th e carot id
st an ces, an d th e in creased p sych ological st ress on th e pat ien t of lesion. Th e su rgeon , based on p reoperat ive im aging, m ay gauge
rem ain ing aw ake. On e review com p aring local an d gen eral an es- th e degree of rot at ion . In m ost p at ien t s, th e ICA lies directly p os-
th esia tech n iqu es for CEA h as fou n d lit tle clin ical ben efit to th e terior to th e ECA, an d rotat ion of th e n eck con t ralaterally sw ings
use of local an esth esia. Alth ough local an esth esia h as been as- t h e ICA laterally in to view , facilit at in g t h e d issect ion . A sm all
sociated w ith a decreased in ciden ce of elect roen cep h alograp h ic p iece of t ap e m ay be p laced on t h e ip silateral p in n a to ret ract
ch anges an d in t raoperat ive sh u n t ing, w e h ave n ot fou n d a reason an d fold it aw ay from th e operat ive field. Th is provides th e su r-
to ch ange our p ract ice based on com pelling differen ces in st roke geon th e opt ion of exten ding th e in cision tow ard th e ret roaural
rate, com p licat ion s, length of stay, or overall outcom e.43 region in th e case of h igh carot id bifurcat ion s.
In addit ion to deciding on th e an esth esia tech n ique, th e sur- Th e su rgical in cision is m ade along th e m edial border of th e
geon m u st also decide prior to th e procedure w h eth er or n ot to stern ocleidom astoid m u scle, w ith it s m idp oin t rough ly over th e
utilize intraoperative m onitoring techniques during carotid artery carot id bu lb. To locate t h e bu lb, on e n eed on ly gen t ly p alp ate
cross-clam ping. A w ide variet y of m odalit ies h ave been devel- t h e length of th e carot id an d correlate w ith angiograp h ic im ag-
oped over th e last several decades aim ed at lim it ing th e in ci- ing. Th e au th ors advise cur ving t h e su perior m argin of th e in ci-
den ce of p ostop erat ive n eu rologic deficit . Th e au th ors u se th ree sion posteriorly in to th e ret roau ral region in expectat ion th at th e
m eth ods in ever y case: in t raoperat ive carot id Doppler for vascu- lesion m ay term in ate h igh er in th e ICA th an expected, n ecessi-
lar assessm en t , an d con curren t elect roen ceph alograp hy (EEG) tat ing greater exp osu re.
an d som atosen sor y evoked poten t ial (SSEP) m on itoring of cere- With th e in cision m ap ped, a st an dard sterile prep an d drape
bral elect rical act ivit y. Su p por t for th e u se of th e lat ter t w o m o- sh ould be perform ed over th e op erat ive field an d sterile op era-
dalit ies, in par t icu lar, h as been ver y convin cing. EEG h as been t ive equ ipm en t organ ized (Fig. 20.3). Ap prop riate perioperat ive
w ell correlated w ith cerebral blood flow (CBF). Trojaborg an d an t ibiot ics sh ould be adm in istered during th e skin prep. If de-
Boysen 44 clearly dem onstrated in 1973 the profound effect dim in- sired, a long-act ing local an esth et ic m ay be in filt rated along th e
ish ed CBF h as u pon EEG t racings, w ith w aves grow ing m arkedly proposed skin in cision to m in im ize operat ive an d p ostop erat ive
dim in ish ed to flat ten ed as CBF drop ped below 22 m L/100 g/m in . pain (w e do n ot do th is, h ow ever).

Fig. 20.3 The Loftus-Scanlan carotid instrument set used


by the authors, with a variet y of clamps and forceps for
varied vascular anatom ies.

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20 Carotid Endarterectomy 257

Th e dissect ion begin s by in cising th e skin an d carr ying th e


dissect ion th rough th e su bcu tan eou s fat u sing Bovie elect rocau -
ter y. Up on reach ing t h e p lat ysm a, th e m u scle is elevated w it h
Debakey forcep s an d d ivid ed w it h elect rocau ter y. Con t rolled
m et iculou s dissect ion w ill lim it bleeding (w e h ave n ever given a
blood t ran sfusion for a CEA). Bipolar cauter y can elim in ate any
su perficial bleeding n ot con t rolled by th e Bovie. After th e p la-
t ysm a h as been op en ed , w e d evelop t h e exp osu re w it h blu n t
skin h ooks in stead of fixed m et al ret ractors. Blu n t skin h ooks
en able low -profile ret ract ion w h ile m in im izing inju r y to th e re-
curren t lar yngeal n er ve.
Ben eat h th e plat ysm a, w e iden t ify th e m edial border of th e
stern ocleidom astoid m u scle an d follow th e m edial edge to th e
IJV. A robu st layer of fat m ay overlie t h e jugu lar vein in som e
obese pat ien ts. Avoid th e tem ptat ion to w ork m edial to th e fat
in to an in correct dissect ion plan e. Add it ion ally, if th e stern oclei-
dom astoid m u scle is ret racted laterally du ring th is dissect ion by
deep en ing th e ret ractors u n dern eath its m edial edge, take cau -
Fig. 20.4 The hypoglossal nerve can be seen here isolated next to an en-
t ion n ot to inju re th e sp in al accessor y n er ve th at lies ben eath th e t wined external carotid artery branch.
m uscle.
After th e jugu lar vein h as been exposed, w e dissect along it s
m ed ial edge an d d ivid e several m in or bran ch es crossin g from
t h e IJV to th e m edial m argin of th e field. Th e largest of th ese sw inging m edially over the ICA. We dissect th e hypoglossal ner ve
crossing vein s, th e com m on facial vein , cu stom arily lies over top free along it s lateral bord er, isolate it w ith a vessel loop , an d gen -
of th e carot id bifu rcat ion or n ear to it . As a m at ter of n ecessit y, tly ret ract it , avoiding cau ter y or ret ract ion dam age to th e n er ve
th e vein m ay n eed to be dou bly ligated an d divided . On ce th is is later in th e su rger y (Fig. 20.4). For t r uly h igh exposures, th e pos-
done, m edial an d deep to th e vein , w e id en t ify th e carot id ar ter y. terior belly of th e digast ric m uscle can be in cised an d par t ially
Usually, th e CCA is exp osed first . Prior to any fu r th er dissect ion t ran sected to exp ose m ore ICA. On ce w e are com for t able th at w e
an d m an ipu lat ion of th e vessel, th e an esth esiologist is asked to h ave sufficien t distal ICA con t rol, w e test fit th e Fogar t y an d bull-
ad m in ister 5,000 U of in t raven ou s h ep ar in . Th e carot id ar ter y dog clam p s an d u se a sterile m arking p en to draw th e ar teriot-
bran ch es sh ou ld be exposed proxim ally un t il th e CCA h as been om y lin e from t h e CCA, across t h e bu lb, an d in to t h e ICA. Th e
cleared far en ough below th e bu lb to allow com for table ap plica- SSEP an d EEG tech n ician s are n ot ified t h at cross-clam p in g is
t ion of a soft-sh oe Fogar t y clam p . Distally, th e exposu re sh ou ld im m in en t , an d th e an esth esiologist is asked to in duce burst sup -
proceed so th at th e ICA is freed w ell beyon d th e p laqu e to en able pression . On ce m on itoring baselin es h ave been verified, w e first
applicat ion of a bulldog clam p. Th e ECA sh ould be exposed dis- occlude th e ICA (w e do it first to protect th e brain from em boli)
tally beyon d th e superior thyroid ar ter y to en able applicat ion of w ith a sm all, low -force, bulldog clam p. Th is is follow ed by occlu-
a bulldog clam p. Each vessel sh ould be isolated w ith in a 0-0 silk sion of th e CCA w ith th e Fogar t y, an d th e ECA w ith a larger bu ll-
su t u re to m ain tain con st an t con t rol of th e carot id ar ter y an d its dog clam p. We open th e m arked ar teriotom y first w ith a No. 15
bran ch es. Th e CCA silk is p u lled t h rough a Ru m m el tou r n iqu et kn ife blade follow ed by a Pot ts scissors. If th ere is a m on itoring
to en able rapid proxim al con t rol. Th e superior thyroid ar ter y su- ch ange, w e p ass a sh u n t (Loft u s sh u n t , In tegra Neurocare, Pleas-
t ure is doubly w rapped aroun d th e arter y (a Pot ts t ie) to keep it an t Prairie, NJ) first dow n th e CCA an d secure it w ith th e Ru m m el
occluded an d lim it unw an ted back bleeding during th e ar teriot- tou rn iqu et . After bleeding th e sh un t free of air an d debris, it can
om y. Du r ing exp osu re of t h e carot id bu lb, t h e p at ien t m ay ex- be gen tly passed up th e ICA an d secured above th e lesion w ith a
p erien ce episodes of bradycardia an d hypoten sion . If vit al sign s pin ch clam p (Figs. 20.5 an d 20.6). We auscultate sh un t flow by
becom e un stable, th e carot id sin u s is injected w ith 2 to 3 m L of applying th e h an dh eld Doppler to th e sh un t t ubing. We expect
1% Xylocain e to d isr u pt t h e baroreceptor reflex d r iving t h ese t h at m on itor in g w ill ret u r n at least p ar t ially to baselin e on ce
vital sign ch anges. flow is establish ed. If it does n ot , th e sh un t m ust be assessed for
Th e d ist al exp osu re of t h e ICA is t h e m ost d ifficu lt p or t ion failu re, an d possibly replaced. Th is is ext rem ely rare.
of th e d issect ion . Th e carot id sh eat h can be t acked u p w ith 4-0 Plaqu e rem oval is facilitated by gen tly grip ping th e vessel w all
Nu rolon su t u res (Medlin e In du st ries, Mu n delein , IL). Th is m a- w ith fin e vascular forceps an d developing a plan e bet w een it an d
n euver elevates th e carot id ar ter y in th e field. It is cr ucial to as- th e p laqu e w ith a Freer elevator. We begin on th e lateral w all an d
certain the distal exten t of th e ICA plaque before cross-clam ping. m ove to th e back w all of th e vessel, th en repeat th e process on
Th is can be p erform ed by au scu lt at ion of th e ICA w ith a Dop p ler th e m edial side u n t il th e p laqu e h as been circu m feren t ially re-
u lt rasou n d (h igh er p itch beyon d t h e p laqu e), visu al cu es su ch m oved. At th e proxim al CCA, th e plaqu e m ay be sh arply cu t aw ay
as ar terial w all discolorat ion (yellow t urn s pin k as th e plaque w ith fin e-poin t Met zen baum scissors, w ith th e in ten t to leave as
en ds), an d d igit al (gen tle) p alpat ion for th e en d of th e stony h ard sm ooth a tran sit ion zon e as possible. The ICA end point is crit ical,
plaqu e. For h igh ICA exposu re, th e dissect ion advan ces along th e an d th e tech n iqu e m ust be m et iculous. If at all possible, th e ICA
m edial border of th e jugular vein . Th e hypoglossal n er ve passes at tach m en t of th e p laqu e sh ou ld be feath ered off th e in t im a,
dow n in th e groove bet w een th e ICA an d th e jugu lar vein before t h ough sh ar p d issect ion m ay be n ecessar y to avoid d issect in g

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258 III Ischemic Stroke and Vascular Insufficiency

Fig. 20.5 A Loftus-t ype shunt situated within the internal carotid artery
and com m on carotid artery (CCA). The black m arking indicates the m id-
point of the tubing, providing a useful indicator to the surgeon as to Fig. 20.6 The Loftus-Scanlan pinch clamps with tailored tips to neatly fit
whether or not the tubing m igrates cephalad after the initial insertion. around the internal carotid artery to secure the indwelling shunt tubing.

th e p laque beyon d th e view of th e exposed ICA ar teriotom y (Fig. Now th at th e plaqu e is resected, th e w alls are in sp ected for
20.7). It is a m istake to ch ase an ICA p laqu e by tearing or pulling any sm all loose fragm en t s st ill st uck along th e lum en . A ring-t ip
it dow n from beyon d th e field of view. Loose w isps of plaqu e th at forceps is ideal for th is task. By gen tly st roking th e in tim a w ith
can n ot be feath ered clean ly at th e ICA in t im a–p laqu e in terface a pean ut sponge, th e surgeon can elevate an d reveal suspect re-
sh ou ld be tacked dow n u sing a dou ble arm ed 6-0 Prolen e su t u re gion s an d pick th em clean . Den sely adh eren t fragm en ts offer n o
w ith th e kn ot t ied outsid e of th e ar ter y w all. th reat of em bolu s an d th erefore n eed n ot be rem oved. Occasion -
On ce th e ICA an d CCA p laqu e at t ach m en t s are free, a sm all ally, w e en cou n ter cases w h ere after rem oval of large ch un ks of
m osquito h em ost at is used to dissect th e plaque free at th e ECA circum feren t ial fragm en t s th ere are th in spots in th e w all th at
orifice. Th e clam p can th en be u sed to reach in to th e ECA an d n eed to be rein forced. Rein forcem en t is accom plish ed w ith an
pull th e plaqu e free. Ver y rarely, sign ifican t fragm en ts of plaqu e en circling ban d of patch m aterial (Fig. 20.9).
m ay rem ain adh eren t w ith in th e ECA. If th ese fragm en t s are n ot On ce th e lum en h as been sat isfactorily clean ed of fragm en ts
ad d ressed p r ior to closu re, t h ey can engen d er p er iop erat ive an d th e loose bit s of in t im a are tacked dow n , th e ar teriotom y
th rom bus form at ion . We th erefore h ave a low th resh old to ex- can be closed. Prim ar y repair can be m icroscope assisted or loupe
ten d th e ar teriotom y in to th e ECA to en sure adequate resect ion m agn ified. It is our pract ice to perform a loupe-m agn ified patch
of th e plaqu e (Fig. 20.8). graft repair in ever y case. We use a Hem ash ield patch cu t to fit

Fig. 20.8 A full closure of the internal carotid artery with patch graft and
Fig. 20.7 Here the plaque has been cleaned from the artery. Note the external carotid artery (ECA) without a patch graft. In this case the ECA was
cleanly cut transition zone at the internal carotid artery, which does not opened to clear residual plaque, and then closed prim arily with a separate
require tacking sutures in this case. suture line.

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20 Carotid Endarterectomy 259

Fig. 20.9 An additional Hem ashield wrap is dem onstrated here to rein-
force a thinned patch of internal carotid artery wall. The ends of the wrap Fig. 20.10 A Hem ashield patch has been cut to fit and tacked proxim ally
are tacked together with 6-0 Prolene suture. and distally with t wo 6-0 Prolene sutures.

over th e arteriotom y defect in an elongated diam on d sh ape. Th e bleed each bran ch of th e carot id t ree to clear air an d debris an d
patch is t acked dow n at th e dist al an d proxim al en ds w ith dou ble verify paten cy. With th at com p lete, a h eparin ized salin e syringe
ar m ed 6-0 Prolen e su t u res (Fig. 20.10). Un d er 3.5× lou p e m ag- is gen tly in serted in to th e arter y lum en via th e rem ain ing lateral
n ificat ion , th e m edial w all of th e su t u re lin e is th en closed in a su t u re lin e defect . Th e assistan t fills th e lu m en w ith h eparin ized
run n ing, n on locking fash ion . W h en th e run n ing st itch reach es salin e w h ile th e su rgeon t ies th e rem ain ing t w o loose 6-0 Prolen e
th e CCA an ch oring st itch , it is t ied to on e of th e free en ds of th at en ds togeth er.
6-0 Prolen e’s t w o arm s. After th e m edial w all h as been repaired, On ce th e fin al sut ure h as been t ied an d secured, th e carot id
th e lateral w all is closed w ith an oth er r u n n ing, n on locking st itch . clam p s can th en be released, begin n ing w ith th e ECA, th en th e
Un like th e m edial w all, th is is don e w ith t w o 6-0 Prolen e st itch es CCA, an d fin ally (after 10 secon ds) th e ICA (Fig. 20.11). Th is al-
th at m eet an d t ie togeth er n ear th e bifu rcat ion . On e arm of th e low s any air or debris to flush in con sequ en t ially up th e ECA, n ot
ICA an ch oring Prolen e is used to close th e lateral w all from th e to th e brain . Th ere are usu ally som e sm all bleeding poin ts along
ICA tow ard th e CCA. An arm of th e CCA an ch oring st itch is th en th e su t u re lin e th at stop w ith digit al pressu re. How ever, w e h ave
u sed to close th e lateral w all from th e CCA tow ard th e ICA. a low th resh old to repair anyth ing but th e m ost m in or leak w ith
If a sh un t h ad been used, it is n ow clam ped w ith t w o sm all a single 6-0 Prolen e st itch to en sure h em ostasis. Th e sen ior au-
h em ostats th rough th e fin al sut ure lin e defect , cu t in t w o, an d th or h as n ever n eeded to ret u rn a pat ien t to su rger y to evacu ate
th en rem oved in p ieces w h ile th e clam p s are reap plied. After a w oun d h em atom a follow ing CEA, presum ably as a result of th is
th is, but before th ese t w o st itch es on th e lateral w all of th e ar te- d iligen t p olicy. We also like to cover t h e ar ter ial rep air w it h a
riotom y h ave been t ied togeth er, th e su rgeon m u st sequ en t ially p iece of Su rgicel (Fig. 20.12). Th is can h elp to stop any su bt le

Fig. 20.12 Surgicel has been laid over top of the arteriotomy graft repair.
Note that with a m eticulous surgical dissection there is lit tle need for ad-
Fig. 20.11 A complete arteriotomy repair. ditional hem ostatic agents or m aneuvers.

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260 III Ischemic Stroke and Vascular Insufficiency

w eeping from along th e arteriotom y repair. Before fin al w oun d of th e carot id ar ter y an d to obtain a n ew baselin e. Follow -up
closu re each bran ch of th e carot id ar ter y is au scu lt ated w ith a rou t in es var y an d on e recom m en ded regim en is to follow th e
Dop p ler u lt rasoun d to con firm flow an d paten cy. Again , if th ere pat ien t w ith ult rasoun ds at 1 an d 6 m on th s an d th en an n u ally.
is any dou bt as to th e qu alit y of th e repair, w e recom m en d re-
explorat ion an d rep air of th e lu m en .
With con fiden ce th at th e arter y h as been successfully open ed
an d repaired, th e surgeon can th en at ten d to h em ostasis an d ■ Patient Outcomes
w ou n d closu re. After t h e blu n t fish h ooks h ave been rem oved
As m en t ion ed earlier in th is ch apter, CEA ou tcom es com pare
an d t h e t ack-u p carot id sh eat h su t u res cu t free, w h at lit t le
ver y favorably w ith altern at ive t reat m en t m odalit ies. Tot al peri-
bleed ing th ere m ay be rarely requ ires m ore th an bipolar elect ro-
procedu ral m orbidit y an d m or t alit y ten ds to ru n bet w een 2%
cau ter y, gen t le p ressu re, an d p at ien ce to stop . We rou t in ely
an d 7% in m ost st udies, w ith m ost com plicat ion s being m in or
t u n n el a sm all drain u n d er th e p lat ysm a an d leave it w ith in th e
an d reversible.30–38,46,47 Our st roke rate is w ell less th an 2%, in clu-
carot id sh eath . Th e sh eat h it self sh ou ld be loosely reap proxi-
sive of all categories in clu ding h igh -risk pat ien ts. Most p at ien t s
m ated w ith in terru pted 2-0 Vicr yl su t u res. Th e plat ysm a an d
can leave t h e h osp it al w it h in 2 to 4 days an d h ave been sh ow n
skin are likew ise closed in dividually, com m on ly w ith 2-0 Vicr yl
to ret urn to preprocedural fun ct ion al stat us w ith in 1 m on th of
inver ted in terr u pted su t u res an d 4-0 Mon ocr yl su bcut icular su -
surger y, w ith ver y h igh levels of pat ien t sat isfact ion .48
t ures, respect ively.
Th e pat ien t sh ou ld be m on itored in th e recover y u n it an d
t ran sferred to th e in ten sive care u n it postop erat ively. If th e p a-
t ien t is n oted to h ave a d eclin e p ostop erat ively, on e sh ou ld p ro -
ceed w ith im m ed iate vascu lar im agin g; if th is opt ion is n ot
■ Conclusion
available, th e pat ien t sh ould be ret u rn ed to th e op erat ing room Carotid en darterectom y rem ains the treatm ent m odalit y of ch oice
for explorat ion an d p ossible th rom bectom y. All pat ien ts sh ou ld for carot id sten osis. With con t in ued im provem en t s in m edical
continue taking aspirin for the rem ainder of their lives. We recom - th erapy an d en d ovascu lar sten t ing, it is p ossible t h at th ese alter-
m en d vascular im aging in all pat ien ts to docum en t th e paten cy n at ives m ay be u sed for select cases of carot id sten osis.

References
1. Kistler JP, Ropper AH, Heros RC. Th erapy of isch em ic cerebral vascular dis- dom ised con t rolled t rial. ASA an d Carot id En dar terectom y (ACE) Trial Col-
ease du e to ath eroth rom bosis (1). N Engl J Med 1984;311:27–34 laborators. Lan cet 1999;353:2179–2184
2. Fish er CM. Obser vat ion s of th e fun du s oculi in t ran sien t m on ocular blin d- 16. Lin dblad B, Persson NH, Takolan der R, Bergqvist D. Does low -dose acet yl-
n ess. Neurology 1959;9:333–347 salicylic acid prevent stroke after carotid surger y? A double-blind, placebo-
3. Hedera P, Bujdáková J, Traubn er P. Effect of collateral flow pat tern s on con t rolled ran dom ized t rial. St roke 1993;24:1125–1128
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4. Kleiser B, Widder B. Course of carot id ar ter y occlusion s w ith im paired bin ed w ith aspirin in reducing cerebral em boli in pat ien t s u ndergoing
cerebrovascular react ivit y. St roke 1992;23:171–174 carot id en darterectom y. Circulat ion 2004;109:1476–1481
5. Loft us CM. Carot id En darerectom y: Prin ciples an d Tech n ique, 2n d ed. 18. Poisik A, Heyer EJ, Solom on RA, et al. Safet y an d efficacy of fixed-dose
New York: In form a Health care; 2006 h eparin in carot id en dar terectom y. Neurosurger y 1999;45:434–441, dis-
6. Hat sukam i TS, Ferguson MS, Beach KW, et al. Carot id plaque m orph ology cu ssion 441–442
an d clin ical even t s. St roke 1997;28:95–100 19. Fields WS, Maslen ikov V, Meyer JS, Hass W K, Rem ington RD, Macdon ald
7. Carr S, Farb A, Pearce W H, Virm an i R, Yao JS. Ath erosclerot ic plaque rup - M. Join t st u dy of ext racran ial ar terial occlu sion . V. Progress repor t of
t u re in sym ptom at ic carot id ar ter y stenosis. J Vasc Surg 1996;23:755– progn osis follow ing surger y or n on surgical t reat m ent for t ran sien t cere-
765, discussion 765–766 bral ischem ic at t acks an d cer vical carot id ar ter y lesion s. JAMA 1970;211:
8. Sauvé JS, Laupacis A, Ostbye T, Feagan B, Sacket t DL. Th e rat ion al clin ical 1993–2003
exam in at ion . Does th is p at ien t h ave a clin ically im p or t an t carot id bru it? 20. MRC Eu rop ean Carot id Su rger y Trial: in terim resu lt s for sym ptom at ic pa-
JAMA 1993;270:2843–2845 t ien t s w ith severe (70–99%) or w ith m ild (0–29%) carot id sten osis. Euro-
9. Davies KN, Hum ph rey PR. Do carot id br uit s predict disease of th e in tern al pean Carot id Su rger y Trialist s’ Collaborat ive Group. Lan cet 1991;337:
carot id ar teries? Postgrad Med J 1994;70:433–435 1235–1243
10. Ballot t a E, Da Giau G, Abbr u zzese E, et al. Carot id en dar terectom y w ith out 21. Nor th Am erican Sym ptom at ic Carot id En dar terectom y Trial Collabora-
angiography: can clin ical evaluat ion an d duplex ult rason ograph ic scan - tors. Ben eficial effect of carot id en dar terectom y in sym ptom at ic p a-
n ing alon e replace t radit ion al ar teriography for carot id surger y w orku p? t ien t s w ith h igh -grade carotid sten osis. N Engl J Med 1991;325:445–453
A prospect ive st udy. Surger y 1999;126:20–27 22. Loftus CM. Carotid endarterectom y: the asym ptom atic carotid. In: Batjer HH,
11. National Center for Health Statistics. Annual sum m ar y of births, m arriages, ed. Cerebrovascular Disease. New York: Lippincot t-Raven; 1996:406–420
divorces, an d death s: Un ited St ates. Mon Vit al St at Rep 1994;42:13 23. Wong KS, Ch en C, Fu J, et al; CLAIR st udy invest igators. Clopidogrel plus
12. Endarterectom y for asym ptom atic carotid artery stenosis. Executive Com - asp irin versu s asp irin alon e for redu cing em bolisat ion in pat ien t s w ith
m it tee for th e Asym ptom at ic Carot id Ath erosclerosis St udy. JAMA 1995; acu te sym ptom at ic cerebral or carot id arter y sten osis (CLAIR st u dy): a
273:1421–1428 ran dom ised, open -label, blin ded-en dpoin t t rial. Lan cet Neu rol 2010;9:
13. An derson KM, Odell PM, Wilson PW, Kan n el W B. Cardiovascular disease 489–497
risk profiles. Am Heart J 1991;121(1 Pt 2):293–298 24. Dien er HC, Cun h a L, Forbes C, Siven ius J, Sm et s P, Low en thal A. European
14. Anderson KM, Wilson PW, Odell PM, Kannel W B. An updated coronar y risk St roke Preven t ion St udy. 2. Dipyridam ole an d acet ylsalicylic acid in th e
profile. A statem ent for health professionals. Circulat ion 1991;83:356–362 secon dar y preven t ion of st roke. J Neurol Sci 1996;143:1–13
15. Taylor DW, Barn et t HJ, Hayn es RB, et al. Low -d ose an d h igh -d ose ace- 25. Halkes PH, van Gijn J, Kap pelle LJ, Kou dst aal PJ, Algra A; ESPRIT St u dy
t ylsalicylic acid for p at ien t s u n d ergoing carot id en dar terectom y: a ran - Grou p. Aspirin plus dipyridam ole versus aspirin alon e after cerebral isch -

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20 Carotid Endarterectomy 261

aem ia of ar ter ial or igin (ESPRIT): ran d om ised con t rolled t r ial. Lan cet 37. Gu r m HS, Yadav JS, Fayad P, et al; SAPPHIRE Invest igators. Long-ter m
2006;367:1665–1673 result s of carot id sten t ing versus en dar terectom y in h igh -risk pat ien t s.
26. Dien er HC, Bogousslavsky J, Brass LM, et al; MATCH invest igators. Aspirin N Engl J Med 2008;358:1572–1579
an d clop idogrel com p ared w ith clop idogrel alon e after recen t isch aem ic 38. Brooks W H, McClure RR, Jones MR, Colem an TC, Breath it t L. Carot id an -
st roke or t ran sien t isch aem ic at t ack in h igh -risk p at ien t s (MATCH): ran - gioplast y an d sten t ing versus carot id en dar terectom y: ran dom ized t rial
dom ised, dou ble-blin d, p lacebo-con t rolled t rial. Lan cet 2004;364:331– in a com m un it y h ospit al. J Am Coll Cardiol 2001;38:1589–1595
337 39. Ederle J, Dobson J, Feath erston e RL, et al; In tern at ional Carot id Sten t ing
27. Bh at t DL, Fox KA, Hacke W, et al; CHARISMA Invest igators. Clopidogrel St u dy invest igators. Carot id ar ter y sten t ing com pared w ith en dar terec-
an d asp irin versu s asp irin alon e for th e p reven t ion of ath eroth rom bot ic tom y in p at ien t s w it h sym ptom at ic carot id sten osis (In ter n at ion al Ca-
even t s. N Engl J Med 2006;354:1706–1717 rot id Sten t ing St u dy): an in ter im an alysis of a ran d om ised con t rolled
28. Sillesen H, Am aren co P, Hen n erici MG, et al; St roke Preven t ion by Aggres- t rial. Lan cet 2010;375:985–997
sive Redu ct ion in Ch olesterol Levels Invest igators. Ator vast at in redu ces 40. Man tese VA, Tim aran CH, Ch iu D, Begg RJ, Brot t TG; CREST Invest iga-
th e risk of cardiovascular even t s in pat ien t s w ith carot id ath erosclerosis: tors. Th e Carot id Revascularizat ion En dar terectom y versus Sten t ing Trial
a secon dar y an alysis of th e St roke Preven t ion by Aggressive Redu ct ion in (CREST): sten t ing versu s carot id en dar terectom y for carot id disease.
Ch olesterol Levels (SPARCL) t rial. St roke 2008;39:3297–3302 St roke 2010;41(10, Su p p l):S31–S34
29. Tu ñ ón J, Mar t ín -Ven t u ra JL, Blan co- Colio LM, Egido J. Mech an ism s of 41. Steiger HJ, Sch äffler L, Boll J, Liech t i S. Result s of m icrosu rgical carot id
act ion of st at in s in st roke. Expert Opin Th er Target s 2007;11:273–278 en dar terectom y. A prospect ive st udy w ith t ran scran ial Doppler an d EEG
30. Halliday A, Man sfield A, Marro J, et al; MRC Asym ptom at ic Carot id Su r- m onitoring, and elective shunting. Acta Neurochir (Wien) 1989;100:31–38
ger y Trial (ACST) Collaborat ive Group. Preven t ion of disabling an d fat al 42. Gelb AW. An esth et ic con siderat ion s for carot id en dar terectom y. In t An es-
st rokes by su ccessfu l carot id en dar terectom y in p at ien t s w ith ou t recen t th esiol Clin 1984;22:153–164
n eu rological sym ptom s: ran dom ised con t rolled t rial. Lan cet 2004;363: 43. Loft us CM. An esth esia for carot id en darterectom y: gen eral vs. local? In :
1491–1502 Bederson JB, Tuh rim S, eds. Treat m ent of Carot id Disease: A Pract it ioner’s
31. Halliday AW, Th om as D, Man sfield A; Steering Com m it tee. Th e Asym p - Man u al. Park Ridge, IL: AANS Pu blicat ion s; 1998:181–190
tom at ic Carot id Su rger y Trial (ACST). Rat ion ale an d design . Eu r J Vasc Su rg 44. Trojaborg W, Boysen G. Relat ion bet w een EEG, region al cerebral blood
1994;8:703–710 flow an d in tern al carot id ar ter y pressure du ring carot id en dar terectom y.
32. Mas JL, Ch atellier G, Beyssen B, et al; EVA-3S Invest igators. En darterec- Elect roen cep h alogr Clin Neu rop hysiol 1973;34:61–69
tom y versu s sten t ing in p at ien t s w ith sym ptom at ic severe carot id sten o- 45. Loft us CM. Historical perspect ive on carot id recon st r uct ion . In : Loft us
sis. N Engl J Med 2006;355:1660–1671 CM, ed. Carot id En darterectom y: Prin ciples an d Tech n ique. New York: In -
33. Ringleb PA, Allen berg J, Br ü ckm an n H, et al; SPACE Collaborat ive Group. form a Health care; 2007:25
30 day resu lt s from t h e SPACE t r ial of sten t -p rotected angiop last y ver- 46. Alber t s MJ, McCan n R, Sm ith TP. A ran dom ized t rial of carot id stent ing
su s carot id en dar terectom y in sym ptom at ic p at ien t s: a ran dom ised n on - versu s en dar terectom y in p at ien t s w ith sym ptom at ic carot id sten osis:
in feriorit y t rial. Lan cet 2006;368:1239–1247 st u dy design . J Neu rovasc Dis 1997;2:228–234
34. En d ovascu lar versu s su rgical t reat m en t in p at ien t s w it h carot id sten o- 47. Yadav JS, W h oley MH, Kun t z RE, et al; Sten t ing an d Angioplast y w ith Pro-
sis in th e Carot id an d Ver tebral Ar ter y Tran slu m in al Angioplast y St u dy tect ion in Pat ien t s at High Risk for En dar terectom y Invest igators. Pro-
(CAVATAS): a ran dom ised t rial. Lan cet 2001;357:1729–1737 tected carotid-artery sten ting versus en darterectom y in high-risk patients.
35. CARESS Steering Com m it tee. Carot id revascularizat ion u sing en darterec- N Engl J Med 2004;351:1493–1501
tom y or sten t ing system s (CARESS): ph ase I clin ical t rial. J En dovasc Th er 48. Bar n ason S, Rasm u ssen D. Pat ien t ou tcom es beyon d h osp it alizat ion :
2003;10:1021–1030 carot id endarterectom y surgical pat ien t ou tcom es after a rapid recover y
36. Naylor AR, Bolia A, Abbot t RJ, et al. Ran dom ized st udy of carot id angio- program . Clin Nu rse Spec 2002;16:100–105
plast y an d sten t ing versus carot id en darterectom y: a stopped t rial. J Vasc
Surg 1998;28:326–334

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21 Endovascular Treatment of
Carotid Stenosis
Travis M. Dum ont, Kenneth V. Snyder, Adnan H. Siddiqui, L. Nelson Hopk ins, and Elad I. Levy

Carot id revascu larizat ion h as been sh ow n to red u ce st roke risk w ell est ablish ed.8,9 More recen tly, local an d system ic in flam m a-
for p at ien t s w it h sym ptom at ic 1,2 an d asym ptom at ic 3,4 carot id tion have been associated w ith carot id ath erosclerosis.10,11 Inflam -
ar ter y sten osis. En dovascular t reat m en t of carot id sten osis rep - m at ion w ith in a carot id plaqu e m ay propagate p laqu e form at ion ,
resen t s an opt ion for revascu larizat ion , w ith a risk profile sim ilar in t raplaqu e h em orrh age, or r upt u re.12–14
to th at of en dar terectom y.5 Th e n at u ral h istor y of carot id at h erosclerosis is d ep en d en t
on sym ptom atology an d plaqu e m orph ology an d m ay be altered
w ith m edical10,15,16 or surgical1–4 m anagem ent. Plaque character-
ist ics such as ulcerat ion or h em orrh age m ay be associated w ith
■ Anatomic Considerations a h igh er risk of isch em ic even ts.17–19
For asym ptom at ic p at ien t s, p rogression of carot id sten osis
Th e paired in tern al carot id ar teries (ICAs) provide th e m ajorit y severit y h as been dem on st rated in in dividual pat ien t s, w ith a
of blood flow to th e cerebral h em isp h eres.6 An un derst an ding of correlat ion w ith an in creased risk of ip silateral in farct ion .20 A
th eir origin from th e aor t ic arch is im por t an t in en dovascu lar sm aller su bset of asym ptom at ic p at ien t s m ay h ave plaqu e reso-
t reat m en t of sten osis of th ese ar teries (Fig. 21.1). Th e com m on lu t ion w ith lifest yle ch anges an d t reat m en t of t ypical con com i-
carot id ar ter y (CCA) bifu rcates at th e level of th e m id-to-u p per tan t s of carot id sten osis. Of in terest , th e in ciden ce of ipsilateral
cer vical region in m ost pat ien t s an d represen ts th e m ost com - st roke in pat ien t s w ith carot id sten osis w h o h ave n ot u n dergon e
m on site for sten osis.6 carot id revascu larizat ion ap p ears to be on th e declin e w ith con -
Alth ough variat ion s in arch an atom y exist , th e m ost com m on tem p orar y m ed ical m an agem en t . Th e in cid en ce of ip silateral
con figu rat ion of th e origin of t h e righ t CCA is as an exten sion of isch em ic st roke in th e m edical arm of th e Asym ptom at ic Carot id
t h e brach iocep h alic (or in n om in ate) ar ter y.6 Th is vessel is t h e Ath erosclerosis St udy (ACAS) (ran dom izat ion bet w een 1987 and
m ost proxim al large bran ch off th e aort ic arch . Th e left CCA is th e 1993, w h en m edical m an agem en t con sisted of aspirin ) w as 2.2%
secon d large bran ch off th e aort ic arch . Th e m ost com m on varia- an n ually.3 Th e in ciden ce of ipsilateral isch em ic st roke in th e
t ion , seen in 25%of angiogram s, is a bovin e con figu rat ion , w ith a m edical arm of th e Asym ptom at ic Carot id Surger y Trial (ACST)
sh ared ost ium of th e brach iocep h alic ar ter y an d left CCA.6 (ran dom izat ion bet w een 1993 an d 2003, w h en m edical th erapy
Variat ion s of aor t ic arch an atom y m ay ch ange w ith age an d progressed to include angioten sin -converting-en zym e inh ibitors,
develop m en t of vascu lar disease. In an t icipat ion of carot id sten t- angioten sin receptor blockers, an d stat in s) w as 1.7% an n u ally.4
ing procedures, th e sites of th e ost ia of th e brach ioceph alic ar- With m odern m edical m an agem en t , prospect ive st udies h ave
ter y an d left CCA relat ive to th e aor t ic apex sh ould be st u died sh ow n an in ciden ce of ip silateral st roke in pat ien t s w ith asym p -
w ith preoperat ive com puted tom ography or m agn et ic reson an ce tom at ic carot id sten osis of less th an 1% an n u ally.15,16
im aging.7 A t akeoff of th e in n om in ate ar ter y or left CCA p roxim al Th e in ciden ce of recu rren t ipsilateral isch em ic st roke for p a-
to t h e aor t ic arch ap ex (t yp e II or III arch an atom y) m ay resu lt t ients w ith sym ptom at ic carot id sten osis is 17 to 25% over 2 to 3
in m ore difficult y for th e en dovascular n eurosu rgeon because years on th e basis of dat a from large t rials p erform ed in th e years
access to th e carot id ar ter y th rough a stan dard fem oral ar ter y bet w een 1981 an d 1994 w h en m edical m an agem en t con sisted
approach requ ires an ext ra ben d of th e cath eters an d oth er de- prim arily of asp irin .1,21,22 Du e to th e dram at ic risk redu ct ion of
vices, com p ared w ith access to an arterial ost iu m at th e apex of st roke dem on st rated by th e Nor th Am erican Sym ptom at ic Ca-
th e aor t ic arch (t yp e I arch an atom y) (Fig. 21.1). rot id En darterectom y Trial (NASCET) 1 an d th e Eu ropean Carot id
Su rger y Trial (ECST),2 carot id revascu larizat ion n ow rep resen t s
th e st an dard of care. Th u s, t h e n at u ral h istor y of recu rren t , ip si-
lateral isch em ic st roke in p at ien ts w ith sym ptom at ic carot id ar-
■ Pathophysiology and Natural History ter y sten osis w ith m odern m edical th erapy is u n clear.

of Disease
Carot id ar ter y sten osis is a n arrow ing of t h e n at ive ar ter y lu m en
w ith form ation of soft (atherom atous) and hard (sclerosis) plaque
deposition . Th is condition m ay be clin ically silent, or lead to n eu-
■ Clinical Presentation
rologic sym ptom s due to flow lim itat ion or em bolism of plaque Carot id ar ter y sten osis m ay or m ay n ot lead to sym ptom s. Pa-
m aterial. The precise understanding of plaque deposition rem ains t ien ts presen t ing w ith an terior circu lat ion isch em ic sym ptom s
u n clear; h ow ever, associat ion s w ith hyp erch olesterolem ia, hy- in th e absen ce of a cardioem bolic sou rce sh ould be evalu ated for
per ten sion , diabetes m ellit u s, obesit y, an d cigaret te sm oking are carot id sten osis w it h a n on invasive im agin g m od alit y, su ch as

262

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21 Endovascular Treatment of Carotid Stenosis 263

Fig. 21.1 Anatomy of the standard aortic arch. Standard arch, t ype I: The innom inate artery proxim al to the aortic arch apex. Standard arch, t ype III:
innom inate artery, left com m on carotid artery (CCA), and left subclavian The origins of the innom inate artery and left CCA are proxim al to the aortic
arteries originate in a proxim al-to-distal order with all artery origins at or arch apex. Access to the carotid arteries is m ore difficult with a t ype II or III
distal to the apex of the aortic arch. Standard arch, t ype II: The origin of the arch.

Dop p ler u lt rason ography or com p u ted tom ograp h ic or m agn et ic ectom y at greater risk for recurren t lar yngeal n er ve inju r y.23–25
reson an ce angiography. If any im aging m odalit y is suggest ive of Addit ion ally, p at ien ts w ith previou s irradiat ion or exten sive sur-
carot id sten osis in excess of 50% of th e n orm al lu m in al d iam eter ger y to th e n eck can be expected to h ave h igh er perioperat ive
by NASCET criteria,1 revascu larizat ion sh ou ld be con sidered. risk w ith en dar terectom y d u e to difficu lt y w ith n eck dissect ion .
Asym ptom at ic carot id sten osis is frequ en t ly d iagn osed on Pat ien ts w ith ipsilateral p roxim al or in t racran ial sten osis in ad-
a rou t in e p hysical exam in at ion w it h au scu lt at ion of a carot id dit ion to carot id bifu rcat ion sten osis are best t reated w ith en do-
br u it . Screen ing u lt rason ograp hy is frequ en t ly offered to p a- vascu lar tech n iques, because all lesion s m ay be t reated as n eces-
t ien ts w ith t ypical con com itan t s or a fam ily h istor y of carot id sar y an d w ith a low er risk of in t raoperat ive even t s.25,26 Medical
ath erosclerot ic disease. Pat ien ts m ay also be iden t ified w ith ca- risk factors, su ch as recen t or act ive m yocardial in farct ion an d
rot id sten osis as an in ciden t al fin ding on im aging perform ed for evolving n eurologic sym ptom s, in crease perioperat ive risk for
an un related reason . carot id en dar terectom y bu t n ot carot id sten t ing.23,27,28

■ Treatment Modalities ■ Devices


On ce th e determ in at ion h as been m ade to perform a carot id re- On ce a pat ien t is deem ed a can didate for carot id ar ter y sten t ing,
vascu lar izat ion p roced u re, an in divid u al’s vascu lar an atom y, prep arat ion for en d ovascu lar access is of u t m ost im por t an ce for
in clu ding th e aor t ic arch , sh ou ld be st udied to determ in e th e a successful result . For each case, sten ts an d em bolic protect ion
presen ce of an atom ic variat ion s th at w ou ld m ake en dovascu lar d evices m u st be selected , as w ell as ot h er d evices su ch as an -
t reat m en t m ore favorable or less favorable. Alth ough m ost ca- gioplast y balloon s. An cillar y devices th at are also useful in clude
rot id lesion s are accessible for en darterectom y th rough a stan - in t ravascu lar ult rasou n d (IVUS) an d aspirat ion cath eters. Angio-
dard an terior access ap proach , cer t ain an atom ic feat u res place a graph ic an atom y is of prin cipal im por t an ce in device select ion .
pat ien t at u n n ecessar y risk w ith en dar terectom y. For exam ple, Carefu l select ion of devices is im p or t an t for su ccessfu l an d safe
a h igh bifurcat ion (above th e secon d cer vical ver tebra [C2]) or placem en t of a carot id ar ter y sten t an d is det ailed in th e discu s-
excessive exten sion of th e p laqu e dist al to th e carot id bifu rcat ion sion below. For all devices u sed du ring carot id ar ter y sten t ing, a
places th e p at ien t u n dergoing an en dar terectom y at greater risk rapid-exch ange deliver y system is em ployed, in stead of an over-
for hyp oglossal n er ve inju r y, w h ereas a low bifu rcat ion or ex- th e-w ire design , resu lt ing in a sh or t w orking lu m en facilit at ing
ten sion of th e carot id plaque m ore th an 3 cm proxim al to th e usage of standard w ire lengths, thereby decreasing tim e by avoid-
carot id bifu rcat ion p laces th e p at ien t u n d ergoin g an en dar ter- ing prot racted w ire an d cath eter exch anges.29

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264 III Ischemic Stroke and Vascular Insufficiency

Embolic Protection Devices of stenosis before its deploym ent, at w hich point the plaque could
be disrupted an d em bolize w ith in th e ICA prior to establish ing
Em bolic p rotect ion decreases th e risk of em bolic st roke du ring em bolic protection. Moreover, em bolic filters var y w idely in term s
carot id sten t in g 30,31 an d h as becom e t h e st an dard of care for of allow ed par t iculate sizes; th erefore, par t iculates sm aller th an
sten t in g p roced u res.32 Opt ion s in clu d e d ist al p rotect ion w it h 40 µm m ay n ot be capt u red by even th e m ost select ive filter.33
in t ravascu lar filter devices an d proxim al protect ion w ith flow For additional em bolic protection w ith a distal protection device,
st asis or flow reversal (Table 21.1). Both proxim al an d distal em - th e gu ide cath eter h u b m ay be op en ed for back-bleeding du ring
bolic p rotect ion d evices are d esign ed to lim it th e em bolism of each step w h ere th e lesion is crossed. Par t iculate m at ter m ay
p laqu e d ebr is liberated d u r in g p lacem en t of t h e sten t an d p re- th en be diver ted th rough th e gu ide cath eter an d (safely) ou t of
or postangioplast y. Th e t w o d evices m ay also be u sed in tan dem th e body, rath er th an dist ally in to th e in t racran ial circu lat ion .
for du al protect ion (“belt an d suspen ders”). Proxim al em bolic p rotect ion devices are specialized 9F gu ide
Dist al em bolic p rotect ion devices are in t ralu m in al filters th at cath eters design ed w ith t w o com p lian t balloon s, of w h ich on e is
are deployed in th e ICA dist al to th e area of sten osis. Due to ease in flated in th e proxim al CCA an d th e oth er in th e extern al carot id
of use (com pared w ith proxim al em bolic protect ion devices) an d ar ter y (ECA). Each balloon is in flated prior to th e t im e of crossing
reliable redu ct ion of perioperat ive st roke in several t rials an d th e sten ot ic carot id plaqu e segm en t w ith a w ire an d deliver y
regist ries, dist al em bolic protect ion devices are used for m ost of th e sten t across th e lesion . With both balloon s in flated, flow
carot id sten t ing procedu res.5 All devices can be easily delivered in to th e ICA p ast th e lesion is stopp ed or reversed w ith act ive or
th rough 6-Fren ch (F) gu ide cath eters, th ereby avoiding larger passive aspirat ion th rough th e lu m en of th e gu ide cath eter. De-
system s w ith h igh er risks of vascu lar inju r y an d bleeding com - bris created from sten t ing is th en w ash ed ou t th rough th e guide
plicat ion s. Th ere is n o su sp en sion of flow du ring th e p rocedu re cath eter, rath er th an em bolizing to th e brain . Th e m ajor draw -
as blood cells an d plasm a easily t raverse th e filter pores; h en ce, back to proxim al protect ion devices is a th eoret ical lack of blood
th ere is n o in terr u pt ion in cerebral p erfu sion , w h ich is a m ajor flow to th e ipsilateral in t racran ial carot id circulat ion due to flow
draw back of p roxim al devices. Th e p rim ar y lim it at ion of dist al st asis or reversal w h ile t h e balloon s are in flated . How ever, in
protect ion devices is th at th e filter m u st be brough t past th e area p ract ice, occlu sion t im e is t yp ically sh or t com p ared to clam p

Table 21.1 Summary of Stent and Embolic Protection Devices Used in Carotid Stenting Studies

Embolic
Stent Description Protection Device Description Study

Xact (Abbot t Vascular) Closed cell, tapered, Neuroshield, Distal protection, SECURITY, EXACT
small free-cell area Emboshield over-the-wire
(both Abbot t Vascular)
ACCULINK (Guidant) Open cell, tapered, ACCUNET (Guidant) Distal protection, fixed wire ARCHER, CAPTURE,
small free-cell area CAPTURE2
Wallstent (Boston Closed cell, cylindrical, FilterWire EX/EZ (Boston Distal protection, fixed wire BEACH
Scientific) sm all free-cell area Scientific)
Exponent (Medtronic) Open cell, cylindrical, Guardwire (Medtronic) Distal protection, distal MAVErIC I and II
larger free-cell area balloon, and aspiration
NexStent (Boston Open cell, cylindrical, FilterWire EX/ EZ (Boston Distal protection, fixed wire CABERNET
Scientific) larger free-cell area Scientific)
Protégé (ev3) Open cell, stepped, Spider (ev3) Distal protection, CREATE
larger free-cell area over-the-wire
Precise (Cordis) Open cell, cylindrical, AngioGuard (Cordis) Distal protection, fixed wire CASES-PMS, SAPPHIRE
small free-cell area Worldwide
Any FDA approved NA Gore flow reversal system Proximal protection, EMPiRE
(W.L. Gore & Associates) balloon with flow reversal
Any FDA approved NA FiberNet (Lumen Distal protection, fixed EPIC
Biomedical) wire, smaller pore,
aspiration with retrieval
Any FDA approved NA Mo.Ma (Invatec) Proxim al protection, PRIAMUS, ARMOUR
balloon with aspiration
Abbreviations: ARCHeR, ACCULINK for Revascularization of Carotids in High-Risk patients; ARMOUR, ProximAl PRotection with the Mo.Ma Device DUring CaRotid
Stenting; BEACH, Boston Scientific EPI: A Carotid Stenting Trial for High-Risk Surgical Patient s; CABERNET, Carotid Artery Revascularization using the Boston Scientific
FilterWire EX/ EZ; CAPTURE, Carotid Acculink/Accunet Post Approval Trial to Uncover Unanticipated or Rare Events; CASES-PMS, Carotid Artery Stenting with Emboli
protection Surveillance–Post Marketing Study; CREATE, Carotid Revascularization with ev3 Arterial Technology Evolution; EMPiRE, Embolic Protection with Reverse
Flow; EPIC, Evaluating the Use of the FiberNet Em bolic Protection System in Carotid Artery Stenting; EXACT, Emboshield and Xact Post Approval Carotid Stent Trial;
FDA, Food and Drug Adm inistration; MAVErIC, Medtronic AVE Self-Expanding Carotid Stent System in the Treatm ent of Carotid Stenosis; NA, not applicable; PRIAMUS,
Proxim al Flow Blockage Cerebral Protection during Carotid Stenting; SAPPHIRE, Stenting and Angioplast y with Protection in Patients at High Risk for Endarterectomy;
SECURITY, Registry Study to Evaluate the Neuroshield Bare Wire Cerebral Protection System and X-Act Stent in Patients at High Risk for Carotid Endarterectomy.

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21 Endovascular Treatment of Carotid Stenosis 265

t im e for en dar terectom y, an d in toleran ce to flow arrest or rever- par t iculates bet ween the stent and the vessel wall, thereby lim iting
sal is u n com m on . Th is is con sisten t w ith a rare n eed for select ive the risk of th rom boem bolism .41 A stent of sufficien t length should
sh u n t ing du ring en dar terectom y or rates of in toleran ce as re- be selected to cover the entire lesion and bridge the ICA to the CCA.
por ted d u ring th e Em bolic Protect ion w ith Reverse Flow (EM-
PiRE) 34 an d Proxim Al PRotection w ith the Mo.Ma Device DUring
Angioplasty Balloon
CaRotid Stent ing (ARMOUR)35 p roxim al p rotect ion t r ials. Th is is
d u e to th e robu st collaterals th at exist in th e vast m ajorit y of Alth ough presten t angioplast y is perform ed rout in ely at som e
pat ien ts at th e level of th e circle of Willis. cen ters, it is th e auth ors’ preferen ce to perform presten t angio-
Determ in at ion of th e t ype of em bolic protect ion d evice is plast y on ly in th ose few cases w h ere th e sten t m ay n ot be easily
based prim arily on an atom ic con siderat ion s.36,37 For exam p le, or safely p assed w ith out an angioplast y.42 Poststen t ing angio-
a distal em bolic protect ion device m ay n ot be opt im al in cases plast y is perform ed in m ost cases for p roper resolu t ion of th e
w h ere a crit ical sten osis or labyrin th in e n arrow ing does n ot site of greatest sten osis. For post sten t angioplast y, an angioplast y
allow easy passage of th e m icrow ire th rough th e lesion w ith out balloon cath eter is selected to be sligh tly un dersized to th e di-
disru pt ion of th e p laqu e, or a tor t u ou s or diseased vessel distal to am eter of th e n on diseased ICA. For procedural sim plicit y (i.e., to
th e sten osis w h ere th e filter is n ot easily p assed w ith ou t poten - lim it device exch anges) an d to lim it th rom boem bolic poten t ial,
t ial t rau m a to th e vessel w all. In su ch cases, p roxim al p rotect ion on e angioplast y after placem en t of th e sten t is preferred. Angio-
is preferred. Conversely, dist al p rotect ion is p referred for cases in plast y balloon s are available in a w ide range of diam eters an d
w h ich : a proxim al balloon m ay n ot be passed in to th e ECA due to lengths to con form to the vessel diam eter and stent used. As w ith
sten osis w ith in t h e CCA, th e degree of sten osis is n ot crit ical, th e oth er devices, rapid-exch ange m ech an ism s are preferred . Th e
con t ralateral carot id ar ter y is occlu ded or circle of Willis is in - con cern w ith angioplast y is th at it is con sidered th e por t ion of
com plete, or th e p at ien t is asym ptom at ic. Th is last con siderat ion th e p rocedu re w ith th e greatest risk of em bolizat ion becau se it
is st ill som ew h at of a hyp oth esis. Th e assu m pt ion , sup ported by creates plaqu e fract ure/r upt ure an d liberates plaque debris in to
som e dat a, is th at th e efficien cy of em bolic p rotect ion is h igh er th e vessel. Th is is w hy th e au th ors lim it angiop last y to on e even t
w ith proxim al devices. Th is is suppor ted by th e result s of th e after d ep loym en t of t h e sten t , w h ich ser ves to con st rain som e
ARMOUR35 an d EMPiRE34 t rials as com p ared w ith con t igu ous t ri- of t h e p laqu e an d it s at ten dan t d ebr is w it h in t h e vessel w all. In
als u sing dist al em bolic protect ion . Th e con ten t ion th at reversal addit ion , th e m ore aggressive th e angioplast y, th e h igh er th e risk
or arrest of flow is m ore absolute w h ile distal em bolic protect ion of plaque debris release, h en ce th e sligh t u ndersizing of th e an -
is relat ive is th e rat ion ale for u sing proxim al p rotect ion for cases gioplast y balloon to n om in al ICA diam eter. Fin ally, angioplast y
in w h ich th e plaque is su sp ected to be at h igh risk for em boliza- ser ves as t h e st rongest act ivator of t h e vagal resp on se d u r in g
t ion , p ar t icu larly liqu id em boli m aterial, w ith m an ip u lat ion , carot id ar ter y sten t ing. Th e resu lt an t bradycardia—or its m an -
su ch as w h en it’s sym ptom at ic, or th e p at ien t is clin ically asym p - agem en t w ith dopam in ergic agon ist s—m ay act u ally cau se m yo-
tom at ic but n on invasive im aging reveals silen t em boli in th e ip - cardial ischem ia in at-risk pat ients. Th e authors th erefore lim it the
silateral in tracran ial circulat ion , or m agn et ic reson an ce p laqu e aggressiven ess of balloon angiop last y especially in p re–coron ar y
im aging reveals a h em orrh agic p laque, suggest ing in st abilit y. ar ter y bypass surger y pat ien ts an d rout in ely pret reat all pat ien t s
u n dergoing carot id ar ter y sten t ing w ith th e ch olin ergic an t ago-
n ist glycopyrrolate to subver t th e occurren ce of bradycardia w ith
Stent angioplast y.
Several sten t s w ith var ying ch aracterist ics h ave disp layed effi-
cacy in t rials an d regist ries (Table 21.1); h ow ever, a closed-cell
Guide Catheter
stent w ith a free-cell area (the uncovered area bet w een the struts
of th e sten t) th at is sm all is preferred for m ost carot id sten t ing A guide cath eter is selected such th at th e sm allest ar teriotom y
cases.38,39 A closed-cell sten t en ables recapt u re after p ar t ial de- m ay be u sed for safe placem en t of th e sten t . For m ost cases, a 6F
ploym en t in th e even t of m alp osit ion ing an d lim it s th e risk of Cook Sh ut tle long sheath (Cook Medical, Bloom ington, IN) is used
distal em bolic protection devices being capt ured on the free edges as th e gu ide cath eter. Th is cath eter h as sufficien t st iffn ess to be
of th e stent . Th e m ost im por t an t at t ribute of closed-cell sten ts is u sed as a sh eath an d gu ide cath eter, w h ich sim plifies th e proce-
that the free-cell area is m uch sm aller than th at of open -cell coun- du re an d p rovides a st able con du it for carot id sten t ing. With a
terp ar t s an d con st rain s plaqu e an d su bsequen tly it s debris from length of 90 cm an d an in n er w orking d iam eter of 0.087 in ch , all
being released in to th e vessel lu m en . Th is essen t ially ser ves as device cath eters are easily delivered to th e site of carot id sten o-
th e m ost im p or t an t form of post p rocedu re em bolic st roke pro- sis th rough th e Cook Sh u t tle. For sten ts w ith 5F deliver y cath e-
phyla xis as evid en ced by m ost ip silateral st rokes being rep or ted ters (e.g., a 6- or 8-m m Wallsten t [Boston Scien t ific, Nat ick, MA],
post p rocedu re bet w een days 1 an d 30.28,40 How ever, th e draw - w ith a diam eter of 1.67 m m ), a 6F Envoy cath eter (in n er w orking
back of th e closed-cell sten t design is th at these sten t s ten d to be diam eter 0.070 in ch ; Codm an , Rayn h am , MA) m ay be u sed as
in flexible an d do n ot con form w ell to th e vessel w all, result ing in a guide cath eter th rough a 6F fem oral ar ter y sh eath . For pat ien ts
st raigh ten ing of th e vessel in th e sten ted segm en t , an d if th ere is w ith a sm all carot id ar ter y an d lim ited vessel tort u osit y, th e
severe vessel tort uosit y, either a proxim al or distal kin k can result, Envoy cath eter m ay be easily posit ion ed p roxim al to th e area of
w h ich can be flow -lim it ing. In stead, in cases of vessel tor t u osit y sten osis. It is a su fficien t ly st iff cat h eter su ch th at t h e p assage
at th e site of sten osis, an open -cell sten t m ay be p referable to of a sten t on a 5F deliver y cath eter m ay be perform ed w ith out
con form to th e vessel an d avoid th e risk of kin king of th e sten ted th e gu ide cath eter h ern iat ing dow nw ard in to th e aor t ic arch . For
vessel. Sten t s w ith sm all free-cell areas th eoret ically t rap plaqu e cases of proxim al p rotect ion , a 9F Mo.Ma cath eter (for u se w ith

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266 III Ischemic Stroke and Vascular Insufficiency

th e Mo.Ma flow st asis system [Medt ron ic, Min n eapolis, MN]) is sedat ives an d local an esth et ic agen ts. Midazolam an d fen t anyl
em p loyed as th e gu ide cath eter. As th ese cath eters are less rigid are adm in istered, t it rated to th e pat ien t’s com for t , allow ing th e
th an t h e Cook Sh u t t le an d h ave sp ecialized t ip s w it h occlu sive pat ien t to be easily assessed for n eu rologic stat u s th rough ou t th e
balloon s, th ey are best used th rough a sh eath , n ecessit at ing case. Con t in u ou s m on itoring of card iac an d pu lm on ar y vit al
placem en t of a 9F fem oral ar ter y sh eat h (t h e sh eat h n eed s to be sign s is p erform ed . In ad dit ion , con t in u ou s invasive blood p res-
9F for com pat ibilit y w ith th is cath eter.) Th e Mo.Ma cath eter is sure m on itoring is perform ed th rough ou t th e procedu re by con -
exch anged directly in to p osit ion over a w ire already in p lace n ect ing th e ar terial sh eath to a t ran sdu cer. Lidocain e is injected
w ith in the ECA (for sten ot ic lesion s en t irely w ith in th e ICA) or at th e site of ar terial pu n ct u re before p lacem en t of th e fem oral
CCA (for lesion s in th e CCA). ar ter y sh eath .

Organization
■ Preoperative and Postoperative Carot id ar ter y sten t in g n ecessit ates t h e p lacem en t of a m icro -
Medication w ire w it h in t h e ICA, w h ich rep resen t s a p oten t ial sou rce of
th rom bu s form at ion . To lim it th is risk (in add it ion to giving th e
Dual an t iplatelet th erapy w ith aspirin (325 m g daily) an d clopi-
h eparin ), any effor t to st ream lin e th e carot id sten t ing p rocedu re
dogrel (75 m g daily) is ideal for preven t ion of p latelet aggrega-
w ith out put t ing th e pat ien t at risk sh ould be con sidered. To th is
t ion on th e sten t , resu lt ing in th e form at ion of an in t ralu m in al
en d , th e d evices selected for th e procedu re are p rep ared w ith
th rom bus during or after th e sten t ing procedu re. Altern ate an t i-
salin e flu sh according to th e m an u fact u rer’s recom m en dat ion s
platelet m edicat ion s for p at ien t s in toleran t to aspirin or clop ido-
an d organ ized for easy accessibilit y. All cath eters are con n ected
grel are accept able. Th e an t iplatelet regim en is st arted 5 days or
to a con t in uous flush system w ith a bleed-back con t rol valve
longer before th e plan n ed procedu re. Oth er w ise, a loading dose
(COPILOT, [Abbot t Vascular, Abbot t Park, IL] or rot at ing h em o-
of asp ir in (650 m g orally, on e d ose) an d clop idogrel (600 m g
static valve [Merit Medical, South Jordan, UT]). The authors prefer
orally, on e dose) sh ou ld be adm in istered p rior to th e p rocedu re
to place each device in th e order it w ill be used un der separate
to in crease plasm a levels to a n ear-th erapeut ic level, an d daily
tow els laid n eatly at th e en d of th e angiograph table (Fig. 21.2).
dosing con t in u ed as n eeded u n t il th e t im e of th e proced u re. Du al
Th is arrangem en t p rovides th e en dovascu lar n eu rosu rgeon (or
an t iplatelet th erapy is con t in ued for at least 1 m on th (preferably
assist an t) w ith rapid access to th e devices an d lim its th e length
3 m on th s) after placem en t of th e sten t , at w h ich poin t clopido-
of th e procedure, par t icularly redu cing th e durat ion for w h ich
grel is discon t in u ed an d aspirin is con t in u ed in defin itely.
th e dist al em bolic filter is deployed (in cases of d ist al em bolic
protect ion ) or th e d u rat ion for w h ich an terograde flow is h alted
Intraoperative Medication or reversed (during proxim al protect ion ) an d th rom boem bolism
risk is greatest . Preparat ion for com plicat ion s m ay lim it su bse-
Th ere is n o con sen su s on th e opt im al agen t an d dose for an t i- qu en t n eu rologic com p rom ise. Th ese com plicat ion s m ay in clu de
coagulation during neuroendovascular procedures 43 ; how ever, on a variet y of poten t ial problem s, from tem porar y an d m ild (vessel
th e basis of th e cardiac literat ure, a w eigh t-based bolu s of h epa- sp asm ) to p oten t ially life t h reaten in g (vessel d issect ion or p er-
rin aim ed at an act ivated coagu lat ion t im e bet w een 250 an d 300 forat ion , th rom boem bolism , cardiopulm on ar y declin e, or access
secon ds m ay lim it periprocedu ral com p licat ion s 44 (~ 60 un its com p licat ion s). Th e follow ing list su m m arizes t h e m edicat ion s
per kilogram bodyw eigh t is t yp ically a su fficien t dose). Th e ad- an d devices th at sh ould be readily available to th e n euroen do-
m in ist rat ion of h eparin prior to crossing th e lesion m ay lim it vascu lar surgeon during carot id sten t ing procedures in prepara-
th rom bu s form at ion on devices p osit ion ed w ith in th e ICA. t ion for both com m on an d rare com plicat ion s.
Hem odyn am ic in stabilit y is w ell docu m en ted during carot id
ar ter y sten t ing procedures, an d preprocedural adm in ist rat ion of • Protam in e (for reversal of an t icoagu lat ion )
an an t ich olin ergic agen t , such as glycopyrrolate or atropin e, m ay • Ept ifibat ide (for th rom boem bolic com plicat ion s)
red u ce t h e r isk of bradycard ic even t s.45,46 A good p ract ice is to • Tissu e-t ype p lasm in ogen act ivator (t-PA) (for th rom boem bolic
h ave a vasop ressor available in t h e even t of bradycard ia or hy- com p licat ion s)
p oten sion during carot id sten t ing procedures. Due to it s cen t ral • Ep in ep h rin e (for severe allergic react ion s)
in ot rop ic effect s, d opam in e is an excellen t opt ion for th e t reat- • Nit roglycerin (for iat rogen ic vasospasm , angin a)
m en t of in t raprocedu ral hypoten sion or bradycardia. • Verapam il (for iat rogen ic vasospasm )
• At ropin e, glycopyrrolate, dop am in e (for t reat m en t of bradycar-
dia, asystole, hypoten sion )
• Lorazepam an d ph osph enytoin (an t iepilept ic agen ts)
■ Endovascular Technique • Trach eostom y set
• Wall-m oun ted su ct ion
Below th e aut h ors describe th e tech n iqu e for perform ing rou t in e • Em ergen cy resu scitat ion car t , in clu ding a defibrillator
carot id sten t ing at th eir in st it u t ion . • Variet y of m icrocath eters an d w ires
• Detach able or push able coils (for h em orrh agic com plicat ion s)
• Liquid em bolic agents (for hem orrh agic com plications): n-but yl
Anesthesia cyan oacr ylate, Onyx (ev3)
At th e auth ors’ in st it ut ion , carot id arter y sten t ing is t ypically • Mech anical th rom bectom y system (such as Pen um bra, Solitaire,
perform ed in con sciou s p at ien ts after th e adm in ist rat ion of m ild or Trevo)

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21 Endovascular Treatment of Carotid Stenosis 267

Fig. 21.2 A schem atic diagram of the neuroendovascular suite. To stream line the carotid stenting procedure, devices are prepared and stacked at the
end of the table in sterile towels for easy access by the endovascular neurosurgeon or assistant during the procedure. AP, anteroposterior.

• In t racran ial sten t s (for p oten t ial cerebral revascularizat ion ) ar ter y w ith a single-pun ct u re tech n ique. A succession of vessel
• Perip h eral vascu lar sten ts (for any groin access com plicat ion ) dilators are em p loyed to dilate th e ar teriotom y u n t il th e app ro-
p r iately sized sh eath is p laced . After sh eat h p lacem en t , an an -
giogram of th e groin region is recom m en ded to con firm arterial
Sheath Placement access, par t icularly to con firm th e absen ce of a h igh st ick. If th e
St an dard righ t fem oral ar ter y access is su it able for m ost carot id vessel st ick is h igh , th e case sh ou ld be abor ted, th e vessel m an u-
ar ter y sten t ing cases. Th e size of th e sh eath placed depen ds on ally com pressed, an d th e pat ien t resch eduled for th e procedure
th e oth er devices to be u sed, from a 5F sh eath (to be rep laced 2 to 3 days later.
w it h a Cook Sh u t t le) to a 9F sh eat h w it h p roxim al p rotect ion
d evices. Pat ien t s sh ould be assessed preoperat ively for a fem oral Target Vessel Selection and Guide
ar ter y pulse. Fem oral ar ter y an atom y of pat ien t s w ith a h istor y
Catheter Placement
of fem oral ar ter y surger y or sten t placem en t sh ould be assessed
w ith preoperat ive im aging, as conven t ion al fem oral arter y ac- Typ ically, th e m ost tech n ically ch allenging p or t ion of carot id
cess m ay be im possible or ill-advised. sten t ing cases is p lacem en t of th e gu ide cath eter. By com p arison
Prior to ar terial p u n ct u re, flu oroscop ic assessm en t of t h e ar- w ith in t racran ial en dovascular procedu res, during ext racran ial
terial pun ct ure site is recom m en ded to en sure safe placem en t of stenting procedures, guide catheter purchase to a stenotic carot id
th e ar terial sh eath for p ercu tan eou s closu re an d to lim it th e risk ar ter y lesion is lim ited; th us, a st iff gu ide cath eter is required so
of access site h em atom a form at ion an d pseudoan eur ysm devel- t h at t h e cat h eter d oes n ot h er n iate d ow nw ard in to t h e aor t ic
opm en t . A h igh n eedle st ick (above th e inguin al ligam en t) is arch w ith passage of th e sten t in to posit ion . Also, pat ien ts w ith
cau se for con cern becau se it p redisp oses th e pat ien t to a ret ro- ath erosclerot ic carot id ar ter y sten osis are likely to h ave tor t u ou s
peritoneal hem atom a, w h ich , un der the anticoagulation regim en ar terial an atom y due to ch ron ic hyper ten sion an d th e aging pro-
u sed du ring sten t ing, can becom e a life-th reaten ing com plica- cess, m aking passage of th e gu ide cath eter in to th e CCA difficult
t ion . A m icrop u n ct u re n eed le is p laced in to t h e r igh t fem oral w ith out sufficien t suppor t from th e guidew ire. Th us, a relat ively

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268 III Ischemic Stroke and Vascular Insufficiency

st iff gu ide cat h eter m u st be p laced w ith in th e CCA in a lim ited Guide Catheter Placement for a Long 6F Catheter
space w ith out dist urban ce of th e t argeted plaque. Th e tech n ique
Th is tech n iqu e is ideal for p lacem en t of any sten t w ith a dist al
is qu ite differen t for placem en t of differen t gu ide cath eters an d is
em bolic p rotect ion d evice. For t h is tech n iqu e, t h e Cook Sh u t t le
described in th e follow ing su bsect ion s for th ree com m on ly u sed
is an ideal guide cath eter. For placem en t of th e Cook Sh ut tle, an
cath eters.
exch ange w ire is advan ced th rough th e fem oral ar ter y sh eat h
an d placed in th e descen ding aor t a. Un der fluoroscopic visual-
ization, the existing fem oral arter y sheath is th en exchanged over
Guide Catheter Placement w ith a Small 6F Catheter
th e w ire for th e Cook Sh u t tle. Th e Cook Sh u t tle an d dilator are
Th is tech n iqu e p rovides a sim p le opt ion w ith a sm all ar teriot - advanced over the w ire into position in the descending aorta, and
om y for placem en t of a carot id sten t delivered w ith a 5F cath eter th e w ire an d sh eath su bsequ en tly rem oved . Th e Cook Sh u t tle is
(Wallstent, 6- or 8-m m diam eter). A 6F guide catheter (e.g., Envoy) n ow in posit ion for select ion of th e target vessel (Fig. 21.4a). A
is brough t u p th rough a 6F fem oral sh eath over a soft 0.035-in ch VTK cath eter (Vitek, Cook Medical, Bloom ington, IN) m ay be used
guidew ire an d parked w ith in th e descen ding aorta (Fig. 21.3a). for select ion of th e left or righ t ICA, w h ereas an angled Slip cath -
The targeted vessel is cannulated under direct fluoroscopic visual- eter (Cook Medical, Bloom ington , IN) can be u sed for th e righ t
ization w ith the angled tip of the Envoy catheter, w ith or w ithout CCA. Th e VTK cath eter is advan ced in a left-to-righ t direct ion
a soft guidew ire placed in th e CCA (Fig. 21.3b). Bip lan e flu oros- across th e aor t ic arch , w ith it s t ip poin ted ceph alad. Th e target
copy an d roadm ap tech n iqu e are h elpfu l in safely advan cing th e vessel is cath eterized w ith direct flu oroscopic visualizat ion (Fig.
guide cath eter in to posit ion in th e CCA. Th e an teroposterior (AP) 21.4b). Biplan e fluoroscopy an d roadm ap tech n ique are h elpful
flu oroscopy un it is cen tered su ch th at th e aort ic arch is visu al- in safely advan cing th e gu ide cat h eter in to posit ion in th e CCA.
ized, an d th e lateral p lan e is cen tered su ch th at th e carot id bifu r- Th e AP p lan e is cen tered su ch th at th e VTK cath eter an d Cook
cat ion is in clear view so t h at t h e ECA m ay be selected . On ce Sh u t tle are seen in th e aor t ic arch . Th e lateral plan e is cen tered
view s are selected, a roadm ap of th e target vessel is created, an d su ch th at th e carot id bifu rcat ion is in clear view so th at th e ECA
th e gu idew ire is advan ced in to th e ECA or CCA, w ith care t aken m ay be selected an d cat h eters advan ced over t h e w ire in to p o -
to avoid dist u rbing th e carot id plaque. Th e guide cath eter is th en sit ion w it h ou t d ist u rbing t h e carot id p laqu e. On ce view s are
advan ced over th e w ire in to posit ion just proxim al to th e sten o- selected, a roadm ap of th e target vessel is created, an d a st iff
sis (Fig. 21.3c). 0.035-in ch or st an dard 0.038-in ch exch ange-length gu idew ire is

a b c

Fig. 21.3a–c Guide catheter placem ent with a sm all 6-French (F) cathe- with the angled tip of the Envoy catheter. The guidewire is advanced into
ter. (a) The 6F guide catheter is brought up through the 6F fem oral sheath the external carotid artery or com m on carotid artery, taking care to avoid
over a soft 0.035-inch guidewire and parked within the descending aorta. disturbing the carotid plaque. (c) The guidewire is then advanced over the
(b) The targeted vessel is cannulated under direct fluoroscopic visualization wire into position just proxim al to the stenosis.

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21 Endovascular Treatment of Carotid Stenosis 269

a b

c d

Fig. 21.4a–d Guide catheter placement for a long 6F sheath. (a) The scopic visualization. (c) A roadm ap of the target vessel is created, and a stiff
Cook Shut tle (Cook Medical, Bloom ington, IN) and dilator are advanced 0.035- or 0.038-inch exchange-length guidewire directed into the external
over the wire into position in the descending aorta, and the wire and sheath carotid artery under direct fluoroscopic inspection with roadmap guidance,
subsequently rem oved. The Cook Shut tle is now in position for selection of taking care to avoid disturbing the carotid plaque. (d) The VTK catheter is
the target vessel. (b) A VTK catheter (Vitek, Cook Medical, Bloom ington, then advanced over the wire, and the Cook Shut tle is advanced over the
IN) is advanced in a left-to-right direction across the aortic arch with its tip VTK catheter until the Cook Shut tle is in place within the com m on carotid
pointed cephalad. The target vessel is catheterized under direct fluoro- artery, proxim al to the stenosis.

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270 III Ischemic Stroke and Vascular Insufficiency

directed in to th e ECA u n der direct flu oroscopic in sp ect ion w ith clu sion balloon s are in flated w it h a 50:50 m ixt u re of salin e an d
roadm ap guidan ce, t aking care to avoid dist u rbing th e carot id con t rast m aterial to en able visu alizat ion . St asis of flow m ay be
plaqu e (Fig. 21.4c). For a CCA lesion , a st iff w ire w ith a J-t ip (Am - tested by inject ing a sm all am oun t of con t rast m aterial in to th e
plat z J, Cook Medical, Bloom ington , IN) is brough t in to p osit ion vessel lu m en . Som e d ifficu lt y m ay be en cou n tered in gu id in g
in th e d ist al CCA, t aking care to avoid d ist u rbing th e carot id t h e m icrow ire t ip aw ay from th e proxim al p rotect ion cath eter
plaqu e. Th e VTK cath eter is h eld in place as is th e w ire, an d th e bet w een th e occlusive balloon s. If th e m icrow ire is n ot freed
Cook Sh ut tle is advan ced over th e VTK cath eter an d w ire u n t il from th e cath eter w ith sim p le torqu e m an ip u lat ion , a dist al ac-
th e Cook Sh u t tle is in place w ith in th e CCA, p roxim al to th e ste- cess cath eter or m u lt ipurpose angled cath eter m ay be used to
n osis (Fig. 21.4d). In cases w h ere a tor t uou s in n om in ate ar ter y– redirect th e m icrow ire ou t of th e proxim al protect ion device an d
r igh t CCA com p lex is en cou n tered , a Slip cat h eter m ay allow tow ard th e lesion . Du ring exch ange for th e distal access cath eter
easier passage of th e Cook Sh ut tle th an th e VTK by st raigh ten ing or m ult ipurpose angled cath eter, th e occlusive balloon s sh ould
th e sh ape of th e in n om in ate ar ter y an d righ t CCA origin . How - be deflated (to p erm it flow ) an d su bsequ en t ly rein flated (for
ever, difficult y con t rolling th e t ip of th e Slip cath eter w ith in th e flow st asis or reversal) w h en t h e m icrow ire h as been p rep ared
aor t ic arch m ay pu t th e p at ien t at h igh er risk for th rom boem bo- to cross th e lesion .
lism from dist urban ce of p laqu e w ith in th e aor t ic arch . Th e m icrow ire is carefu lly d irected u n d er roadm ap gu idan ce
th rough th e sten osis so th at th e p laqu e is n ot dist u rbed . On ce
th rough th e area of sten osis, th e m icrow ire is easily n avigated to
Proximal Protection or a Difficult Aortic Arch
a posit ion dist al to th e lesion (Fig. 21.6). Ideally, th e m icrow ire
For placem en t of a proxim al p rotect ion gu ide cath eter or dist al t ip w ill be p osit ion ed w ith in th e p et rou s segm en t of th e ICA for
p rotect ion in cases w h ere t h e gu id e cat h eter can n ot be easily passage of th e sten t in to p osit ion . For p at ien t s w ith a tor t u ou s or
d elivered over th e w ire to it s target posit ion , a cath eter exch ange looped ICA, n avigat ion in to th e dist al cer vical ICA m ay be m ore
m ay be required. In th is tech n ique, a 9F sh eath is placed. A diag- difficu lt . In su ch cases, th e m icrow ire is p assed to a p oin t in th e
n ost ic cath eter is em ployed to cath eterize th e t arget vessel w ith cer vical ICA th at en ables passage of th e sten t safely beyon d th e
direct flu oroscopic visu alizat ion . Biplan e flu oroscopy an d road- lesion but does not cause undue injury to the vessel wall. For prox-
m ap tech n ique are h elpfu l in safely advan cing th e guide cath eter im al protect ion cases, th e w ire is n ow in posit ion for crossing
in to posit ion in th e CCA. Th e AP p lan e is cen tered such th at th e w ith th e sten t . For dist al protect ion cases, th e filter is deployed
guide cath eter is visualized w ith in th e aort ic arch . Th e lateral in the distal cer vical segm ent of th e ICA, and the introducer cath -
plane is centered such that the carotid bifurcation is in clear view eter is exch anged for th e sten t .
so th at th e ECA m ay be selected an d cath eters advan ced over a Most lesion s can be n avigated w it h a steerable m icrow ire;
soft 0.035-in ch gu idew ire in to p osit ion w ith in th e ECA w ith ou t h ow ever, in som e cases, a st iffer w ire is required. For exam ple, a
dist u rbing th e carot id p laqu e. On ce view s are selected, a road- crit ical sten osis or labyrin th in e n arrow ing does n ot allow easy
m ap of th e t arget vessel is created , an d t h e soft gu id ew ire ad - passage of th e m icrow ire th rough th e lesion w ith ou t d isru pt ion
van ced in to t h e ECA u n d er d irect flu oroscop ic in sp ect ion w it h of th e plaqu e. In such cases, a m ult ipurpose angled cath eter an d
roadm ap gu idan ce, t aking care to avoid dist u rbing t h e carot id a soft 0.035-in ch w ire w ill facilitate passage of such a lesion , al-
plaqu e (Fig. 21.5a). Th e diagn ost ic cath eter is advan ced over th e beit w ith som e p laqu e d isr u pt ion . In t h is scen ar io, p roxim al
w ire in to th e ECA (Fig. 21.5b) an d th e soft guidew ire rem oved. p rotect ion w ith flow reversal is favorable to reduce th e risk of
An exch ange-length st iff w ire (Supra Core, Abbot t Vascular, Ab - em bolism . On ce t h e 0.035-in ch w ire is directed th rough th e le-
bot t Park, IL) is advan ced th rough t h e diagn ost ic cat h eter in to sion , th e m u lt ip u rp ose angled cath eter is brough t th rough th e
posit ion w ith in th e ECA, an d th e diagn ost ic cath eter is rem oved lesion , an d th e 0.035-in ch w ire is exch anged ou t th rough th is
(Fig. 21.5c). Th e st iff w ire in it s d ist al p osit ion w ill st raigh ten cath eter for a 0.014-in ch w ire. Th e sten t can be delivered over
t h e tor t u ou s segm en ts of th e vessel an d facilitate p assage of th e th e m icrow ire an d in to posit ion at th e site of th e sten osis.
gu ide cath eter in an over-th e-w ire tech n iqu e (Fig. 21.5d).

Exchange Technique
Microw ire Manipulation Rem oval of a dist al protect ion filter device, placem en t of th e
W it h t h e gu id e cat h eter in p osit ion p roxim al to t h e sten osis, sten t , an d post sten t angiop last y represen t th e m ost im p or t an t
m icrow ire m an ipu lat ion m ay begin . For cases of p roxim al p ro- parts of the procedure. Th ese steps require careful exchange tech -
tect ion , a steerable 0.014-in ch gu idew ire m ay be u sed for cross- n ique for a successfu l sten t ing an d angioplast y procedure. Th e
in g t h e sten ot ic lesion . For d ist al p rotect ion cases, a steerable part icu lar tech n iqu e em ployed is called “rapid exch ange,” as op -
0.014-in ch m icrow ire is in cluded in th e system . In eith er case, posed to “over-the-w ire exchange.” The reason for rapidit y is that
som e angu lat ion of t h e t ip of t h e m icrow ire is recom m en d ed at any t im e on ly a sm all por t ion of th e device being delivered is
for ease of gu idan ce t h rough t h e area of sten osis. Microw ire act u ally ru n n ing on th e w ire. Th e rapid-exch ange system , popu-
sh ap ing is u n iqu e to t h e p at ien t ’s an atom y an d m ay requ ire a larized du ring cardiac in ter ven t ion s, is also called th e m on orail
sh or ter or longer angu lat ion , dep en ding on th e sh ap e of th e ca- system . Th is system en ables devices to be pu sh ed u p to th e le-
rot id bifu rcat ion . sion an d back ou t rapidly, w ith out th e n eed for m et iculous ex-
Th e m icrow ire or m icrow ire–filter system is advanced th rough ch anges as requ ired in th e over-th e-w ire sit u at ion . Th e on ly t im e
th e gu ide cath eter w ith an in t rodu cer sh eath to th e t ip of th e w h en an act ual exch ange is required is w h en th e cath eter th at is
guidew ire, an d a roadm ap is created en abling a view th at facili- act ually “m on orailing” on th e m icrow ire n eeds to be rem oved.
tates easy differen t iat ion of th e ICA an d ECA an d visu alizat ion of Exch ange over th e m icrow ire m ay be perform ed by a single op -
th e sten osis. For proxim al protect ion cases, th e CCA an d ECA oc- erator bu t is best p erform ed w ith an en dovascu lar n eu rosu rgeon

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21 Endovascular Treatment of Carotid Stenosis 271

a b

Fig. 21.5a–d Guide catheter placem ent for proxim al protection and
a difficult arch. (a) Under direct fluoroscopic visualization, a diagnostic
catheter is used to catheterize the target vessel. Biplane fluoroscopy
with roadm ap technique is employed to guide the soft guidewire into
the external carotid artery. (b) The diagnostic catheter is advanced over
the wire into the ECA, and the guidewire rem oved. (c) An exchange-
length stiff wire (Supra Core, Abbot t Vascular, Abbot t Park, IL) is ad-
vanced through the diagnostic catheter into position within the ECA; the
diagnostic catheter is rem oved. (d) The stiff wire in its distal position will
c d
straighten the tortuous segments of the vessel and allow passage of the
guide catheter in an over-the-wire technique.

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272 III Ischemic Stroke and Vascular Insufficiency

a b

Fig. 21.6a,b Microwire m anipulation and crossing the lesion. (a) Distal lates dislodged from the clot to exit through the catheter, rather than travel
protection case: A distal protection system has a 0.014-inch steerable m i- into the brain. (b) Proxim al protection case: A proxim al protection system
crowire with an at tached filter system . The m icrowire is carefully navigated provides protection during lesion crossing with the m icrowire. The balloons
across the lesion under roadm ap guidance to m inim ize plaque trauma. The positioned within the com m on carotid and external carotid arteries are
m icrowire is advanced to the petrous segm ent of the internal carotid ar- expanded to arrest or reverse flow, such that particulates dislodged during
tery. Once distal to the lesion, the filter device is deployed. For protection crossing of the lesion are aspirated through the guide catheter, rather than
during lesion crossing before deploym ent of the filter, the hub of the guide traveling into the brain.
catheter m ay be opened for back-bleeding and to encourage any particu-

an d an exp er ien ced assist an t . Th e en d ovascu lar n eu rosu rgeon m oves th e device deliver y cath eter from th e w ire an d loads th e
is resp on sible for t h e dist al t ip of t h e m icrow ire an d en su res n ext device on to th e w ire (Fig. 21.7c). Th rough out th is exch ange
m in im al m ovem en t s of t h e m icrow ire t ip as w ell as t h e d ist al process, th e en dovascu lar n eu rosu rgeon is con t in u ou sly m on i-
protect ion device (if ap p licable). Th e assist an t is resp on sible for toring th e site of th e distal t ip of th e m icrow ire w ith th e aid of
m ain taining st abilit y of th e m icrow ire an d m on itoring th e gu ide th e fluoroscope.
cath eter for sign s of dow nw ard h ern iat ion in to th e aor t ic arch in For th e deliver y of a device across th e lesion , th e n ext device
conjun ction w ith passage of d evices. cat h eter in sequ en ce is d elivered over t h e w ire u p to t h e sh eat h
Th e first par t of th e exch ange en t ails rem oving a device d eliv- en t r y site. Th e assist an t t h en grasp s con t rol of t h e m icrow ire
er y cath eter over th e m icrow ire. For a m icrow ire exch ange, th e at th e p oin t w h ere t h e m icrocat h eter m on orail system en ds an d
en d ovascu lar n eu rosu rgeon carefu lly p u lls t h e d evice d eliver y th e free w ire is n oted exit ing th e m icrocath eter. Th e assist an t
cath eter along th e length of th e m icrow ire w ith ou t losing grasp stead ies t h e w ire, en su r in g t h at t h e t ip in t h e h igh cer vical/
of th e m icrow ire (Fig. 21.7a). To perform th is task, th e en dovas- p et rou s carot id d oes n ot m ove u n d er d irect flu oroscop ic visu al-
cular n eurosurgeon grasp s th e m icrow ire w ith th e left h an d an d izat ion (Fig. 21.7d). Th e en dovascu lar n eu rosu rgeon pu sh es th e
drags th e cath eter to be exch anged ou t of th e body w ith th e righ t m icrocath eter in to th e sh eath , delivering th e en t ire m on orail
h an d. W hen th e cath eter can n o longer be pulled w ith out pulling system , w h ile t h e assist an t stead ies t h e w ire. On ce t h e en dovas-
th e m icrow ire, th e m on orailed m icrocath eter is at th e h u b of th e cu lar n eu rosu rgeon regain s con t rol of th e m icrow ire, th e w ire
guide cath eter. At th is poin t , w e begin th e brief exch ange by th e is h eld w it h t h e left h an d w h ile th e cat h eter is p u sh ed d ist ally
left h an d grasping th e m icrocath eter an d w ith draw ing it ou t of w it h t h e r igh t h an d u n t il it em erges from t h e d ist al t ip on d i-
t h e body as t h e r igh t h an d stead ies t h e m icrow ire by m ovin g rect flu oroscopy. At th is p oin t , th e device is delivered over th e
m ore proxim ally along th e m icrow ire sequen t ially, grasping it at w ire in to p osit ion at t h e lesion w it h th e en d ovascu lar n eu rosu r-
m ore proxim al posit ion s un t il th e en t ire m icrocath eter is ou t of geon’s righ t h an d w h ile th e w ire is pin ch ed an d con t rolled by
th e h u b (Fig. 21.7b). At th at poin t , th e en dovascular n eurosu r- th e n eu rosu rgeon’s left h an d . Th is p rocess is p er for m ed u n d er
geon pinch es th e m icrow ire at th e sh eath an d th e assistan t re- d irect flu oroscop ic visu alizat ion of t h e m icrow ire t ip t h rough -

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21 Endovascular Treatment of Carotid Stenosis 273

Fig. 21.7a–d The exchange technique. The endovascular neurosurgeon down the wire and reestablishes control of the wire. (c) Steps a and b are
carefully pulls the device delivery catheter along the length of the m icro- continued until the catheter tip is beyond the sheath and the wire can be
wire without losing grasp of the m icrowire. (a–c) The first portion of the controlled. (d) The next device is delivered over the wire by the endovascu-
exchange consists of rem oving a device delivery catheter over the m icro- lar neurosurgeon with the right hand while the sheath is controlled with the
wire. (a) The catheter is removed over the straightened wire with the left left hand. The assistant controls the wire during this process. The exchange
hand while the wire is stabilized with the right hand. (b) The left hand process is repeated for each step of the stenting procedure.
grasps the catheter and stabilizes the wire while the right hand m oves

ou t . Th e exch an ge p rocess is rep eated for each step of t h e sten t - be un reliable at th is poin t of th e procedure due to vessel defor-
in g procedu re. m at ion w ith posit ion ing of th e sten t . Con t in uou s fluoroscopic
visu alizat ion is u sed for p lacem en t of th e sten t an d angioplast y.
Th e sten t is brough t in to p osit ion u sing an exch ange tech n iqu e.
Stent Placement and Angioplasty
If th e sten t is n ot easily passed th rough th e lesion over th e m i-
Sten t posit ion ing is determ in ed w ith th e u se of angiography. An crow ire, a presten t angioplast y is perform ed. Th e (n on deployed)
osseous lan dm ark (a cer vical ver tebral level) sh ould be iden t i- sten t sh ou ld be exch anged for an u n dersized angiop last y balloon
fied for th e distal lan ding site of th e sten t , as th e roadm ap m ay (t ypically 2–3 m m ) to create a path w ay for th e sten t . Th e balloon

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274 III Ischemic Stroke and Vascular Insufficiency

cath eter is exp an ded to n om in al p ressu re an d deflated abru ptly. just proxim al to th e sten t . Un der fluoroscopic visualizat ion , th e
An u n dersized balloon is used to m in im ize plaque t raum a. In th e recapt u re cat h eter is brough t t h rough t h e sten t ju st p roxim al
case of presten t angiop last y, th e angioplast y balloon is th en ex- to th e dist al protect ion filter. Th e filter is th en pulled back in to
ch anged over th e m icrow ire for th e sten t . th e recapt u re cath eter. Th e m icrow ire an d dist al p rotect ion filter
Th e sten t is easily visu alized in it s n on deployed st ate on th e (w it h in t h e recapt u re cath eter) are t h en rem oved as a u n it
d eliver y cath eter. It sh ou ld be cau t iou sly bu t exp ed it iou sly th rough th e sten t an d gu ide cath eter w h ile th e gu ide cath eter
brough t over th e w ire in to posit ion cen tered about th e area of h ub is open ed for back-bleeding to fur th er m in im ize th rom bo-
greatest sten osis. Alth ough th e en dovascu lar n eurosu rgeon d e- em bolism .
livers th e sten t to th e site of sten osis, th e assistan t m on itors th e Som e d ifficu lt y m ay be en cou n tered w ith bringing th e re-
guide cath eter posit ion for sign s of dow nw ard h ern iat ion tow ard t rieval cath eter th rough th e sten t , in eith er direct ion . Th is m ay
th e aor t ic arch . In t h is even t , th e gu ide cath eter m ay n eed to be be p ar t icu larly p roblem at ic w it h op en -cell sten t s, w h ere t h e
reposit ion ed for safe deliver y to th e site of sten osis. With th e cath eter t ip m ay be caugh t n ot on ly on eith er en d of th e sten t bu t
sten t in posit ion across th e lesion , th e dist al p or t ion of t h e sten t on any of th e open -cell segm en t s of th e sten t . In th is even t , th e
is placed at th e predeterm in ed osseou s lan dm ark an d deployed pat ien t m ay be asked to t u rn h is or h er h ead in eith er direct ion
an d th en delivered according to th e m an ufact u rer’s recom m en - as passage of th e ret rieval cath eter th rough th e sten t is at tem pted
dat ion s. For closed-cell sten t s, a m alposit ion ed sten t m ay be re- again . If th is is n ot su ccessfu l, th e gu ide cath eter m ay be ad-
capt u red if p ar t ially d ep loyed (u p to 80% for m ost closed -cell van ced tow ard th e sten t to im prove th e angle of deliver y of th e
sten ts) an d rep osit ion ed. Typ ically, a p ersisten t n arrow ing of th e recapt u re device. If n eith er is successful, a m u lt ipurpose angled
sten t at th e site of greatest sten osis is eviden t , requ iring p ost- cath eter m ay be em p loyed in stead of th e recapt u re cath eter.
sten t ing angioplast y. After th e devices are rem oved from th e gu ide cath eter, th e
Th e sten t deliver y cath eter is exch anged over th e m icrow ire auth ors rou t in ely perform a cerebral angiogram to assess sm ooth
for the angioplast y balloon, w hich is centered at th e residual n ar- syn ch ron ized perfu sion th rough ou t th e en t ire carot id territor y
row ing of th e sten t u sing th e radiopaqu e m arkers on th e angio- to look specifically for any delayed capillar y fill or oth er larger
plast y balloon cath eter. On ce in p osit ion , th e angioplast y balloon occlusion s. Th e auth ors also exam in e th e pat ien t by perform ing
is in flated to n om in al p ressu re an d su bsequ en t ly d eflated an d an abbreviated n eurologic exam in at ion to en sure th at th ere is n o
rem oved. clin ical eviden ce of debris h aving been released in to th e in t ra-
cran ial circu lat ion . If th e pat ien t is sym ptom at ic or th ere is evi-
den ce of som e areas of slow filling an d n o large vessel occlu sion ,
Distal Protection Device Recapture an in t raar terial or an in t raven ou s loading dose of glycoprotein
After sten t d ep loym en t an d p ost sten t an giop last y, an angio - IIb/IIIa in h ibitors is ad m in istered .48 If in it iated , t h is in fu sion is
grap h ic r u n of t h e cer vical carot id ar ter y at t h e site of sten osis t ypically con t in ued for 24 h ou rs. Eviden ce of large-vessel occlu-
is perform ed to en su re adequ ate revascularizat ion an d n o vessel sion m ay n ecessit ate th e p erform an ce of in t raar terial or in t rave-
injur y (Fig. 21.8). In addit ion , th e auth ors t ypically ut ilize on e or n ou s th rom bolysis or m ech an ical th rom bectom y.
t w o addit ion al steps at th is poin t . First , w h en u sing dist al em -
bolic protect ion , an aspirat ion cath eter (i.e., Expor t AP cath eter
Arteriotomy Closure
[Med t ron ic, Min n eapolis, MN] or Pron to cath eter [Vascu lar Solu -
t ion s, Min n eap olis, MN]) is u sed an d advan ced u p to th e cau dal A closure device is used w h en possible to lim it th e length of pa-
exten t of th e deployed filter. Blood (60–100 m L) is aspirated to t ien t im m obilit y post procedu rally. After device closure, bedrest
rem ove em bolic d ebr is t h at m ay be su sp en d ed p roxim al to or for 1 to 2 h ou rs is recom m en d ed . If safe u se of a closu re device
w ith in th e filter. Th e aspirated blood is run th rough m icrofilters is n ot possible, th e sh eath is left in place un t il th e pat ien t’s act i-
to en sure a clean ret urn . Th is approach is suppor ted by lim ited vated coagulat ion t im e or par t ial th rom boplast in t im e is n or-
dat a w h ereby som e debris w as n oted in filters u p on su ch asp ira- m alized prior to sh eath rem oval to lim it h em atom a form at ion .
t ion .47 Th e asp irat ion cath eter is rem oved on ce t w o sequ en t ial Man u al p ressu re for 30 to 40 m in u tes follow ed by bedrest for
draw s are n egat ive for em bolic debris. 4 h ou rs is t ypically su fficien t to lim it h em atom a form at ion .
Th e secon d step rou t in ely p er for m ed for bot h p roxim al- an d
d ist al-p rotected p roced u res is d oing a single, slow sw eep w it h
t h e IVUS cat h eter, obt ain in g a carefu l exam in at ion of t h e sten t
Postprocedure Course
t in es to en su re th at n o evagin at ing debris ou t of th e sten t or Neu rovascu lar m on itoring is p erform ed in a crit ical care or in -
oth er in t ralum in al debris or th rom bu s are n oted. On ce th e IVUS term ediate care set t ing for at least 12 h ou rs postoperat ively. Pa-
st u dy is n egat ive, th e p roced u re is n early com p lete, except for t ien ts m ay exp erien ce w ide variat ion s in n orm al blood p ressu re
rem oval of th e m icrow ire an d em bolic protect ion devices. or h ear t rate after angioplast y at th e carot id bu lb. After revascu -
For cases of p roxim al protect ion , th e au th ors do n ot p erform larizat ion , systolic blood p ressu re is m ain t ain ed at a level of 60
a post sten t cer vical angiogram un t il th e IVUS is n egat ive for po- to 80% of n orm al to m in im ize th e risk of rep erfu sion h em or-
ten t ial em bolic sources. After th e angiogram is perform ed an d rh age. Vasop ressors or an t ihyp er ten sive agen ts are adm in istered
considered adequate, no distal protection device recapture is nec- as n eeded. Most pat ien ts are disch arged h om e on th e first post-
essar y, an d th e m icrow ire is sim p ly rem oved u n der flu oroscopic operat ive day. Doppler u lt rason ography of th e sten ted vessel is
visu alizat ion to en su re th at it is rem oved th rough th e sten t w ith - perform ed to ser ve as a n ew baselin e for follow -u p . Pat ien ts are
out difficu lt y. For cases w ith a distal p rotect ion device, th e re- m on itored at 1 m on th , 6 m on th s, an d yearly w ith Doppler ult ra-
t rieval cath eter is exch anged over th e m icrow ire in to posit ion son ography to assess sten t paten cy.

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21 Endovascular Treatment of Carotid Stenosis 275

a b

c d

Fig. 21.8a–d Examples of carotid stenting cases. Angiogram (a) before and (b) after placem ent of a closed-cell cylindrical stent. Angiogram (c) before
and (d) after placem ent of an open-cell stepped stent. An open-cell stent was used due to vessel curvature at the site of stenosis.

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276 III Ischemic Stroke and Vascular Insufficiency

based on t h e st rengt h of m u lt ip le ran d om ized con t rolled t ri-


■ Patient Outcomes als.1,3,4,21,22 Alth ough carot id sten t ing h as n ever sh ow n superior-
Th e Carot id Revascu larizat ion En dar terectom y versu s Sten t ing it y over carot id en dar terectom y by com p arison in t rials, w ith
Trial (CREST) 5 rep resen ts th e best est im ate of p erip rocedu ral st ringen t use of em bolic p rotect ion d evices, th e periproced u ral
com plications and long-term outcom es after carotid arter y stent- risk of carotid stenting is com parable to that of endarterectom y,5
ing, alth ough th e CREST experien ce does n ot in clude th e poten - an d com plicat ion rates h ave dim in ish ed w ith successive carot id
t ial ben efits of p roxim al protect ion . Periprocedu re m orbidit y in stenting trials and technological advances.49 Ongoing experien ce,
CREST in cluded an aggregate 5.2% risk of st roke, m yocardial in - tech n ological advan ces, an d a populat ion w ith a pen ch an t for
farct ion , or death w ith in 30 days of th e carot id sten t ing proce- m in im ally invasive procedu res m ay ult im ately lead to sten t ing
du re. Th is w as n ot st at ist ically differen t from th e 4.5% aggregate on e day superseding en dar terectom y for periprocedural safet y
risk of th e sam e ou tcom es for p at ien t s u n dergoing carot id en d- in carot id revascu larizat ion .
arterectom y. With either treatm ent, the postprocedural incidence
of ipsilateral stroke rem ain ed low at 4 years, at 2%.

■ Acknow ledgments
We t h an k Pau l H. Dressel for p rep arat ion of t h e im ages an d
■ Conclusion Debra J. Zim m er for editorial assist an ce.
Carot id en dar terectom y h as t h e dist in ct ion am ong su rgical in -
ter ven t ion s of being an im provem en t over m edical th erapy alon e

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2. Ran dom ised t rial of en dar terectom y for recen tly sym ptom at ic carot id st roke in p at ien t s w ith asym ptom at ic carot id sten osis on best m ed ical
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6. Osborn AG, Jacobs JM. Diagn ost ic Cerebral Angiography, 2nd ed. Ph iladel- 20. Hir t LS. Progression rate an d ipsilateral neurological event s in asym ptom -
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13. Stoll G, Bendszus M. Inflam m ation and atherosclerosis: novel insights into 1999;30:1116–1120
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14. Redgrave JN, Lovet t JK, Gallagher PJ, Roth w ell PM. Histological assessm ent and preoperative assessm ent of risk. Mayo Clin Proc 1975;50:301–306
of 526 sym ptom at ic carot id plaques in relat ion to th e n at u re an d t im ing 26. Gasecki AP, Eliasziw M, Ferguson GG, Hach in ski V, Barn et t HJ; Nor th
of isch em ic sym ptom s: th e Oxford plaque st udy. Circulat ion 2006;113: Am er ican Sym ptom at ic Carot id En dar terectom y Tr ial (NASCET) Grou p .
2320–2328 Long-term progn osis an d effect of endarterectom y in pat ien t s w ith sym p -
15. Goessen s BM, Visseren FL, Kappelle LJ, Algra A, van der Graaf Y. Asym p - tom at ic severe carot id sten osis and con t ralateral carot id sten osis or oc-
tom at ic carot id ar ter y sten osis an d t h e r isk of n ew vascu lar even t s in clusion : resu lt s from NASCET. J Neurosurg 1995;83:778–782

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27. Sun dt TM Jr, Sh arbrough FW, Traut m an n JC, Gron er t GA. Mon itoring tech - 39. Bosiers M, Deloose K, Verbist J, Peeters P. Carot id ar ter y sten t ing: w h ich
n iqu es for carot id en d ar terectom y. Clin Neu rosu rg 1975;22:199–213 sten t for w h ich lesion ? Vascu lar 2005;13:205–210
28. Yadav JS, W h oley MH, Kun t z RE, et al; Sten t ing an d Angioplast y w ith Pro- 40. Hopkin s LN, Myla S, Grube E, et al. Carot id ar ter y revascularizat ion in h igh
tect ion in Pat ien t s at High Risk for En darterectom y Invest igators. Pro- su rgical risk pat ien t s w ith th e NexSten t and th e Filter w ire EX/EZ: 1-year
tected carotid-arter y stenting versus endarterectom y in high-risk patients. result s in th e CABERNET t rial. Catheter Cardiovasc In ter v 2008;71:950–
N Engl J Med 2004;351:1493–1501 960
29. Am igh i J, Sabet i S, Dick P, et al. Im pact of th e rapid-exch ange versus over- 41. Har t JP, Bosiers M, Deloose K, Uflacker R, Sch ön h olz CJ. Im pact of sten t
th e-w ire tech n iqu e on p rocedu ral com p licat ion s of ren al ar ter y angio- design on the outcom e of in ter ven t ion for carot id bifurcat ion sten osis.
plast y. J En dovasc Th er 2005;12:233–239 J Cardiovasc Su rg (Torin o) 2010;51:799–806
30. Kast r u p A, Grösch el K, Krap f H, Breh m BR, Dich gan s J, Sch u lz JB. Early 42. Ricot t a JJ, Aburahm a A, Asch er E, Eskan dari M, Faries P, Lal BK; Societ y for
outcom e of carot id angioplast y and sten t ing w ith an d w ith ou t cerebral Vascular Surger y. Updated Societ y for Vascular Su rger y guidelin es for
protect ion devices: a system at ic review of th e literat u re. St roke 2003; m an agem ent of ext racran ial carot id disease. J Vasc Su rg 2011;54:e1–e31
34:813–819 43. Durran AC, Wat t s C. Curren t t ren ds in h eparin use during arterial vascular
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Neuroprotect ion during carot id ar ter y sten t ing using th e GORE flow re- 46. Chung C, Cayne NS, Adelm an MA, et al. Im proved hem odynam ic outcom es
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36. Orion D, Siddiqui AH, Levy EI, Hopkin s LN. W h en an d h ow to use proxim al 48. Du m on t TM, Kan P, Snyder KV, Hopkin s LN, Siddiqui AH, Levy EI. Adjun c-
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22 Medical Management of Vertebrobasilar
Occlusive Disease
Mat thew R. Reynolds, Gyanendra Kum ar, Jin-Moo Lee, and Gregory J. Zipfel

Ver tebrobasilar (VB) isch em ia accou n t s for 20% of isch em ic Natural History of Vertebrobasilar
strokes.1 Pathologies that occlude th e posterior circulation largely Occlusive Disease
determ in e th e clin ical p resen t at ion an d in clu de (1) sm all ar ter y
disease (lip ohyalin osis); (2) m ajor basilar ar ter y (BA) disease Few st u d ies h ave evalu ated isch em ic st roke r isk in sym ptom -
from an at h erom a, th rom bu s, or em bolu s; an d (3) large vessel at ic VBOD.5–15 We p er for m ed a ran d om effect s m et a-an alysis of
steno-occlusive disease (vertebrobasilar occlusive disease, VBOD) t h e exist ing stu dies (Fig. 22.1).3–7 Th e m ean w eigh ted probabil-
resu lt ing from ath erom atous sten osis, em bolic occlu sion , in sit u it y (MW P) of st roke recu rren ce w as 23%w h en evaluat ing VB ste-
throm bosis, or dissection. Multiple con dit ions w ith variable prog- n osis ≥ 50% (Fig. 22.1a).8–14 Th e MW P of death or depen den cy
n oses fall un der th e rubric of “VB ar ter y isch em ia.”2 Th is ch apter from fou r st u dies th at exam in ed severe VB sten osis or BAO w as
focu ses on VBOD to large vessel occlusion an d discusses (1) BA 44% (Fig. 22.1b).4,10,14,15 Th e m ean follow -up durat ion varied
occlusion (BAO), w h ich is gen erally catast roph ic; (2) VB dissec- from 3 m on th s to 6 years acros s st u dies. Th ere w as sign ifican t
t ion , w h ich can var y from t ran sien t isch em ic at tacks (TIAs) to h eterogen eit y in th e synth esis, at t ributable to differen ces in
BAO; an d (3) VB sten osis or d iffu se ath erom atou s disease, w h ich st u dy design , drug regim en s, length of follow -u p, an d tem poral
can p resen t w ith recu rring TIA, recu rren t VB isch em ic st rokes, bias (st u dies in cluded from 1986 to 2009).
an d BAO.
Acute Basilar Artery Occlusion
Acute BAO is a clin ically devastat ing disease w ith h igh m orbidit y
an d m or talit y. A ran dom effect s m et a-an alysis of 11 st udies in
■ Etiology w h ich conven t ion al m edical th erapy w as used to t reat BAO (an -
Large ar ter y occlusive disease is a m ore com m on cause of isch - t iplatelet an d/or an t icoagu lat ion ) gen erated a MW P of d eath of
em ic st roke in th e posterior circu lat ion as com p ared w ith th e 51% (Fig. 22.2a).1,16–25 Th e syn t h esis w as st at ist ically h eteroge-
an terior circulat ion , w h ereas th e frequen cy of ar ter y-to-ar ter y n eous w ith sou rces of h eterogen eit y sim ilar to th ose m en t ion ed
em bolism an d pen et rat ing ar ter y lesion s is sim ilar bet w een both above. Not ably, th e cu m u lat ive forest plot illust rates ch ron ologi-
circulat ion s.3 A com parison of VB st roke et iology across various cal im provem ent in pooled m ortalit y estim ates over tim e, reflect-
regist ries is illu st rated in Table 22.1.3–7 Large ar ter y disease (ste- in g an im p rovem en t in t reat m en t (Fig. 22.2b).1,16–25 A sim ilar
n osis or ath erom atou s disease) is th e m ost com m on m ech an ism ch ron ological t ren d is n oted in p ooled w eigh ted est im ates of
of VB isch em ia (30%), follow ed by card ioem bolism (22%), an d p robabilit y of d eat h or d ep en d en cy (77%) in BAO t reated w it h
lipohyalin osis (16%). Oth er et iologies (e.g., m igrain e an d dissec- conven t ion al m ed ical t h erapy (Fig. 22.3).1,16–25 In t h ese st u d ies,
t ion ) are u n com m on ly seen . w e w ere u n able to com p are ou tcom es bet w een an t ip latelet an d
In th e New Englan d Medical Cen ter Regist r y,3 occlusive le- an t icoagulan t t reat m en t .
sion s of > 50%w ere p resen t in th e bilateral in t racran ial ver tebral
ar ter y (VA) in 9% of pat ien ts, in th e bilateral ext racran ial VA in
Dissection
7%, an d in th e BA in 27%. Dissect ion of th e VA w as seen in 6/407
(1.5%) of cases. Am ong th ose pat ien ts w ith bilateral in t racran ial Cat ast rop h ic VB occlu sion u n com m on ly resu lt s from dissect ion
VA disease, 76%w ere hyper ten sive, 52%h ad elevated ch olesterol, (5% in th e BASICS regist r y). How ever, it is an im por tan t et iology
36% h ad diabetes, an d 36% sm oked cigaret tes. Of th ose w ith BA of VBOD w ith con t roversial m an agem en t im plicat ion s. A large
occlu sive disease, t w o-t h ird s w ere hyp er ten sive an d on e-th ird obser vat ion al st u dy, Cer vical Ar ter y Dissect ion s an d Isch em ic
had diabetes, high cholesterol, coronary arter y disease, or sm oked St roke Pat ien ts (CADISP) 26 fou n d th at pat ien t s w ith VA dissec-
cigaret tes. Th e Basilar Ar ter y In tern at ion al Cooperat ion St udy t ion (VAD) w ere you nger, m ore often w om en , less often h ad a
(BASICS)1 is a p rospect ive in tern at ion al regist r y design ed to bet- recen t in fect ion , less often h ad a h eadach e at adm ission , less
ter un derst an d outcom es after BAO an d differen ces in t reat m en t often h ad cerebral isch em ia, an d m ore often repor ted a recen t
respon se given th e absen ce of ran dom ized clin ical t rials on th is m in or n eck t rau m a as com p ared w ith p at ien t s w ith in tern al ca-
su bject . In BASICS, 62% of p at ien t s w ere hyper ten sive, 22% h ad rot id ar ter y d issect ion (ICAD). Th e score at ad m ission on t h e
diabetes, 28% w ere dyslip idem ic, 21% h ad at rial fibrillat ion (AF), Nat ion al In st it u tes of Health St roke Scale (NIHSS) w as low er in
an d 18% h ad coron ar y ar ter y d isease. Of t h e 592 p at ien t s, VB pat ients w ith VAD than in patients w ith ICAD, and 3-m onth func-
st roke et iology w as em bolic in 36%, ath erosclerot ic in 35%, an d t ion al ou tcom es w ere m ore favorable in VAD th an ICAD (odds
5% h ad d issect ion . rat io [OR] of p oor outcom e, i.e., m odified Ran kin Scale score > 2

278

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22 Medical Management of Vertebrobasilar Occlusive Disease 279

Table 22.1 Comparison of Stroke Mechanisms in the Posterior Circulation Across Various Registries

Large Artery Stenosis


Cardioembolic ± Atherothrombosis Lacunar
Study Author/Year N (%) (%) (%)

NEMCR3 Caplan/2004 407 24 46 14


LSR4 Devuyst/2002 233 16 39 16
BSR5 Moulin/2000 251 30 34 7
ASR6 Vemmos/2000 259 23 16 23
TOAST7 Libm an/2001 180 17 14 24
Mean weighted pooled estimate 22% 30% 16%
Abbreviations: ASR, Athens Stroke Registry; BSR, Besancon Stroke Registry; LSR, Lausanne Stroke Registry; NEMCR, New England Medial Center
Registry; TOAST, Trial of ORG 10172 in Acute Stroke Treatm ent.

[sligh t disabilit y or w orse], 3.99; 95% con fiden ce in ter val [CI], lesion s.31 Am er ican St roke Associat ion gu id elin es recom m en d
2.32–6.88). How ever, after adju st ing for baselin e NIHSS score, n on invasive im aging by CTA or MRA (rath er th an ult rasoun d) for
3-m on t h ou tcom es w ere n ot sign ifican t ly d ifferen t bet w een detect ion of VA disease as par t of an in it ial evalu at ion for p a-
ICAD an d VAD. A com bin at ion of pain an d progressive on set of t ien ts w ith isch em ic sym ptom s referable to th e VB circulat ion .32
st roke can h elp diagn ose VAD.27 In t racran ial VAD h as a poorer
progn osis th an ext racran ial VAD. Bilateral dissect ion s an d in it ial
severit y of st roke are associated w ith p oor ou tcom e.27
■ Medical Treatment
Intravenous Tissue -Type Plasminogen Activator
■ Diagnosis and Neuroimaging Th e Nat ion al In st it u te of Neu rological Disord ers an d St roke
Cerebral im aging is recom m en ded before in it iat ing any acu te (NINDS) t rial est ablish ed in t raven ous (IV) t issue-t ype plasm in o-
isch em ic st roke th erapy.28 In m ost in st an ces, com p u ted tom og- gen act ivator (t-PA) as th e m ain stay of th erapy for acu te isch em ic
raphy (CT) of t h e h ead p rovid es im p ort an t in form at ion for em er- st roke w ith in 3 h ou rs of on set .33 Th e Eu rop ean Coop erat ive
gen cy m an agem en t . For exam ple, th e presen ce of a hyperden se Acute St roke St udy III (ECASS III) 34 t rial p rovided eviden ce to
BA on CT is a st rong predictor of BA th rom bosis an d is associated allow th at w in dow to st retch to 4.5 hours.35 How ever, kn ow ledge
w ith poor sh or t- an d long-term outcom es after st roke.29 Com - regarding th e safet y an d efficacy of IV t-PA in VB isch em ic st rokes
pared w ith CT, m agn et ic reson an ce im aging (MRI) affords bet ter rem ain s sp arse for several reason s. First , on ly 5%of pat ien t s from
visualizat ion of p osterior fossa con ten ts an d im proved sensit iv- the NINDS st udy had VB isch em ic strokes (despite est im ates that
it y for d etect ing in fracted brain t issu e. How ever, MRI is often 20% of all strokes are localized to the VB circulation).1 Secon d, n o
im p ract ical in t h e set t ing of acu te isch em ic st roke w h en t im e ran dom ized con t rolled t rial h as invest igated th e safet y an d effi-
is of t h e essen ce, given it s p rolonged acqu isit ion t im e, lim ited cacy of IV t-PA based on st roke territor y. Th ird, th e ECASS I36 an d
availabilit y, an d in com pat ibilit y w ith m etal im p lan ts. Diffusion - II37 st u d ies on ly in clu d ed p at ien t s w ith h em isp h er ic st rokes,
w eigh ted im aging (DW I) h as h igh sen sitivit y an d specificit y for w h ereas t h e ECASS III32 an d Altep lase Th rom boLysis for Acu te
detect ing isch em ic lesion s an d correlates w ell w ith clin ical m ea- Non in ter ven t ion al Th erapy in Isch em ic St roke (ATLANTIS) 38,39
su res of st roke severit y.28 Perfusion w eigh ted im aging (PW I), on t rials did n ot rep or t th e n u m ber of p at ien t s w ith VB isch em ic
th e oth er h an d, p rovides a rep resen t at ion of isch em ic t issu e at st rokes. At least on e st udy, h ow ever, sh ow ed th at outcom e an d
risk by gen erat ing m aps of cerebral blood volu m e an d m ean m ortalit y follow ing an terior an d posterior circulat ion isch em ic
t ran sit t im e. A m ism atch bet w een DW I an d PW I m ay in dicate st rokes w ere sim ilar.40
isch em ic t issu e at r isk for in farct ion . Grad ien t ech o (GRE) se- Based on a ran dom -effect m et a-an alysis of five st ud ies,1,41—44
qu en ces h ave h igh sen sit ivit y for detect ing acu te h em orrh age. th e pooled recan alizat ion rate of acu te BAO w ith IV t-PA w as 57%
Thus, a m ultim odal MRI obtained w ithin the tim e constraint m ay (Fig. 22.4a). In acu te BAO t reated w ith IV t-PA, th e MW P of death
su p plan t CT as th e im aging m odalit y of ch oice for acu te st roke in w as 40% (Fig. 22.4b) an d th at of a poor outcom e w as 63% (Fig.
th e n ear fut ure. 22.4c). Th e MW P of in t racerebral h em or rh age (ICH) w as 13%
Con t rast-en h an ced m agn et ic reson an ce angiograp hy (MRA) (Fig. 22.4d), w h ich is in con t rast to th e low er risk of sym ptom -
w as rep or ted to be th e m ost sen sit ive n on invasive tech n iqu e to at ic ICH after IV t-PA in VB st rokes as com p ared w ith carot id
d etect VA sten osis an d w it h h igh sp ecificit y.30 CT an giograp hy st rokes repor ted in a previou s st u dy.40 Th is discrepan cy m ay be
(CTA) also h as good sen sit ivit y an d h igh sp ecificit y.31 In con t rast , exp lain ed by th e fact th at lacu n ar st rokes an d oth er sm all in -
ult rasoun d h as low sen sit ivit y for d etect ing VBOD an d m isses farcts w ere in cluded in st udies involving VB isch em ic st rokes.
m any vertebral sten oses.30 MRA is su p erior for recogn izing BA With th ese caveat s, IV t-PA rem ain s th e corn erston e of acute
occlu sive lesion s t h an for sim ilar ext racran ial/in t racran ial VA isch em ic st roke m an agem en t , regardless of path ology locat ion .
(text cont inues on page 285)

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280 III Ischemic Stroke and Vascular Insufficiency

Fig. 22.1a,b (a) Mean-weighted stroke recurrence rate in vertebrobasilar by Devuyst and Voet sch included patient s with basilar artery occlusion
occlusive disease (Registries by Devuyst and Voetsch included patients with in addition to basilar artery stenosis. Others only included those with ver-
basilar artery occlusion in addition to basilar artery stenosis. Others only tebrobasilar stenotic disease). *Lausane stroke registry. †NEPCSR. ‡Mean
included those with vertebrobasilar stenotic disease). (b) Mean-weighted weighted probabilit y.
death or dependency rate in vertebrobasilar occlusive disease (Registries

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22 Medical Management of Vertebrobasilar Occlusive Disease 281

Fig. 22.2a,b (a) Mean-weighted m ortalit y rate in basilar artery occlusion tional therapy. This delineates the impact of year of publication. As healthcare
(BAO) treated with conventional therapy (antiplatelet and/or anticoagula- and technology improve over tim e, m ortalit y decreases. ‡Mean weighted
tion). (b) Cum ulative forest plot of m ortalit y in BAO treated with conven- probabilit y.

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282 III Ischemic Stroke and Vascular Insufficiency

Fig. 22.3a,b (a) Mean-weighted death or dependency rate in basilar ar- treated with conventional therapy. Rates of death or dependency decline as
tery occlusion (BAO) treated with conventional therapy (antiplatelet and/or a function of tim e. ‡Mean weighted probabilit y.
anticoagulation). (b) Cum ulative forest plot of death or dependency in BAO

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22 Medical Management of Vertebrobasilar Occlusive Disease 283

Fig. 22.4a–d (a) Mean-weighted recanalization rate with intravenous throm bolysis in basilar artery occlusion. (b) Mean-weighted m ortalit y rate in basi-
lar artery occlusion treated with intravenous throm bolysis. (continued on page 284)

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284 III Ischemic Stroke and Vascular Insufficiency

Fig. 22.4a–d (continued ) (c) Mean-weighted death or dependency rate in basilar artery occlusion treated with intravenous throm bolysis. (d) Mean-
weighted intracerebral hem orrhage rate with intravenous thrombolysis in basilar artery occlusion.

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22 Medical Management of Vertebrobasilar Occlusive Disease 285

Antiplatelet Agents St at in t h erapy is recom m en d ed w ith a t arget ch olesterol goal


for th ose w ith congest ive h ear t disease (CHD) or sym ptom at ic
For secon dar y p reven t ion of st roke/TIA, asp irin (50 to 325 m g
ath erosclerosis of low -den sit y lipop rotein (LDL) < 100 m g/dL. An
daily), asp ir in p lu s an exten d ed -release d ipyr idam ole (25 an d
LDL < 70 m g/dL is recom m en ded for ver y h igh -risk p at ien t s w ith
200 m g t w ice daily, resp ect ively), or clop id ogrel (75 m g daily)
m ultiple risk factors. Based on th e St roke Preven t ion by Aggres-
is an acceptable opt ion .45 An t ip latelet t h erapy sh ou ld be in it iated
sive Reduction of Cholesterol Levels (SPARCL) trial, adm in istration
w ith in 48 h ours of st roke.28 Th e an t iplatelet regim en sh ou ld be
of st at in s is recom m en ded for secon dar y preven t ion of isch em ic
in dividu alized based on pat ien t risk factors, cost , toleran ce, clin i-
st roke or TIA.
cal ch aracterist ics, as w ell as gu idan ce from regu lator y agen -
cies.32 Dual an t iplatelet th erapy w ith aspirin an d clopidogrel h as
n ot been sh ow n to be useful an d is n ot recom m en ded due to th e Blood Pressure Management
in creased risk of h em orrh age 46 un less an oth er in dicat ion exist s.
Blood pressure (BP) redu ct ion is recom m en ded for both preven -
t ion of recu rren t st roke an d p reven t ion of oth er vascu lar even t s
Anticoagulants in p at ien t s w h o h ave h ad an isch em ic st roke or TIA an d are be-
yon d th e first 24 h ou rs.45 An absolu te t arget BP an d th e d egree of
Th ere is n o role of u rgen t an t icoagu lat ion in acu te isch em ic redu ct ion are un cert ain , but sh ould be in dividualized. Ben efit is
st roke.28 Also, an t icoagu lat ion sh ou ld n ot be in it iated w ith in 24 associated w ith an average reduct ion of 10/5 m m Hg, an d n or-
h ours of IV t-PA t reat m en t .28 For p reven t ion of deep vein th rom - m al BP levels h ave been defin ed as < 120/80 m m Hg. In addit ion
bosis, it m ay be safely begu n in prophylact ic doses 24 h ou rs after to dietar y an d lifest yle m odificat ion , drug th erapy is often in di-
IV t-PA. cated. Th e opt im al drug regim en to ach ieve th e recom m en ded
level of redu ct ion is u n cer tain , bu t th e available dat a in dicate
Prevention that diuretics or the com bin ation of diuretics and an angioten sin-
conver t ing en zym e in h ibitor (ACEI) are u seful.
Opt im al m edical th erapy, in clu ding an t ip latelet th erapy, st at in
th erapy, an d risk factor m odificat ion , is recom m en ded for all pa-
t ien ts w ith VA sten osis an d a TIA or st roke.45 Th e im por t an ce of Diet and Lifestyle Modifications
m edical th erapy is u n derscored by a recen t large ran dom ized In ad d it ion to salt rest r ict ion ; w eigh t loss; an d con su m pt ion of
con t rolled t rial dem on st rat ing su p eriorit y of aggressive m ed ical a diet rich in fruit s, vegetables, an d low -fat dair y products, it is
m an agem en t over en dovascu lar angiop last y an d sten t ing in pa- vital to advise sm oking cessat ion .45 Oral cessat ion m edicat ion s,
t ien t s w ith sym ptom at ic in t racran ial ath ero-occlu sive disease.47 cou n selin g, an d n icot in e p rod u ct s are often effect ive. Pat ien t s
In gen eral, p at ien t s w ith sym ptom at ic VBOD sh ou ld receive an - w ith isch em ic st roke or TIA w h o are h eavy drin kers sh ould elim -
t iplatelet th erapy w ith asp irin (75 to 325 m g daily) to p reven t in ate or redu ce th eir con sum pt ion of alcoh ol. Ligh t-to-m oderate
m yocardial in farct ion (MI) an d oth er isch em ic even t s.32 Long- levels of alcoh ol con su m pt ion (< 2 d r in ks/day for m en an d
term oral an t icoagulat ion w ith a vit am in K an t agon ist (e.g., Cou - 1 drin k/day for n onpregn an t w om en ) is reason able. For pat ien ts
m adin ) is in dicated for st roke preven t ion in pat ien t s w ith AF.45 cap able of engaging in p hysical act ivit y, at least 30 m in utes of
For pat ien ts w ith AF at h igh st roke risk (st roke or TIA w ith in 3 m oderate- in ten sit y physical exercise, defin ed as vigorou s act iv-
m on th s, a CHADS2 score of 5 or 6, m ech an ical or rh eu m at ic valve it y sufficien t to break a sw eat or raise h eart rate, on e to th ree
disease) w h o require tem porar y in terr u pt ion of oral an t icoagu - t im es per w eek m ay redu ce risk factors an d com orbid con dit ion s
lat ion , bridging th erapy w ith a low -m olecu lar-w eigh t h ep arin th at in crease th e likelih ood of recu rren t st roke.
(LMW H) adm in istered su bcu tan eou sly is reason able.45
A special m en t ion of VB dissect ion is w arran ted. Clin ical equi-
poise exists bet w een th e u se of an t ip latelet th erapy an d an t i-
coagu lat ion in VAD an d ICAD.48 Cu rren tly, n o ran dom ized t rials ■ Surgical Treatment
exist to est ablish th e su periorit y of eith er th erapy. In a m et a-
an alysis of 34 n on ran dom ized st udies (n = 762), th ere w as n o Endovascular Surgery
differen ce in th e risk of st roke or death in th ose pat ien ts w ith In add it ion to m edical th erapy, opt ion s for VBOD t reat m en t in -
VAD or ICAD receiving eith er an t iplatelet or an t icoagu lan t th er- clu de en dovascu lar st rategies to augm en t cerebral blood flow to
apy.49 In th e absen ce of a ran dom ized clin ical t rial, t reat m en t isch em ic areas. Th e tech n ical det ails of en dovascu lar t reat m en t
w ith either an anticoagulant (heparin, LMW H, or Coum adin) or a of VBOD are discussed in an oth er ch apter. Here, w e review th e
platelet in h ibitor (asp irin , clop idogrel, or asp irin plu s exten ded- literat ure com p aring m edical m an agem en t to en dovascular sur-
release dipyridam ole) for at least 3 to 6 m on th s is reason able for ger y. Eviden ce from clin ical t rials such as th e Warfarin -Aspirin
pat ients w ith VAD an d isch em ic st rokes or TIAs.48 Sym ptom at ic In t racran ial Disease Trial (WASID),50 w h ich docu-
m en ted a h igh rate of recurren t st rokes in th e territor y of a ste-
n ot ic in t racran ial ar ter y w ith m edical th erapy alon e, provides
Lipid-Low ering Agents som e eviden ce su p p or t ing in ter ven t ion in th ese p at ien t s. How -
Isch em ic st roke or TIA pat ien t s w ith elevated ch olesterol, coro- ever, m ost of th e literat ure on en dovascular t reat m en t of VBOD
n ar y ar ter y disease, or any eviden ce of an ath erosclerosis sh ould con sist s of sm all case series an d rep or t s. On e recen t clin ical t rial,
be m an aged accord ing to t h e Nat ion al Ch olesterol Ed u cat ion the Stenting versus Aggressive Medical Managem ent for Prevent-
Program (NCEP III) gu id elin es, w h ich in clu d e lifest yle m od ifi- ing Recurrent stroke in Intracranial Stenosis (SAMMPRIS),51 found
cat ion , d iet ar y gu id elin es, an d m ed icat ion recom m en dat ion s.45 th at in pat ien t s w ith sym ptom at ic in t racran ial at h erosclerosis,

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286 III Ischemic Stroke and Vascular Insufficiency

th e best m edical t h erapy w as su perior to angiop last y an d sten t- Am ong th e m ost com m on ly ut ilized self-expan ding sten t is
ing. Alth ough th is t rial provides eviden ce for aggressive m edical th e Wingsp an device (Boston Scien t ific, Marlborough , MA). Th e
m an agem en t in th ese pat ien ts, it rem ain s ch allenging to ext rap - data supporting the safet y and efficacy of this device cam e from a
olate th e results of th is st udy to all pat ien ts w ith sym ptom at ic series of patients w ith sym ptom atic intracranial stenosis (50–99%)
VBOD. At m any instit ut ions, endovascular treatm ent of VBOD has w h o h ad recurren t isch em ic even t s w h ile on an t ith rom bot ic
becom e a viable, if n ot rout in e, t reat m en t opt ion . En dovascular th erapy.71 Sten t deploym en t w as su ccessful in 44 of 45 pat ien ts
t reat m en t opt ion s in clu d e an giop last y alon e or an giop last y in (98%) w ith a periprocedural st roke/death rate of 4.4%. Th e 1-year
com bin at ion w ith sten t ing (eith er balloon - or self-expan ding). rate of ip silateral st roke/d eat h w as 9.3% (fou r of 43 p at ien t s).
Im p or tan tly, on ly th ree of 40 pat ien ts (7.5%) h ad a resten osis at
6 m on th s an d n on e w as sym ptom at ic.71 Th e Wingspan sten t w as
Angioplasty Alone u t ilized in th e SAMMPRIS t rial,51 w h ich invest igated w h eth er an -
gioplast y an d sten t ing w as superior to best m edical m an age-
Sundt et al52 provided an initial report in 1980 of balloon-assisted
m en t (asp irin 325 m g an d clop idogrel 75 m g daily for th e first
angioplast y for sym ptom at ic BA sten osis. Sin ce th at t im e, n u-
90 days, in addit ion to aggressive lip id- an d BP-low ering agen ts)
m erou s groups h ave reported using angioplast y as a st an d-alon e
in p at ien ts w ith sym ptom at ic in t racran ial sten osis. Th is t rial w as
th erapy for th e t reat m en t of VBOD.52–56 Ret rospect ive case series
h alted in 2011 ow ing to th e greater th an expected 30-day m or-
docum ent a reduct ion of sten osis (< 50%of baseline) in m ore than
bidit y an d m ort alit y in th e sten t ing group an d a low er th an ex-
80% of pat ien t s, w ith a rate of st roke or death var ying bet w een
pected st roke rate in th e m edical grou p. Overall, 14% of p at ien t s
4%and 40%.54,56–63 Lim ited data exist on long-term outcom es after
ran dom ized to sten t ing h ad a st roke or died 30 days after th e
in t racran ial angioplast y, but post procedu ral resten osis rates are
procedure, w hereas the 30-day risk of stroke or death in the m edi-
sign ifican t (24–40%).59 A repor t of p at ien t s u n dergoing in t racra-
cal grou p w as 5.8%. Th e risk of recu rren t st roke after 30 days w as
n ial angioplast y (n = 120) docu m en ted an an n u al st roke rate of
n o differen t bet w een th e t w o t reat m en t arm s. Th e st udy invest i-
4.4% (3.2% in th e territor y of sten osis).64 Given th e lim ited n u m -
gators con clu ded th at best m edical th erapy w as su p erior to an -
ber of pat ien ts, it s ret rospect ive design , an d th e lack of adjudica-
gioplast y an d sten t ing in th is patien t coh or t .
t ion of even ts by a n eu rologist , it is difficu lt to derive a precise
Th e Carot id an d Vertebral Arter y Tran slu m in al Angiop last y
an n ual st roke rate from th is st u dy alon e.
St u dy (CAVATAS) w as a ran dom ized clin ical t rial th at com pared
outcom es of pat ien ts w ith sym ptom at ic ICA or VA sten osis after
en dovascu lar th erapy w ith best m ed ical t h erapy alon e. In t h ose
Angioplasty w ith Stenting pat ien ts w ith sym ptom at ic VA sten osis ran dom ized to en dovas-
Given the tendency for elastic plaque recoil follow ing intracranial cular t reat m en t , successfu l in ter ven t ion s occurred in 100% w ith
angioplast y, this technique is com m only com bined w ith sten t ing no perioperative strokes or deaths.72 However, the subgroup anal-
to prevent stenosis of the paren t vessel. Data from a m eta-analysis ysis failed to sh ow a ben efit for en dovascu lar t reat m en t for VA
com p aring th ese t w o tech n iqu es sh ow ed th at th e 1-year st roke sten osis. Desp ite sm all p at ien t n u m bers, th is st u dy rep resen t s
an d death rates w ere low er w ith angioplast y w ith sten t ing th an th e on ly ran dom ized t rial com paring en dovascular th erapy w ith
w ith angioplast y alon e.65 Tech n ical success, com plicat ion rates, best m edical th erapy for VA sten osis.
an d sym ptom at ic resten osis rates ap p ear sim ilar bet w een t h e Curren tly un d er w ay is a m u lt icen ter, ran dom ized t rial, th e
t w o tech n iqu es.66 Alth ough th e prep on deran ce of dat a suggest s Ver tebral Ar ter y Sten t ing Trial (VAST), design ed to com pare best
th at in t racran ial sten t ing can be p erform ed w ith h igh safet y an d m edical m an agem en t w ith or w ithou t VA sten t ing in pat ien ts
efficacy, th ese repor ts h ave m ostly been lim ited to single-cen ter w ith recen tly sym ptom atic VA stenosis (≥ 50%). Prim ar y outcom e
case series.67–69 More recen t st u dies suggest th at st roke rates in m easures are any perioperat ive st roke, death , or n on fat al MI. We
pat ien ts w ith in tracran ial sten osis m ay be low er after sten t ing en th u siast ically aw ait th e resu lt s of th is im por t an t t rial to delin -
th an w as p reviou sly rep or ted w ith m edial th erapy alon e in th e eate the safet y and efficacy of VA stenting in this patient cohort.73
WASID st u dy.
Th e safet y an d efficacy of a balloon -expan dable, bare-m et al
stent for the treatm ent of intracranial stenosis (Neurolink, Guidant
Cerebrovascular Bypass
Cor p ., In d ian ap olis, IN) w as recen t ly invest igated in a m u lt i- For pat ien ts w ith h em odyn am ic cerebral isch em ia involving th e
cen ter ph ase I t rial, th e Sten t ing of Sym ptom at ic Ath erosclerot ic posterior circu lat ion , su rgical revascu larizat ion of th e sten osed/
Lesion s in th e Ver tebral or In t racran ial Ar teries (SSYLVIA).70 Th is diseased segm en t m ay be a th erap eu t ic con siderat ion . Alth ough
st u dy w as design ed to evalu ate t h e safet y an d perform an ce of th e m ajorit y of byp ass procedu res are perform ed to provide
sten t ing in 61 pat ien t s w ith in t racran ial ar terial sten osis, ver te- revascu lar izat ion of t h e carot id circu lat ion , tech n ical su ccess
bral pre–posterior in ferior com m un icat ing ar ter y (PICA) sten o- involving th e p oster ior circu lat ion h as been rep or ted . Byp ass
sis, or ver tebral ost iu m sten osis of 50% or m ore. Su ccessfu l sten t opt ion s for augm en t ing flow to th e basilar apex in clu de u sing
dep loym en t occu rred in 95% of pat ien ts. With in 30 days of post- th e su p erior tem p oral ar ter y (STA) as th e don or ar ter y an d eith er
sten t ing, fou r of 55 (7.3%) p at ien t s w ith in t racran ial or p re-PICA t h e su p er ior cerebellar ar ter y (SCA) or p oster ior cerebellar ar-
sten osis exp erien ced a st roke (30-day rate 7.2%). Th e frequ en cy ter y (PCA) as t h e recip ien t vessel.7 4 Pat ien t s h arbor in g p roxim al
of st roke w ith in 1 year w as 10.9%(six of 55 pat ien ts). Not ably, all VA disease m ay requ ire eith er an occip ital ar ter y to PICA byp ass
st rokes w ere in th e territor y of th e t reated ar ter y. Recurren t ste- or a sid e-to -sid e PICA byp ass. Tech n ical d et ails on t h e su rgical
n osis (≥ 50%) at 6 m on th s w as docu m en ted in 18 of 51 (35%) m an agem en t of VBOD are d iscu ssed elsew h ere.75 Here, w e re-
pat ien ts. Factors associated w ith resten osis w ere diabetes m elli- view t h e literat u re com p ar in g m ed ical m an agem en t to byp ass
t us, sm all vessel diam eter, an d post p rocedu ral sten osis of > 30%. surger y.

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Mu lt ip le sm all ret rosp ect ive case series h ave docu m en ted th e vs 2.0%, resp ect ively). A secon d repor t det ailing th e su rgical re-
safet y an d efficacy of direct ext racran ial to in t racran ial (EC-IC) su lts of th e EC–IC byp ass p rocedu res in COSS sh ow ed th at th e
bypass for patients w ith sym ptom atic in tracranial stenosis. How - su rgical grou p exh ibited (1) h igh rates of byp ass graft paten cy
ever, th e m ajorit y of th ese st udies in clu de pat ien ts w ith h etero- (96% on last follow -up exam in at ion ), (2) im proved cerebral h e-
geneous disease processes, w hereas the m inorit y include patients m odyn am ics, an d (3) low er rates of recu rren t ipsilateral st roke
w ith sym ptom at ic, m edically refractor y in t racran ial ath eroscle- after postoperative day 2 as com pared w ith the nonsurgical group
rosis. Wein stein et al76 w ere th e first to report surgical results of (9% vs 22.7% at 2 years, respect ively).79
EC–IC byp ass in pat ien ts exclusively w ith sym ptom at ic isch em ic An altern at ive approach to direct surgical revascu larizat ion is
in t racran ial ath erosclerosis. In th eir series of 105 pat ien ts, th ey an in direct bypass, w ith th e goal of prom ot ing in creased collat-
obser ved a graft paten cy rate of 97% w ith a perioperat ive m or- eral blood su pp ly to th e isch em ic region over t im e. In th eir co-
bidit y an d m or talit y of 2.8% an d 1%, respect ively. For long-term h ort of pat ien ts w ith sym ptom at ic in t racran ial ath ero-occlu sion
ou tcom es, t h ey obser ved a late st roke rate of 1.5% p er year—a (as m easu red by single ph oton em ission com puted tom ography
rate th at is favorable com pared w ith th e n at u ral h istor y of m edi- [SPECT] w ith acet azolam ide ch allenge) t reated by eith er en cep h -
cally t reated p at ien ts. alodu roar teriosyn angiosis or m ult iple bur h oles, Kom otar et al80
Th e st u dy to m ost profou n dly affect t h e su rgical m om en t u m rep or ted a p er iop erat ive m orbid it y an d m or t alit y rate of 27%
of EC–IC bypass surger y w as th e EC–IC Bypass Trial.70 Th is pro- an d 0%, respect ively. On late follow -u p im aging w ith SPECT, on ly
spect ive, ran dom ized t rial invest igated w h eth er EC–IC bypass t w o pat ien t s developed in creased perfusion (relat ive to baselin e)
plu s best m edical th erapy w as su perior to m edical th erapy alon e w h ereas five suffered repeat isch em ic in farct ion s. Com paring
in p at ien t s w ith isch em ic in t racran ial ath ero-occlu sive disease. th eir su rgical resu lt s w ith a m et a-an alysis of m edically t reated
Eligible pat ien ts experien ced on e or m ore TIAs or m in or isch - pat ien ts w ith sym ptom at ic carot id occlu sion an d h em odyn am ic
em ic st rokes w ith in 3 m on th s of en rollm en t , an d dem on st rated cerebral isch em ia, t h e au t h ors fou n d t h at in d irect byp ass p ro-
eviden ce of com plete carot id occlusion or h igh -grade sten osis. vided n o p rotect ion again st su bsequen t isch em ic st roke.80
Th e st u dy resu lt s sh ow ed a byp ass p aten cy rate of 96%, p eriop -
erat ive t ran sien t isch em ic sym ptom rate of 12.2%, p eriop erat ive
m ajor st roke rate of 4.5%, an d perioperat ive m ortalit y rate of
1.1%. Min or an d m ajor perioperat ive st rokes w ere h igher in pa-
t ien ts ran dom ized to EC–IC bypass su rger y th an in p at ien t s re-
■ Conclusion
ceiving m edical th erapy alon e. Th ese st rongly n egat ive results Sym ptom atic VBOD significantly contributes to the rapidly grow -
led to a w idesp read redu ct ion in EC–IC bypass su rger y. ing fiscal, em ot ion al, an d societ al h ealth burden of st roke in th e
On e m ajor crit icism of th e EC–IC Bypass Trial w as th e lack of Un ited States, both as a prim ar y cause of isch em ic st roke an d as
assessm en t of cerebral h em odyn am ics to iden t ify a subgrou p of a secon dar y source of recurren t isch em ic even ts. Modern m in i-
pat ien ts w ith redu ced cerebral blood flow w h o m ay ben efit from m ally invasive im agin g tech n iqu es facilit ate t h e accu rate d iag-
su rger y. Th e Carot id Occlu sion Su rger y St u dy (COSS)78 w as fash - n osis of VBOD an d th e oppor t un it y for effect ive t reat m en ts. At
ion ed to an sw er th is qu est ion . It w as a prosp ect ive, ran dom ized presen t , su bstan t ial eviden ce su p p or ts an t iplatelet th erapy over
t reat m en t t rial aim ed at test ing w h eth er EC–IC byp ass, in addi- an t icoagulat ion for th e preven t ion of recu rren t st rokes in sym p -
t ion to best m edical th erapy, redu ces recurren t ip silateral isch - tom at ic VBOD. Eviden ce from SAMMPRIS suggests th at angio-
em ic even t s in p at ien t s w ith recen tly sym ptom at ic ICA occlu sion p last y an d sten t p lacem en t sh ou ld n ot be recom m en d ed p r ior
an d h em odyn am ic cerebral isch em ia as m easured by oxygen ex- to aggressive m edical m an agem en t . Moreover, both direct an d
t ract ion fract ion (OEF) on p osit ron em ission tom ography (PET). in direct surgical bypass p rocedu res for p at ien t s w ith sym ptom -
Th e resu lt s of th is st udy sh ow ed th at th e 2-year rates for ipsilat- at ic VBOD are n ot su p por ted by clin ical t rials to date. We rem ain
eral st roke recu rren ce w ere sim ilar for th e su rgical an d n on su r- cautiously opt im istic th at as novel tech nologies and surgical tech -
gical groups (21.0%vs 22.7%, respect ively). Also, th e 30-day even t n iques evolve, select pat ien t subgrou ps m ay be iden t ified th at
rate for ipsilateral isch em ic st roke w as sign ifican t ly h igh er in th e ben efit from th ese in ter ven t ion s. How ever, th ese in ter ven t ion s
su rgical grou p as com pared w ith th e n on su rgical grou p (14.4% w ill n eed to be validated in ran dom ized clin ical t rials.

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2011;42:227–276 rosurger y 2002;51:23–27, discu ssion 27–29
46. Adam s RJ, Albers G, Alber t s MJ, et al; Am erican Hear t Associat ion ; Am eri- 63. Gupt a R, Schu m ach er HC, Mangla S, et al. Urgen t en dovascular revascu lar-
can St roke Associat ion . Update to th e AHA/ASA recom m en dat ion s for th e izat ion for sym ptom at ic in t racran ial ath erosclerot ic sten osis. Neurology
preven t ion of st roke in pat ien t s w ith st roke an d t ran sien t isch em ic at- 2003;61:1729–1735
t ack. St roke 2008;39:1647–1652 64. Marks MP, Wojak JC, Al-Ali F, et al. Angioplast y for sym ptom at ic int ra-
47. Ch im ow it z MI, Lyn n MJ, Derdeyn CP, et al; SAMMPRIS Trial Invest igators. cran ial sten osis: clinical outcom e. St roke 2006;37:1016–1020
Sten t ing versu s aggressive m edical th erapy for in t racran ial ar terial sten o- 65. Siddiq F, Mem on MZ, Vazquez G, Safdar A, Quresh i AI. Com parison be-
sis. N Engl J Med 2011;365:993–1003 t w een prim ar y angioplast y an d sten t placem en t for sym ptom at ic in t ra-
48. Brot t TG, Halperin JL, Abbara S, et al. ASA/ACCF/AHA/AANN/AANS/ACR/ cranial atherosclerot ic disease: m eta-analysis of case series. Neurosurger y
ASNR/CNS/SAIP/SCAI/SIR/SNIS/SVM/SVS guidelin e on the m an agem en t 2009;65:1024–1033, discussion 1033–1034
of pat ien t s w ith ext racran ial carot id an d ver tebral ar ter y disease: execu- 66. Jiang W J, Xu XT, Du B, et al. Long-term outcom e of elect ive sten t ing for
t ive sum m ar y: a report of th e Am erican College of Cardiology Foun da- sym p tom at ic in t racran ial ver tebrobasilar sten osis. Neu rology 2007;68:
t ion /Am erican Heart Associat ion Task Force on pract ice guidelines, an d 856–858
th e Am erican St roke Associat ion , Am erican Associat ion of Neu roscien ce 67. Gom ez CR, Misra VK, Cam pbell MS, Soto RD. Elect ive sten t ing of sym p -
Nu rses, Am erican Associat ion of Neu rological Su rgeon s, Am erican Col- tom at ic m iddle cerebral ar ter y sten osis. AJNR Am J Neuroradiol 2000;
lege of Radiology, Am erican Societ y of Neuroradiology, Congress of Neu- 21:971–973
rological Surgeons, Societ y of Ath erosclerosis Im aging and Preven t ion , 68. Gom ez CR, Misra VK, Liu MW, et al. Elect ive sten t ing of sym ptom at ic basi-
Societ y for Cardiovascular Angiography an d In ter ven t ions, Societ y of In - lar arter y sten osis. St roke 2000;31:95–99
ter ven t ional Radiology, Societ y of NeuroIn ter ven t ional Surger y, Societ y 69. Jiang W-J, Wang Y-J, Du B, et al. Sten t ing of sym ptom at ic M1 sten osis of
for Vascular Medicin e, an d Societ y for Vascu lar Surger y. St roke 2011;42: m iddle cerebral ar ter y: an in it ial experien ce of 40 pat ien t s. St roke 2004;
e420–e463 35:1375–1380
49. Men on R, Ker r y S, Nor r is JW, Marku s HS. Treat m en t of cer vical ar ter y 70. SSYLVIA St udy invest igators. Sten t ing of sym ptom at ic ath erosclerot ic le-
dissect ion : a system at ic review an d m et a-analysis. J Neurol Neu rosurg sion s in th e ver tebral or in t racran ial ar teries (SSYLVIA). St roke 2004;35:
Psych iat r y 2008;79:1122–1127 1388–1392
50. Ch im ow it z MI, Lyn n MJ, How let t-Sm ith H, et al; Warfarin -Aspirin Sym p - 71. Bose A, Har t m an n M, Hen kes H, et al. A n ovel, self-exp an d in g, n it in ol
tom at ic In t racran ial Disease Trial Invest igators. Com p arison of w arfarin sten t in m ed ically refractor y in t racran ial at h erosclerot ic sten oses: t h e
an d aspirin for sym ptom at ic in t racran ial ar terial sten osis. N Engl J Med Wingspan st udy. St roke 2007;38:1531–1537
2005;352:1305–1316 72. Cow ard LJ, McCabe DJ, Ederle J, Feath erstone RL, Clifton A, Brow n MM;
51. Ch im ow it z MI, Lyn n MJ, Derdeyn CP, et al; SAMMPRIS Trial Invest igators. CAVATAS Invest igators. Long-term outcom e after angioplast y an d sten t-
Sten t ing versu s aggressive m edical th erapy for in t racran ial ar terial sten o- ing for sym ptom at ic vertebral ar ter y sten osis com pared w ith m edical
sis. N Engl J Med 2011;365:993–1003 t reat m en t in th e Carot id An d Ver tebral Ar ter y Tran slum in al Angioplast y
52. Sun dt T Jr, Sm ith H, Cam pbell J, Vliet st ra R, Cucch iara R, St an son A. Tran s- Study (CAVATAS): a ran dom ized trial. Stroke 2007;38:1526–1530
lum in al angioplast y for basilar arter y sten osis. Mayo Clin Proc 1980;55: 73. Com pter A, van der Worp HB, Sch on ew ille W J, et al. VAST: Ver tebral Ar-
673–680 ter y Sten t ing Trial. Protocol for a ran dom ised safet y an d feasibilit y t rial.
53. Ah uja A, Guterm an LR, Hopkin s LN. Angioplast y for basilar ar ter y ath ero- Trials 2008;9:65
sclerosis. Case repor t . J Neurosurg 1992;77:941–944 74. Kalan i MY, Hu YC, Sp et zler RF. A d ou ble-bar rel su p er ficial tem p oral
54. Higash ida RT, Tsai FY, Halbach VV, et al. Tran slum in al angioplast y for ath - ar ter y-to-su p erior cerebellar ar ter y (STA-SCA) an d STA-to-p oster ior ce-
erosclerot ic disease of th e ver tebral and basilar ar teries. J Neurosurg rebral ar ter y (STA-PCA) bypass for revascularizat ion of th e basilar apex.
1993;78:192–198 J Clin Neu rosci 2013;20:887–889
55. Higash ida RT, Hieshim a GB, Tsai FY, Halbach VV, Norm an D, New ton TH. 75. Kalan i MY, Zabram ski JM, Nakaji P, Spet zler RF. Bypass an d flow redu ct ion
Translum in al angioplast y of th e vertebral an d basilar ar ter y. AJNR Am J for com plex basilar an d ver tebrobasilar jun ct ion an eur ysm s. Neurosur-
Neuroradiol 1987;8:745–749 ger y 2013;72:763–775, discussion 775–776
56. Takis C, Kw an ES, Pessin MS, Jacobs DH, Caplan LR. In t racran ial angio- 76. Wein stein PR, Rodriguez y Baen a R, Ch ater NL. Resu lt s of ext racran ial-
plast y: exp erien ce an d com plicat ion s. AJNR Am J Neu roradiol 1997;18: in t racranial arterial bypass for in t racran ial in tern al carot id arter y steno-
1661–1668 sis: review of 105 cases. Neu rosurger y 1984;15:787–794
57. Clark W M, Barnw ell SL, Nesbit G, O’Neill OR, Wyn n ML, Cou ll BM. Safet y 77. Group TEIBS; Th e EC/IC Bypass St udy Group. Failu re of ext racran ial-in t ra-
an d efficacy of p ercu t an eou s t ran slu m in al angioplast y for in t racran ial cran ial ar ter ial byp ass to red u ce t h e r isk of isch em ic st roke. Resu lt s of an
ath erosclerot ic sten osis. St roke 1995;26:1200–1204 internation al random ized trial. N Engl J Med 1985;313:1191–1200
58. Marks MP, Marcellus M, Norbash AM, Stein berg GK, Tong D, Albers GW. 78. Pow ers W J, Clarke W R, Gru bb RL Jr, Videen TO, Adam s HP Jr, Derdeyn CP;
Ou tcom e of angiop last y for ath erosclerot ic in t racran ial sten osis. St roke COSS Invest igators. Ext racran ial-in t racran ial byp ass su rger y for st roke
1999;30:1065–1069 preven t ion in h em odyn am ic cerebral isch em ia: th e Carot id Occlu sion
59. Con n ors JJ III, Wojak JC. Percut an eou s t ran slum in al angioplast y for in t ra- Surger y St udy random ized t rial. JAMA 2011;306:1983–1992
cran ial ath erosclerot ic lesion s: evolu t ion of tech n iqu e an d sh ort-term 79. Gr ubb RL Jr, Pow ers W J, Clarke W R, Videen TO, Adam s HP Jr, Derdeyn CP.
resu lt s. J Neu rosu rg 1999;91:415–423 Surgical result s of th e Carot id Occlusion Surger y St udy. J Neurosurg 2013;
60. Alazzaz A, Th orn ton J, Alet ich VA, Debru n GM, Au sm an JI, Ch arbel F. In t ra- 118:25–33
cran ial p ercu t an eou s t ran slu m in al angiop last y for ar teriosclerot ic sten o- 80. Kom ot ar RJ, St arke RM, Ot ten ML, et al. Th e role of in direct ext racran ial-
sis. Arch Neurol 2000;57:1625–1630 in t racran ial bypass in th e t reat m en t of sym ptom at ic in t racran ial ath ero-
61. Nah ser HC, Hen kes H, Weber W, Berg-Dam m er E, Yousr y TA, Kü hn e D. occlusive disease. J Neurosurg 2009;110:896–904
In t racran ial ver tebrobasilar sten osis: an giop last y an d follow -u p . AJNR
Am J Neu roradiol 2000;21:1293–1301

Neurosurgery Books Full


23 Surgical Treatment of
Vertebrobasilar Insufficiency
Moham ed Sam y Elham m ady and Jacques J. Morcos

an d XII as w ell as th e den t ate ligam en t . In t radu ral bran ch es of


■ Relevant Anatomy th e VA in clu de th e PICA, th e an terior an d posterior sp in al ar ter
Vertebral Artery ies, an d p erforat ing bran ch es to th e olive an d in ferior cerebellar
pedu n cle. Occasion ally, th e VA m ay term in ate in a n orm al sized
Th e ver tebral ar ter y (VA) can be conven ien tly divided in to fou r PICA or m ay be hypoplast ic th rough ou t its course.
segm en t s. Th e first segm en t , also kn ow n as th e ext raosseou s or
V1 segm en t , cou rses from th e ar ter y’s origin to th e t ran sverse
foram en of th e cer vical ver tebra. Th e VA usually arises from th e Basilar Artery
posterosup erior w all of th e su bclavian ar ter y. It cou rses poste Th e BA origin ates at t h e pon tom ed u llar y su lcu s, ascen ds along
rior to th e an terior scalen e m u scle an d en ters th e t ran sverse for th e ven t ral su rface of th e p on s, an d term in ates n ear th e p on to
am en at C6, C5, or C7 in 90%, 7%, an d 3% of cases, resp ect ively.1 m esen cep h alic ju n ct ion . It su p p lies t h e p on s via m u lt ip le m e
An om alou s origin s of th e VA h ave been w ell recogn ized. In 5% of dian , p aram ed ian , an d lateral p on t in e perforat ing ar teries. Th e
cases, th e left VA arises directly from th e aor t ic arch .2 Sim ilarly, BA also gives rise to th e labyrin th in e ar teries an d th e p aired an
an om alous origin s of th e righ t VA from th e arch ,3 of both VAs terior in ferior cerebellar ar teries (AICAs) at th e m idpon t in e level
from th e arch ,4 an d of th e righ t VA from th e righ t com m on ca as w ell as th e paired superior cerebellar ar teries (SCAs) at th e
rot id ar ter y (CCA) 5 are som e of th e m any variat ion s th at h ave pon tom esen ceph alic ju n ct ion . Th e BA bifu rcates at th e level of
been reported. Other rare an om alies in clude VA duplicat ion or t h e in ter p ed u n cu lar cister n in to t h e p aired p oster ior cerebral
fen est rat ion .6 Th e left VA is dom in an t in 50%of cases; oth er w ise, ar ter ies (PCAs). Th e p oster ior t h alam op er forators ar ise from
th e righ t VA is dom in an t (25%) or codom in an t (25%).7 t h e top of th e basilar as w ell as th e proxim al PCAs an d con t ribu te
Th e secon d VA segm en t , also kn ow n as th e foram in al or V2 im port an t supply to th e rost ral m idbrain an d m edial dien ceph a
segm en t , star t s at th e t ran sverse foram en of C6 an d cou rses to lon . Th e posterior com m u n icat ing ar teries (PCoAs) con n ect to
th e t ran sverse foram en of C1. In th is segm en t th e VA in it ially as th e PCAs in fron t of th e cerebral p edu n cles, an d, in th e face of
cen ds in a ver t ical path th rough an osseou s ch an n el form ed by ver tebrobasilar occlusive disease, th ey can ser ve as im por tan t
th e foram in a t ran sversaria of C6 to C3. At t h e level of th e a xis th e sou rces of collateral flow eith er p roxim ally dow n th e basilar ar
VA t u rn s laterally as it p asses th rough th e t ran sverse foram en of ter y in a ret rograde fash ion or distally to th e supraten torial PCA
C2. Th e arter y th en ascen ds an d ru n s sligh tly an teriorly to pass territories.
th rough t h e C1 t ran sverse foram en . Bran ch es of th e V2 segm en t
in clude radiculom edu llar y ar teries, w h ich arise at th e levels of
Superficial Temporal Artery
C1 to C5; th e ar ter y of cer vical en largem en t , w h ich arises from
both VAs bet w een th e levels of C4 an d C6 an d an astom oses w ith Th e su perficial tem poral ar ter y (STA) is th e sm aller of th e t w o
th e an terior sp in al ar ter y; t h e an terior m en ingeal ar ter y; as w ell term in al bran ch es of th e extern al carot id ar ter y (ECA). Th e STA
as m uscu lar bran ch es. arises w ith in th e substan ce of th e parot id glan d posterior to th e
Th e th ird segm en t of th e VA, also kn ow n as th e ext rasp in al or n eck of t h e m an d ible. Th e ar ter y ascen ds as a con t in u at ion of
V3 segm en t , st ar t s from th e t ran sverse foram en of C1 an d en ds t h e ECA an d crosses th e p osterior root of th e zygom at ic process
at th e poin t w h ere th e ar ter y pierces th e du ra. After exit ing th e of th e tem poral bon e. Th e STA th en divides in to a sm aller fron tal
C1 t ran sverse foram en , t h e VA t u rn s posterom edially arou n d th e an d larger parietal bran ch . Th e fron tal bran ch courses superiorly
atlan to occip ital join t an d ru n s along th e p osterior arch of C1 in and anteriorly tow ard the forehead w here it anastom oses w ith the
t h e su lcu s ar ter iosu s. Th e ar ter y t h en cou rses in an an ter ior, su p raorbit al an d fron tal ar teries.9 Th e parietal bran ch courses
su per ior, an d m ed ial d irect ion to p ierce t h e p oster ior at lan to su p eriorly an d p osteriorly su perficial to th e tem p oralis fascia
occipital m em bran e an d dura at th e level of th e foram en m ag w h ere it an astom oses w ith th e cont ralateral STA as w ell as th e
n um . Bran ch es of th e V3 segm en t in clude an ext radural origin of p oster ior au r icu lar an d occip it al ar ter ies.9 Th e STA at t h e level
th e posterior in ferior cerebellar ar ter y (PICA) in 5 to 20%of cases of th e zygom a m easu res 1.93 m m (± 0.48 m m ).9 In a cadaveric
an d th e p osterior m en ingeal ar ter y.8 st u dy by Maran o et al,10 th e average diam eters of th e STA at th e
Th e fou r th segm en t of th e VA, also kn ow n as th e in t radu ral or level of t h e zygom a an d at t h e level of t h e STA bifu rcat ion w ere
V4 segm en t , describes t h e in t racran ial cou rse of th e VA. Th e ar 2.2 an d 1.9 m m , respectively. Th e average length s of th e fron tal
ter y ascen ds along th e an terior aspect of th e m edu lla an d join s an d parietal bran ch from th e zygom at ic arch to th e poin t th e ves
th e con t ralateral VA to form th e basilar ar ter y (BA) at th e pon to sel n arrow ed to 1 m m w ere 99.2 m m (range, 45–200 m m ) an d
m edu llar y ju n ct ion . It cou rses an terior to cran ial n er ves IX, X, XI, 106.0 m m (range, 35–163 m m ), resp ect ively.

290

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23 Surgical Treatment of Vertebrobasilar Insufficiency 291

Occipital Artery th e ar ter y r u n s p osteriorly arou n d th e m edu lla past t h e exit of


th e hyp oglossal n er ve rootlet s from th e an terior bord er of th e
Th e cou rse of th e occipit al ar ter y (OA) can be d ivided in to th ree
in ferior olivar y com plex to th e boun dar y bet w een th e an terior
segm en t s.11 Th e first segm en t , also kn ow n as th e digast ric seg
an d lateral surfaces of th e m edulla, w h ich is m arked by a rost ro
m en t , exten ds from th e origin of th e OA from th e ECA to th e
cau dal lin e th rough th e m ost prom in en t par t of th e in ferior olive.
poin t of em ergen ce from th e occip ital grove of th e m astoid p ro
Th e lateral m ed u llar y segm en t begin s at th e poin t th e PICA
cess. Th e OA origin ates from th e posterior or lateral w all of th e
passes th e m ost p rom in en t p ar t of th e in ferior olive an d exten ds
ECA at th e level of th e angle of th e m an dible. Th e ar ter y ascen ds
posteriorly arou n d th e lateral asp ect of th e m edu lla to th e origin
m edial to the ECA an d lateral to th e in tern al jugular vein to a
of th e glossoph ar yngeal, vagus, an d accessor y rootlets from th e
poin t posterior an d m edial to th e st yloid p rocess. Th e OA th en
posterior border of th e in ferior olivar y com plex. Th e PICA con
cou rses p osteriorly an d laterally su p erficial to t h e rect u s cap it is
t in u es m ed ially as th e ton sillom edu llar y segm en t bet w een th e
lateralis m u scle first an d th en th e sup erior obliqu e m u scle.12 Th e
low er h alf of th e cerebellar ton sil an d th e posterior asp ect of th e
ar ter y is covered by th e posterior belly of th e digast ric m uscle
m edu lla oblongat a. Th e ar ter y m akes a caudally convex cur ve as
laterally; h en ce it is kn ow n as th e digast ric segm en t . Th e arter y
it p asses arou n d t h e low er p ole of t h e cerebellar ton sil kn ow n
then runs in the occipital grove or occasionally a true bony canal11
as th e caudal or in fraton sillar loop. Th e caudal loop is frequen tly
m edial to th e m astoid n otch , in w h ich th e posterior belly of th e
u sed as a recipien t during OA–PICA bypasses, an d it s diam eter
digast ric m u scle arises.12
ranges from 0.9 to 1.4 m m (m ean 1.2 m m ).14
Th e secon d segm en t , also kn ow n as th e su boccip it al or h ori
After form ing th e caudal loop, th e PICA ascen ds to th e m id
zontal segm en t , exten ds from th e em ergen ce of th e OA from th e
level of th e m edial surface of th e ton sil, w h ere it becom es th e
occipital groove of th e m astoid process to th e superior n uch al
teloveloton sillar segm en t . Th e ar ter y con t in u es along th e m edial
lin e. Th e OA exit s th e occipit al groove bet w een th e superior
su rface of th e ton sil tow ard th e roof of th e fou r th ven t ricle. Th e
obliqu e m u scle an d posterior belly of th e digast ric an d is covered
PICA th en form s a rost rally convex cu r ve referred to as th e cra
by th e splen ium capit is an d stern ocleidom astoid. Th e ar ter y
n ial or supraton sillar loop. Th is loop con sists of proxim al ascen d
cou rses m edially in a h orizon t al p lan e eith er su p erficial or deep
ing an d dist al descen ding lim bs an d an ap ex t h at lies caudal to
to th e longissim u s cap it is m u scle depen ding on w h eth er th e oc
th e fast igiu m at th e cen ter of th e in ferior m edu llar y velu m . Th e
cipital groove is absen t or presen t . Th e OA th en con t in u es super
ascen ding lim b run s posterior to th e tela ch oroidea an d in ferior
ficial to th e sem ispin alis capit is m uscle just below th e superior
m edu llar y velum tow ard th e fast igium of th e fourth ven t ricle.
n uch al lin e in th e upper par t of th e posterior t riangle. Th e ar ter y
Th e descen ding lim b r u n s posteriorly in th e fissure bet w een th e
t h en ch an ges cou rse an d r u n s ver t ically u pw ard , p iercin g t h e
verm is m edially an d th e superom edial su rface of th e ton sil an d
fascia con n ect ing th e cran ial at t ach m en t of th e t rap eziu s an d
cerebellar h em isp h ere laterally. Th e PICA em erges from t h e fis
ster n ocleid om astoid m u scles to t h e su p er ior n u ch al lin e.13 Th e
su re an d con t in u es as t h e cor t ical segm en t . Th e ar ter y d ivides
su boccip it al segm en t gives r ise to ascen ding an d d escen ding
in to a sm aller m edial an d a larger lateral t ru n k an d subsequ en t ly
m uscular bran ch es as w ell as t ran sosseous bran ch es to th e dura
gives rise to h em isph eric, verm ian , an d ton sillar bran ch es. Th e
of th e posterior fossa. Th e diam eter of th e suboccipital segm en t
PICA h as th e follow ing bran ch es: (1) perforat ing ar teries to th e
ranges from 1.6 to 2.2 m m (m ean 1.9 m m ) an d th e length ranges
brain stem from th e an terior m edullar y, lateral m edu llar y, an d
from 75 to 85 m m (m ean 79.3 m m ).14
tonsillom edullar y segm en ts; (2) ch oroidal bran ch es to th e tela
Th e th ird segm en t , also kn ow n as th e occip it al or su bgaleal
ch oroid ea an d ch oroid plexu s of th e fou r th ven t ricle from th e
segm en t , begin s at th e su perior n u ch al lin e after th e OA pierces
tonsillom edullar y an d teloveloton sillar segm en ts an d to a lesser
th e fascial at t ach m en t of th e t rap eziu s an d stern ocleidom astoid
exten t from t h e lateral m ed u llar y segm en t; an d (3) cor t ical
m uscles. In a cadaveric st u dy, th e OA w as fou n d to cross th e su
bran ch es th at supply th e ipsilateral suboccipital surface of th e
perior n u ch al lin e 35 m m (± 0.5 m m ) lateral to th e in ion .11 Th e
cerebellu m , ton sil, an d verm is.
ar ter y con t in ues un dern eath th e galea an d above th e occipit al
m u scle before divid ing in to it s term in al bran ch es. Th e diam eter
of th e OA at th e su perior n u ch al lin e is 1.4 m m (± 0.3 m m ).11 Anterior Inferior Cerebellar Artery
Th e AICA arises from th e proxim al BA as a single t r u n k an d oc
casion ally as du plicated or t rip licated ar teries. Th e AICA th en
Posterior Inferior Cerebellar Artery en circles th e pon s tow ard th e cerebellop on t in e angle (CPA),
It is ver y conven ien t to subscribe to th e con cept advan ced by w h ere it cou rses eit h er above or below cran ial n er ve VI. Th e
Lister et al,15 t h at t h e PICA can be d ivid ed in to five segm en t s ar ter y th en passes n ear t h e in tern al au ditor y can al w h ere it
based on its relat ion sh ip to th e m edu lla an d th e cerebellum : an gives off bran ch es to th e cran ial n er ve VII–VIII com p lex as w ell
terior m edu llar y, lateral m edu llar y, ton sillom edu llar y, telovelo as t h e ch oroid p lexu s at t h e foram en of Lu sch ka. Th e ar ter y t h en
ton sillar, an d cort ical. p asses arou n d t h e floccu lu s an d con t in u es over t h e p et rosal su r
Th e an terior m edu llar y segm en t begin s at th e origin of t h e face of t h e cerebellu m . Th e ar ter y d ivid es in to rost ral an d cau dal
PICA from th e VA an terior to th e m edu lla oblongata. Congen ital bran ch es eit h er before or after crossing cran ial n er ves VII an d
an om alies of th e PICA in clu de dou ble origin , fen est rat ion , or d u VIII. Th e AICA is divided in to fou r segm en t s: an terior pon t in e,
plicated PICAs, a com m on AICA–PICA con figu rat ion , a VA term i lateral p on t in e, floccu lon od u lar, an d cor t ical.13 In a cadaver ic
n at ion at th e PICA, ext radu ral origin s at C1 an d C2 levels, origin s st u dy by Kaw ash im a an d colleagu es,13 th e m ean diam eters of th e
at th e hypoglossal, proatlan tal, or posterior m en ingeal ar teries, an terior p on t in e an d cor t ical segm en t s w ere 1.34 an d 1.07 m m ,
an d at all poin ts along th e in t radural VA.8,16–21 From it s origin , resp ect ively.

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292 III Ischemic Stroke and Vascular Insufficiency

Superior Cerebellar Artery volve both th e ext racran ial vessels (aor t ic arch , subclavian ar
ter y, VA) as w ell as th e in t racran ial ver tebrobasilar system . Ath
Th e SCA or igin ates from t h e d ist al BA at t h e p on tom esen ce
erosclerosis m ay also affect bran ch es of t h e VA an d BA. AICA
p h alic jun ct ion . Alth ough th e ar ter y usually arises as a single
occlusion s are frequ en tly a resu lt of in sit u ath eroth rom bosis.
t ru n k, it m ay also be du p licated. Th e ar ter y cou rses arou n d th e
PICA occlu sion s are equ ally divid ed bet w een in sit u at h ero
brain stem , first below t h e ocu lom otor n er ve an d t h en below
th rom bosis an d cardioem bolic p h en om en a. SCA occlu sion s are
t h e ten toriu m . It is divided in to fou r segm en t s.13 Th e an terior
m ost com m on ly cardioem bolic in n at u re.22 Th e p roxim al PCAs
pon tom esen ceph alic segm en t exten ds from th e SCA origin to th e
are also com m on sites of at h erosclerot ic disease. Th e m ech a
an terolateral m argin of th e brain stem an d m easures 1.67 m m .
n ism by w h ich ath erosclerot ic disease produces posterior circu
Th e lateral p on tom esen cep h alic segm en t begin s at th e an tero
lat ion isch em ia is eith er hyp operfu sion secon dar y to p rogressive
lateral m argin of th e brain stem an d en ds at th e an terior m argin
ar ter ial sten osis or t h rom boem bolic p h en om en on (or a com
of th e cerebellom esen ceph alic fissure. All SCAs that arise as a
bin at ion of th ese factors). Th rom bus propagat ion w ith in th e BA
single t r u n k d ivid e in to rost ral an d cau dal bran ch es. In t h e ca
is usually lim ited an d does n ot exten d beyond th e n ext long cir
daver ic st u dy by Kaw ash im a et al,13 t h e m ean d iam eters of t h e
cum flex cerebellar arter y (AICA or SCA). Em boli are m ost com
lateral p on tom esen cep h alic t r u n k an d t h e rost ral an d cau dal
m on ly fou n d at th e top of th e BA or PCAs. Th is can be exp lain ed
bran ch es w ere 1.51, 1.25, an d 1.15 m m , respect ively. Th e cere
by t h e fact t h at t h e d iam eter of t h e BA is u su ally larger t h an t h e
bellom esen ceph alic segm en t courses w ith in th e correspon ding
d iam eter of t h e in t racran ial VA, so t h at if an em bolu s is able
fissu re an d gives rise to perforat ing bran ch es to th e brain stem
to pass th rough th e VA, it w ill t ypically also t ravel un im peded
an d cerebellum . Th e cor t ical segm en t gives rise to distal bran ch es
th rough th e BA u n less th ere is proxim al lu m in al ath erosclerot ic
to th e ten torial su rface of th e cerebellu m .
sten osis. Alt h ough sm all p en et rat ing ar ter y occlu sion h as been
classically attributed to the process of lipohyalinosis, such vessels
Posterior Cerebral Artery can also be involved w ith m icroatherom as an d result in brain stem
in farct ion .
Th e PCAs arises at th e BA bifu rcat ion n ear th e pon tom esen ce
Th e n at u ral h istor y of ext racran ial VA ath erosclerosis is n ot
ph alic ju n ct ion . Th e PCAs th en en circle th e m esen cep h alon to
w ell kn ow n . In th e New Englan d Medical Center Posterior Circu
su p ply th e p osterior p or t ion of th e cerebral h em isp h ere. Th e
lat ion Regist r y, ext racran ial VA ath erosclerosis w as con sidered a
PCA is d ivid ed in to fou r segm en t s (P1 to P4). Th e P1 segm en t
con t ribu t ing factor in 10 to 20%of p osterior circu lat ion st rokes.23
exten d s from th e BA bifu rcat ion to th e p oin t w h ere th e PCoAs
In th e prospect ive ran d om ized Carot id An d Ver tebral Ar ter y
connect to the PCAs in front of the cerebral peduncles. The P2 seg
Tran slu m in al Angiop last y St u dy (CAVATAS), a tot al of 16 pat ien ts
m en t exten ds from th e PCoA to th e poin t w h ere th e PCA en ters
w ith sym ptom at ic ≥ 50%VA sten osis w ere ran dom ized to receive
th e qu adrigem in al cistern an d is fu r th er divid ed in to an terior
en d ovascu lar balloon angioplast y an d sten t ing or best m edical
(P2a) an d posterior (P2p) segm en ts by th e lateral m esen ceph alic
m an agem en t . Over th e m ean follow up period of 4.7 years, n o
su lcu s. Th e P3 segm en t cou rses th rough th e qu adrigem in al cis
pat ien t in eith er t reat m en t grou p exp erien ced a ver tebrobasilar
tern an d exten ds from th e posterior aspect of th e m idbrain to
st roke.24 Sim ilarly, in a ret rospect ive st u dy by Moufarrij et al,25
th e an terior lim it of th e calcarin e fissu re. Th e P4 segm en t con st i
96 pat ien t s w ith VA sten osis ≥ 50% w ere follow ed for an average
tutes the distal PCA branches. In the cadaveric study by Kawashim a
of 4.6 years. Th e VA origin w as involved in 89 (93%) pat ien t s.
et al,13 th e m ean diam eters of th e P2a, P2b, an d P3 segm en t s
During th e follow up period, 19 pat ien ts (19.8%) experien ced
w ere 2.13, 1.73, an d 1.67 m m , respect ively. Th e PCA gives rise to
possible sym ptom s of ver tebrobasilar in su fficien cy (VBI), n on e
th e follow ing bran ch es: (1) perforat ing bran ch es to th e m idbrain
of w h om h ad a st roke. On ly t w o pat ien ts suffered brain stem
an d dien ceph alon (th alam operforat ing, pedu n cular perforat ing,
st rokes (both fatal) an d w ere kn ow n to h ave BA sten osis in addi
and thalam ogeniculate arteries); (2) ventricular branches, such as
t ion to th eir VA sten osis.
th e lateral an d m edial p osterior ch oroidal ar teries, w h ich su p ply
Th e n at u ral h istor y of in t racran ial ver tebrobasilar ath eroscle
the choroid plexus of the atrium and th ird ventricle, respectively;
rosis disease is n ot as w ell st u died or un derstood as com pared
an d (3) cerebral bran ch es to th e posterior cerebral h em isph ere
w ith an terior circulat ion disease. Moufarrij an d colleagues 26 ret-
an d splen iu m (in ferior tem poral bran ch es, parietooccipital, cal
rosp ect ively follow ed 44 p at ien t s w ith ≥ 50%dist al VA an d/or BA
carin e, an d splen ial arteries).
sten osis for an average of 6.1 years. Du ring th e follow u p p eriod,
seven p at ien t s (16%) exp erien ced defin it ive sym ptom s of VBI,
w h ereas th ree pat ien t s experien ced possible VBI sym ptom s. Five
(11%) pat ien t s suffered a vertebrobasilar territor y st roke. Three
■ Pathophysiology and Natural History p at ien t s (7%) d ied secon dar y to st roke (t w o brain stem in farc
Ver tebrobasilar in sufficien cy results from in terru pt ion of blood t ion s an d on e in t raven t ricu lar h em orrh age). Based on th eir dat a
flow to th e posterior circu lat ion an d can be at t ribu ted to several from p roxim al VA occlu sive disease,25 th e auth ors con cluded th at
et iologies. dist al ver tebrobasilar occlu sive d isease carries a h igh er risk for
brain stem isch em ia. Th e Warfarin Aspirin Sym ptom at ic In t ra
cranial Disease (WASID) study group retrospectively analyzed the
Atherosclerotic Disease progn osis of p at ien ts w ith sym ptom at ic in t racran ial ver tebro
Ath erosclerosis is by far th e m ost com m on et iology respon sible basilar sten osis.27 A tot al of 68 pat ien t s w ith 50 to 99% sten osis
for posterior circulat ion isch em ia. Ath erosclerot ic lesion s can in of t h e in t racran ial VA (n = 31), BA (n = 28), PCA (n = 6), or PICA

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23 Surgical Treatment of Vertebrobasilar Insufficiency 293

(n = 3) w ere t reated w ith w arfarin (n = 42) or aspirin (n = 26) is th e term u sed for a sym ptom at ic steal p h en om en on . Th e first
over a m edian follow up of 13.8 m on th s. During th is t im e pe rep or t of a su bclavian steal p h en om en on w as by Con tor n i28 in
riod, 15 pat ien t s (22%) su ffered a recu rren t st roke of w h ich fou r 1960. Th e follow in g year, Reivich et al29 d escr ibed a case of
(27%) w ere fat al. Th e st roke rate in th e sam e territor y of th e ste sym ptom at ic su bclavian steal p h en om en on . Fish er coin ed t h e
n ot ic ar ter y per 100 pat ien t years of follow up w as 10.7 in pa term subclavian steal syndrom e in th e editorial discussion of th e
t ien ts w ith BA sten osis, 7.8 in p at ien t s w ith VA sten osis, an d 6.0 classic report by Reivich et al. Th e m ost com m on et iology of su b
in p at ien ts w ith PCA or PICA sten osis. clavian steal is at h erosclerot ic sten osis of t h e su bclavian ar ter y.
It is m ore com m on ly seen on th e left side an d is believed to be a
result of th e acu te angle of origin of th e left subclavian ar ter y,
Arterial Dissection w h ich m ay cause local t urbulen ce of blood flow an d su bsequ en t
Ar terial dissect ion can involve both th e VA an d BA. Posterior cir ath erogen esis.30–33 Oth er rare causes in clude large vessel vascu
culat ion isch em ia related to dissect ion m ost com m on ly involves lit is (eg, Takayasu or gian t cell ar terit is), ext rin sic com pression
th e ext racran ial VA. Th e d issect ion u su ally begin s above th e ori (costoclavicular syn drom e), iat rogen ic sten osis (e.g., radiat ion
gin of th e VA. It m ay occur follow ing n eck rot at ion /m an ipulat ion in d u ced), an d con gen it al vascu lar an om alies.34 Su bclavian steal
or t rau m a (blu n t or p en et rat in g), or sp on t an eou sly. VA d issec syn d rom e gen erally occu rs in t h e con text of exercise or u se of
t ion s h ave been associated w it h several con d it ion s in clu d in g t h e ip silateral u p p er ext rem it y an d m an ifest s w it h sym ptom s
Marfan’s syn drom e, Eh lers Dan los syn drom e, p seu doxan t h om a of VBI an d ip silateral u p p er ext rem it y isch em ia. Th e d iagn osis
elast icum , system ic lupus eryth em atosus, and fibrom uscular dys of subclavian steal can be suspected clin ically by th e presen ce of
plasia. In addit ion to sym ptom s of VBI, p at ien t s u su ally com p lain a bru it in th e region of th e su bclavian ar ter y and a differen ce in
of h eadach e an d n eck pain radiat ing to th e occiput or sh oulder. systolic blood pressu re of m ore th an 20 m m Hg bet w een th e
In farct s in th e PICA ter r itor y resu lt ing in a lateral m ed u llar y arm s.32,33,35 Th e p resen ce an d degree of su bclavian ar ter y sten o
syn drom e are n ot an in frequ en t occu rren ce. In t racran ial VA dis sis can be dem on st rated u sing com p u ted tom ograp hy angiogra
sect ion is less com m on th an ext racran ial VA dissect ion . Pat ien ts p hy (CTA) or m agn et ic reson an ce angiograp hy (MRA). Digit al
can p resen t w ith su barach n oid h em orrh age, isch em ia, or less subst ract ion angiograp hy, ult rason ography, or qu alit at ive m ag
com m on ly w ith m ass effect . Th e isch em ia m ay be du e to p aren t n et ic reson an ce im aging (MRI) can con firm reversal of VA blood
vessel occlusion , perforator occlu sion , or th rom boem bolic ph e flow.
n om en a. Hem orrh agic versus isch em ic presen tat ion is probably
related to w h ich layer of t h e ar ter ial w all t h e d issect ion occu rs Cardiac Emboli
in (subin t im al versu s subadven t it ial). In com parison w ith th e
VA, dissect ion of th e BA an d it s m ajor bran ch es is u n com m on . As Cardiac abn orm alit ies su ch as valvu lar disease, en docardit is, an d
w ith in t racran ial VA dissect ion , pat ien ts can presen t w ith h em dysrhyt h m ias are p ossible sou rces of em boli. As p reviou sly
orrh age, isch em ia, or m ass effect . m en t ion ed, em bolic m aterial is m ost often fou n d w ith in th e dis
tal BA t ributaries an d th e em boli usually affect th e cerebellar an d
occipit al lobes.
Compression
Com prom ise of blood flow th rough th e ext racran ial VA by exter
n al com pression can presen t clin ically as VBI in th e set t ing of a ■ Clinical Presentation
hypoplast ic, sten ot ic, or occluded con t ralateral vertebral ar ter y
w ith m in im al collaterals from th e an terior circulat ion . Offen ding Vertebrobasilar insufficiency is a term u sed to describe a m u lt i
lesion s in clu de th e an terior scalen e or longu s colli ten don s, fi t u de of sym ptom s secon dar y to in ad equ acy of blood su p ply to
brous ban ds, or th e sym path et ic ganglia or n er ve fibers along th e st r u ct u res su p p lied by t h e p osterior circu lat ion . Th e m ost com
V1 segm en t; sp on dylit ic osteop hytes or disk spu rs bet w een th e m on clin ical m an ifestat ion s of VBI are th e follow ing:
levels of C6 an d C2; or com p ression at th e level of C1–2, classi • Decreased con sciou sn ess
cally referred to as bow h u n ter’s syn drom e. Sym ptom s are u su • Syn cop e
ally t ran sien t an d frequ en tly t riggered by h ead rotat ion or n eck • Nau sea/vom it ing
exten sion . Occasion ally, th e low flow state m ay p rom ote th rom • Visu al field deficit
bus form at ion an d em boli. Dyn am ic angiography is ext rem ely • Pu pillar y abn orm alit ies
h elpful in dem on st rat ing in term it ten t extern al com pression by • Diplop ia/op h th alm op aresis
com p ar in g VA blood flow d u r in g inject ion s w it h t h e p at ien t ’s • Facial n u m bn ess/w eakn ess
h ead in n eut ral an d rotated p osit ion (Fig. 23.1). • Ver t igo/dizzin ess
• Hearing loss
• Horn er’s syn drom e
Subclavian Steal Syndrome • Dysar th ria/dysp h on ia
Su bclavian steal syn d rom e is a ben ign vascu lar h em odyn am ic • Dysp h agia
con d it ion ch aracterized by reversal of flow in th e VA du e to ste • Dysgeu sia
n osis or occlu sion of th e ipsilateral in n om in ate or subclavian ar • Gait/lim b ataxia
ter y proxim al to th e origin of th e VA. Subclavian steal syndrom e • Ext rem it y w eakn ess/n u m bn ess
(text cont inues on page 298)

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294 III Ischemic Stroke and Vascular Insufficiency

a b

c d

Fig. 23.1a–q A 57-year-old wom an presents with several m onths of syn- C6/7. (b,c) Coronal computed tomography angiography (CTA) shows atretic
copal at tacks anytime she turns her head more than 30 degrees to the right. left vertebral artery (VA), entrance of right VA at foram en transversarium of
She gives a vague history of neck traum a in the distant past with possible C6 with suggestion of at tenuation of caliber just distal to it. (d) Magnetic
nonoperative cervical spine fractures and no neurologic deficits. (a) Lateral resonance angiography (MRA) in neutral neck position also suggests some
cervical spine X-ray demonstrates congenital fusion (Klippel-Feil) at C2/3 and narrowing of right VA at the V1/V2 junction at C6.

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23 Surgical Treatment of Vertebrobasilar Insufficiency 295

e f

g h

Fig. 23.1a–q (continued ) (e,f) Left VA angiogram dem onstrates a sm all distal left V3 with som e contribution to basilar artery. (g,h) Right VA angiogram
(neutral neck position) dem onstrates good flow in spite of m ild distortion of right VA at C6. (continued on page 296)

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296 III Ischemic Stroke and Vascular Insufficiency

i j

k l

Fig. 23.1a–q (continued ) (i) Right VA angiogram (patient turning head to


the right) dem onstrates im mediate complete occlusion of right VA at C6.
(j) Right VA angiogram as soon as patient begins to return to neutral neck
position, dem onstrates reopening of right VA at C6. (k) Surgical treatm ent
via oblique right neck incision, approach to anterior spine with lateral m o-
bilization of longus colli. The right VA is exposed at C6/C7. C6/7 Klippel-
Feil is noted. (l) The right C6 foram en transversarium being opened with
m Kerrison rongeur. (m) The right VA becom es m ore prom inent.

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23 Surgical Treatment of Vertebrobasilar Insufficiency 297

n o

p q

Fig. 23.1a–q (continued ) (n) Fibrous band constricting VA in foramen grade flow. (q) Intraoperative right VA angiogram with passive head turn
transversarium being incised sharply. (o) After decompressing right foramina to the right fails to dem onstrate any extrinsic compression. Her positional
transversaria at C6 and C5, the VA is completely free and mobilizable. (p) In- syncope was cured postoperatively.
traoperative right VA angiogram in neutral position shows excellent ante-

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298 III Ischemic Stroke and Vascular Insufficiency

Table 23.1 Brainstem Syndrome

Syndrome Ipsilateral Signs Contralateral Signs

Midbrain
Weber CN III palsy Weakness
Claude CN III palsy Ataxia, trem or
Benedikt CN III palsy Weakness, ataxia, trem or
Nothnagel CN III palsy, ataxia Ataxia
Parinaud Paralysis of upward gaze, convergence-retraction Paralysis of upward gaze, convergence-retraction
nystagmus, lid retraction, and light-near dissociation nystagmus, lid retraction, and light-near dissociation
Pons
Raym ond-Céstan Internuclear ophthalm oplegia, CN VI Weakness, ataxia
Raymond Weakness
Ataxic-hem iparesis Weakness, ataxia
Millard-Gubler CN VI, VII Weakness
Foville CN VI and som etimes VII Weakness, sensory loss
Medulla
Wallenberg Loss of pain and temperature from the face; weakness Loss of pain and temperature from the body
of the soft palate, larynx, and pharynx; Horner
syndrom e; ataxia
Babinski-Nageot te Same as Wallenberg Same as Wallenberg’s + weakness
Cestan-Chenais Loss of pain and temperature from the face; weakness Loss of pain and temperature from the body, weakness
of the soft palate, larynx, and pharynx; Horner’s
syndrome
Reinhold’s Sim ilar to Cestan-Chenais + ataxia and CN XII Sim ilar to Cestan-Chenais
Avellis’ Weakness of the soft palate, larynx, and pharynx Loss of pain and temperature from the body
Jackson’s CN XII, weakness of the soft palate, larynx, and pharynx Weakness
Dejerine CN XII Weakness, and som etimes position and vibration sense
Abbreviation: CN, cranial nerve.

Several brain stem syn drom es h ave also been described an d


are su m m ar ized in Table 23.1. Th e p resen ce of bilateral m otor
■ Preoperative Evaluation
or sen sor y sym ptom s, cerebellar dysfun ct ion , an d cran ial n er ve Th e first step s in evalu at ing a p at ien t p resen t ing w ith isch em ia
palsies w ith crossed long t ract sign s are h allm arks of VBI. It of th e ver tebrobasilar system are obtain ing a th orough h istor y
sh ou ld be n oted th at vert igo an d dizzin ess alon e are n ot u su al an d doing a physical exam in at ion , w h ich facilitate establish ing
presen t ing sym ptom s of VBI, an d oth er cau ses sh ou ld be sough t . th e diagn osis of VBI an d th e exclu sion of oth er p ossible n on isch
Depen ding on th e et iology, sym ptom s m ay be t ran sien t or per em ic et iologies. It sh ou ld be rem em bered th at VBI is a vascu lar
m an en t , flu ct uat ing or progressive (t ypically in a stepw ise fash ph en om en on an d, as su ch , th e on set of sym ptom s is sudden .
ion ), m ild or severe, bu t alw ays su dd en an d episodic, reflect ing Preoperative evaluation includes standard preoperative labora
th e “vascu lar” n at u re of th e p roblem . In severe cases, w h ere th e tories, an electrocardiogram , a chest radiograph , and assessm en t
m ech an ism is “h em odyn am ic,” th e sym ptom s can be reproduc of th e pat ien t’s gen eral h ealth . Radiograph ic im aging in clu des
ible an d var y w ith ch anges in body posit ion an d blood pressu re. assessm en t of bot h t h e brain p aren chym a an d t h e ext ra an d
Sym ptom s associated w ith VBI are n um erous an d often vague. in t racran ial cerebrovascular system . Com puted tom ography (CT)
Th ey can be easily con fu sed w it h sym ptom s related to ot h er of th e h ead is an excellen t screen ing tech n ique for ruling out
system ic and neurologic diseases. In fection or dysfun ction of ves m ass lesion s or h em orrh age. Brain MRI is a m ore sen sit ive im ag
t ibu lar or labyrin th in e st ru ct u res (labyrin th it is, vest ibu lar n eu ing m odalit y an d can dem on st rate isch em ic injur y in th e terri
ronitis, Meniere’s disease, benign paroxysm al positional vertigo), tor y of th e posterior circulat ion an d rule out dem yelin at ing or
dem yelin at ing diseases, m igrain es, posterior fossa t u m ors (CPA m ass lesion s. CTA an d MRA are excellen t n on invasive screen ing
or in t ra axial cerebellar lesion s), Ch iari m alform at ion , an d spin al tools for evaluat ion of both th e ext ra an d in t racran ial cerebro
cord lesions can all present w ith VBI sym ptom s. Sim ilarly, cardiac vascu lar circulat ion . How ever, th eir abilit y to accurately defin e
diseases th at resu lt in decreased cardiac ou t p u t (dysrhyth m ias, th e exten t of ar terial sten osis is lim ited, bu t m ore im p or t an tly
in farct ion ) or presen t as a sou rce of th rom boem boli (valvular th ey lack th e cap acit y to dem on st rate t h e dyn am ic st at u s of flow
disease, endocarditis, dysrhyth m ias) produce sym ptom s that m ay com p rom ise an d collateral developm en t . Ult rasou n d an d t ran
be con fused w ith VBI. scran ial Dop pler (TCD) are u sefu l screen ing tools for evalu at ion

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23 Surgical Treatment of Vertebrobasilar Insufficiency 299

of th e ext racran ial VA an d in t racran ial ver tebrobasilar system . Table 23.2 The Mean Values and Ranges of Blood Flow for
Advan tages of TCD include its low cost, w idespread availabilit y, Posterior Circulation Vessels in 50 Healthy Volunteers 37
and noninvasiven ess. How ever, as w ith all son ograph ic exam in a
Vessel Mean Flow (cc/min) Range* (cc/min)
t ion s, it is operator dep en den t an d it s sen sit ivit y ap pears to be
low er th an th at of CTA or MRA. BA 190 150–230
Cerebral d igit al su bt ract ion angiograp hy (DSA) is th e gold LPCA 72 50–94
st an dard for evalu at ing th e in t ra an d ext racran ial vascu lat u re RPCA 68 50–86
an d, in ou r op in ion , is an essen t ial im aging m odalit y in cases LVA 126 94–158
RVA 110 81–139
of VBI. In con t rast to n on invasive im aging, cerebral DSA is a dy
n am ic st udy capable of detect ing ret rograde flow, as seen in *Range (Mean minus standard deviation – Mean plus standard deviation)
cases of su bclavian steal syn drom e or th rough collaterals su ch as Abbreviations: BA, basilar artery; PCA, posterior cerebral artery; VA, vertebral
artery; L, left; R, right.
t h e an ter ior circu lat ion via PCoAs, or by p rovid in g a sen se of
h em odyn am ic flow across a sten ot ic vessel. Fur th erm ore, DSA
is u seful in detect ing ext racran ial VA com p rom ise associated
w ith h ead posit ion as seen w ith bow h u n ter’s syn drom e, w h ere
th e V2/V3 segm en t can be in term it ten tly occlu ded at C1/C2 w ith n or m al flow grou p . Th e Ver tebrobasilar Flow Evalu at ion an d
h ead t urn ing. Th e aor t ic arch , as w ell as th e origin an d course of Risk of Tran sien t Isch em ic At tack an d St roke (VERiTAS) is an on
both carot id an d ver tebral ar teries, m ust be visualized in cases going prospect ive m ult icen ter obser vat ion al st udy fun ded by th e
of ext racran ial VA disease. In cases of in t racran ial VBI, th e caliber Nat ion al In st it u tes of Health aim ed at determ in ing th e u t ilit y of
of both VAs an d th e presen ce an d caliber of th e PCoAs m u st be QMRA in assessing pat ien t s w ith sym ptom at ic ver tebrobasilar
evalu ated, an d if n ecessar y an Alcock’s test sh ou ld be p erform ed occlusive disease of ≥ 50%. If predict ive, QMRA evalu at ion cou ld
(carot id com pression during ver tebral ar ter y inject ion ) to dem h elp iden t ify h igh risk pat ien t s w h o w ould ben efit m ost from
on st rate th e presen ce, absen ce, or size of th e PCoAs. In cases eith er su rgical revascu larizat ion or en dovascu lar angioplast y
w h ere an extracranial to intracranial (EC–IC) bypass is contem an d sten t ing.
plated, the caliber an d course of th e STA an d OA as w ell as th e
caliber an d con figu rat ion of th e PCA, SCA, AICA, an d PICA vessels
an d th eir t ribut aries sh ou ld be carefu lly st u died.
Physiological im aging m odalit ies su ch as p osit ron em ission ■ Perioperative Preparation, Anesthetic
tom ography (PET), xen on com pu ted tom ography (Xe CT), single
ph oton em ission com p u ted tom ograp hy (SPECT), com pu ted to
Technique, and Neuroprotection
m ography perfusion (CTP), an d m agn et ic reson an ce perfusion Most pat ien t s w ith VBI are eith er on an t iplatelet or an t icoagu
(MRP), com m on ly used to detect h em odyn am ic com prom ise in lan t th erapy. We start daily aspirin (325 m g) in pat ien t s n ot al
an terior circulat ion occlusive disease, are less effect ive in assess ready on aspirin an d do n ot w ith h old it or discon t in ue it in th e
ing th e posterior circulat ion as a resu lt of th eir lim ited region al perioperat ive p eriod. Th e on ly except ion is in cases of OA by
resolu t ion .36 Fu r th erm ore, th e validit y of th ese im aging m odali passes, becau se h ar vest ing th e OA requ ires con sid erable m u scle
t ies in d etect in g p oster ior circu lat ion hyp op er fu sion rem ain s dissect ion as com pared w ith h ar vest ing th e STA. In th ese cases
u n cer t ain . Ph ase con t rast qu an t it at ive m agn et ic reson an ce an w e prefer to stop th e aspirin 1 w eek prior to surger y to avoid
giograp hy (QMRA) h as becom e available in recen t years an d is postop erat ive h em atom as. In su ch sit u at ion s, it is reason able to
cap able of direct ly m easu ring volu m et ric blood flow (m illiliters place th e pat ien t on eith er in t raven ou s or low m olecu lar w eigh t
per m in u te) th rough th e m ajor vessels of th e p osterior (an d an h ep ar in to be d iscon t in u ed 6 h ou rs or 1 day p r ior to su rger y,
terior) circulat ion . Th e tech n ique is n ow im plem en ted an d en resp ect ively. For p at ien ts on du al an t ip latelet th erapy, su ch as
h an ced in com m ercially available soft w are called t h e NOVA aspirin an d clopidogrel (Plavix), w e gen erally discon t in ue Plavix
(Non invasive Opt im al Vessel An alysis) system (VasSol, In c., Ch i and continue aspirin alone or in com bination w ith low m olecular
cago, IL). Table 23.2 list s th e m ean blood flow values an d ranges w eight heparin until the day prior to surger y. Patients on Coum a
for posterior circulat ion vessels in 50 h ealthy pat ien ts.37 Such din are conver ted to in t raven ou s h ep arin , w h ich is discon t in u ed
vessel flow m easurem en t s h ave been sh ow n to be h igh ly predic 6 h ou rs prior to surger y as aspirin is star ted.
t ive of recu rren t st roke in p at ien t s w ith sym ptom at ic ver tebro Th e surger y is perform ed w ith th e pat ien t un der gen eral an
basilar sten osis ≥ 50% or occlusion . In a ret rospect ive st udy of 47 est h esia. Hypovolem ia an d hyp oten sion m u st be avoided du ring
patients w ith sym ptom atic vertebrobasilar disease, patients w ith th e in it ial p ar t of t h e p roced u re p ar t icu larly in p at ien t s w it h
greater t h an 20% red u ct ion of blood flow in th e basilar arter y m argin al cerebral p er fu sion . In fact , w e d o n ot h esit ate to keep
(< 120 cc/m in ) an d PCAs (< 40 cc/m in ) h ad a h igh er risk of stroke, th e blood p ressu re sign ifican tly elevated u n t il th e proced u re or
over an average of 28 m on th s’ follow up, as com pared w ith pa bypass is com pleted in pat ien t s w h o are ext rem ely blood pres
t ien ts w ith n orm al blood flow (19% p er p erson year vs 0% p er su re dep en den t . Hyper ven t ilat ion an d α -ad ren ergic agen ts are
person -year).37 Sim ilarly, th e st roke free su r vival at 24 m on th s avoid ed at all cost s becau se of t h eir vasocon st rict ive effect s. In
w as 71% in th e low flow grou p as com p ared w it h 100% in t h e p at ien t s u n d ergoing in t racran ial p roced u res, brain rela xat ion is

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300 III Ischemic Stroke and Vascular Insufficiency

p referen t ially ach ieved via a lu m bar d rain an d cerebrosp in al i. In rem ote access: fem oral, brach ial, descen ding/ascen d-
flu id (CSF) drain age, part icularly w ith subtem poral exposu res, to ing aor ta
avoid the need for hyperosm olar agents and hyper ventilation. We ii. In local access: aor t ic arch , brach ioceph alic, VA, CCA
rout in ely u se m odest hypoth erm ia (33°C) th rough out th e p roce b. Occlu ded access vessels
du re, as w ell as in du ced blood pressu re elevat ion to 20 to 30% 2. Target vessels n ot am en able to sat isfactor y an d du rable sten t
above baselin e during th e period of tem porar y cross clam ping ing/angioplast y
to augm ent collateral flow. Electrophysiological m on itoring using 3. Kn ow n resistan ce to an t ip latelet agen t s
som atosen sor y, m otor evoked, an d brain stem auditor y evoked
poten t ials (SSEP, MEP, BAEP) facilitates early detect ion of isch
em ia or excessive ret ract ion an d m an ip u lat ion . Barbit u rates h ave Surgical Procedures
been u sed du ring bypass su rger y by oth ers to in crease toleran ce Su rger y for ver tebrobasilar in su fficien cy can be categorized in to
to cerebral hypoperfusion . Th e m ech an ism of barbit urate n euro t w o m ain t yp es—ext racran ial or in t racran ial—as ou tlin ed below
p rotect ion is m u lt ifactor ial an d in com p letely u n d erstood . It is an d described in detail in th e follow ing sect ion s.
believed to resu lt from reversible, d ose d ep en d en t d ep ression
of cerebral blood flow w ith subsequen t reduct ion in cerebral I. Ext racran ial procedu res:
m et abolic rate an d in t racran ial pressure.38–41 Fu r th erm ore, vaso A. Proxim al ver tebral ar ter y (V1)
con st r ict ion in n or m al areas of t h e brain m ay resu lt in an in 1. Recon st ruct ion
verse steal p h en om en on w it h red ist r ibu t ion of cerebral blood a. VA to CCA t ran sposit ion
flow to isch em ic t issue.42 At a cellular level, barbit urates reduce b. VA to su bclavian ar ter y or t hyrocer vical t r u n k re
isch em ia in du ced glu tam ate release,43 en h an ce γ-am in obut yric im plan tat ion
acid (GABA) ergic transm ission,44,45 and reduce ischem ia induced c. VA in terposit ion grafts to CCA or su bclavian ar ter y
in t racellu lar calcium t h rough in h ibit ion of both voltage gated 2. En dar terectom y
calcium chan nels and N m ethyl D aspartate (NMDA) receptors.46 3. Decom p ression
In add it ion to th e aforem en t ion ed n eu rop rotect ive p rop er t ies, B. Midver tebral ar ter y (V2)
barbit u rates m ay also act as a scavenger of m em bran e dam aging 1. Decom pression of osteop hyt ic ext rin sic ver tebral arter y
free radicals. Despite th ese potent ial benefits, w e do not routin ely sten osis
use barbiturate neuroprotection due to problem s associated w ith 2. Recon st ru ct ion
circulator y an d respirator y depression , as w ell as delayed post a. ECA to VA t ran sposit ion
operat ive w ake up. How ever, if tech n ical difficult ies during th e b. VA in terposit ion graft s to CCA, in tern al carot id arter y
anastom osis result in excessively prolonged tem porar y occlusion, (ICA), or ECA
w e m ay con sider u sing barbit u rates. C. Distal ver tebral ar ter y (V3)
1. Decom pression
2. Recon st ru ct ion
a. ECA or OA to V3 bypass
■ Surgery for Vertebrobasilar II. In t racran ial procedures:
A. Recon st ru ct ion
Insufficiency 1. Upper VB territor y:
Advan ces in en dovascu lar tech n iques an d th e availabilit y of a. STA–PCA en d to side bypass
ext ra/in t racran ial sten t s as w ell as balloon angiop last y cap able b. STA–SCA en d to side byp ass
of adequately t reat ing m any causes of ver tebrobasilar isch em ia c. SCA–PCA side to side bypass
h ave largely su p p lan ted su rgical revascu lar izat ion . How ever, 2. Low er VB territor y:
th ere st ill rem ain sit u at ion s in w h ich open su rgical p rocedu res a. VA–PICA in terposit ion bypass
are n ecessar y, par t icu larly w h en on e con siders th e disappoin t b. PICA reim plan tat ion in VA
ing n egat ive resu lt s of th e Sten t ing versu s Aggressive Medical c. OA–PICA en d to side bypass
Man agem en t for Preven t ing Recu rren t st roke in In t racran ial Ste d. PICA–PICA side to side bypass
n osis (SAMMPRIS) t rial.47 A few pu blicat ion s discu ss in det ail th e 3. Middle VB territor y
tech n iques of posterior circulat ion su rgical revascularizat ion , a. OA–AICA en d to side bypass
bu t t h ree p ar t icu larly excellen t on es are from Sp et zler et al,48 B. En dar terectom y
Hop kin s et al,49 an d Ch arbel et al.50 1. V4

Indications for Surgical Revascularization


of the Vertebrobasilar System ■ Extracranial Procedures
Su rger y is in dicated in cases of p osterior circu lat ion h em ody
Surgery of the First Vertebral (V1) Segment
n am ic com prom ise w ith repeated circulat ion appropriate t ran
sien t isch em ic at t acks (TIAs)/st rokes refractor y to best m edical Exposure of the Proximal Vertebral Artery (V1)
t reat m en t , an d if any of th e follow ing applies:
Th e V1 segm en t exten ds from th e origin of th e VA to th e t ran s
1. Difficult or im possible en dovascu lar access to lesion du e to: verse foram en of th e sixth cer vical ver tebra. Th e proxim al VA
a. Tor t u ou s vascu lar an atom y in access vessels an d CCA are exposed via a supraclavicular approach . A 6 to 7 cm

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23 Surgical Treatment of Vertebrobasilar Insufficiency 301

a b

Fig . 23.2a–b Typical surgical steps on left side of neck. (a) Supraclavic- the following structures can be identified: internal jugular vein, internal
ular skin incision to expose V1 (A) and longitudinal skin incision to expose m amm ary artery, phrenic nerve, subclavian artery, thoracic duct, thyrocer-
V2 (B). (b) After transecting the sternocleidomastoid muscle, mobilizing the vical trunk, V1 section of vertebral artery, and vagus nerve. (Courtesy of
com m on carotid artery m edially and dissecting through the fat t y layers, Barrow Neurological Institute.)

lin ear in cision is m ade from th e stern oclavicu lar ar t icu lat ion Th e ver tebral ar ter y can be iden t ified in t w o w ays. Th e ar ter y
an d exten ded laterally parallel to an d ~ 2 cm above th e clavicle. m ay be iden t ified in a lateral to m edial direct ion by first expos
Th e u n derlying p lat ysm a is divided h orizon tally. Th e clavicular ing th e su bclavian arter y dist ally an d follow ing it proxim ally to
h ead of th e stern ocleidom astoid m uscle is iden t ified an d cut , its bran ch es. Th e subclavian ar ter y is recogn ized as h aving th ree
leaving a cu ff for later reapp roxim at ion . Th e m u scle is th en re division s, defin ed by th e an terior scalen e m u scle, w h ich covers
t racted su p eriorly. Th e u n derlying om ohyoid m uscle m ay also the secon d segm en t. Th e vertebral arter y arises from th e postero
be divided. Th e carot id sh eath is open ed an d th e in tern al jugu lar sup erior aspect of th e first segm en t of th e subclavian ar ter y an d
vein ret racted laterally an d th e CCA m edially. Care sh ou ld be h as n o proxim al bran ch es. Th is differen t iates it from th e thyro
exercised so as n ot to injure th e vagu s n er ve, w h ich u su ally lies cer vical t run k, w h ich arises from th e an terosuperior aspect of
on th e posterior aspect of th e sh eath , alth ough a rare an om aly th e su bclavian ar ter y an d divides in to m u lt iple bran ch es. Addi
involves an an terior p osit ion of th e n er ve. Th e an terior scalen e t ion ally, th e VA is th e first bran ch from th e su perior su rface of
m uscle an d th e overlying ph ren ic n er ve m ay be iden t ified later th e su bclavian , w h ereas th e thyrocer vical t ru n k is secon d. Alter
ally in th e exposure but sh ould n ot require any dissect ion (Fig. n at ively, t h e ver tebral ar ter y m ay be exp osed m ed ially an d su
23.2). p eriorly as it en ters th e t ran sverse foram en of C6 by palpat ing
Dep en d in g on t h e sid e of t h e ap p roach , t h e r isk of inju r y to th e an terior (carot id) t u bercle of t h e t ran sverse process. Th e ver
t h e recu r ren t lar yn geal n er ve an d lym p h at ic d rain age d iffers. tebral ar ter y ascen ds th rough a t riangle form ed by th e an terior
Th e r igh t recu r ren t lar yn geal n er ve loop s arou n d t h e su bcla scalen e m u scle (laterally), th e longu s colli m u scle (m edially),
vian ar ter y as it ap p roach es t h e t rach ea an d is t h erefore m ore an d th e first par t of th e subclavian ar ter y (in feriorly) w ith th e
vu ln erable to inju r y w ith m ed ial ret ract ion of t h e t rach ea. On carot id t u bercle at it s ap ex. Th e vertebral vein , form ed from th e
t h e ot h er h an d , t h e left recu r ren t lar yn geal n er ve loop s arou n d ver tebral ven ous plexus, can be seen an terior to th e ar ter y as it
t h e aor t ic arch an d ap p roach es th e t rach ea at a low er level, an d exits the tran sverse foram en of C6. The recurren t lar yngeal ner ve,
is t h u s less vu ln erable to a ret ract ion inju r y. Lym p h at ic d rain t h e cer vical sym p at h et ic t r u n k, an d t h e low er brach ial p lexu s
age on t h e r igh t sid e occu rs th rough sm all t r u n ks in to th e r igh t m ust be p rotected du ring th e exp osu re.
su bclavian an d jugu lar vein s. In con t rast , lym p h at ic d rain age
on t h e left is t h rough t h e m ore su bst an t ial t h oracic d u ct , w h ich
Vertebral Artery Transposition/ Reimplantation
d rain s in to t h e ju n ct ion of t h e left su bclavian an d in ter n al jugu
lar vein . Th erefore, t h e recu r ren t lar yngeal n er ve is at a greater Th is p rocedu re can be u sefu l in p at ien t s w ith p roxim al su bcla
r isk of inju r y w it h r igh t sid ed ap p roach es, w h ereas t h e r isk of vian arter y occlusion an d clin ical an d angiograph ic eviden ce of
lym p h at ic fist u la is greater w it h left sid ed ap p roach es. Regard ver tebral “steal” or in cases of ver tebral ar ter y origin occlusion
less of t h e sid e of ap p roach , it sh ou ld be n oted t h at lym p h at ic w ith rest ricted flow in th e con t ralateral ver tebral ar ter y. It can
d u ct s d o n ot coagu late w ell, an d it is bet ter to id en t ify an d li be t ran sposed in to th e CCA or reim plan ted in to th e subclavian
gate t h em . ar ter y or th e thyrocer vical t r un k.

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302 III Ischemic Stroke and Vascular Insufficiency

Vertebral Artery-to-Common Carotid Artery Transposition n ique of en d to side an astom osis). We prefer to an ch or th e h eel
(th e fish m ou th ed corn er) of th e VA an d th en separately sut ure
After exposure, both th e proxim al VA an d CCA are prepared for
th e back w all of th e an astom osis first follow ed by th e fron t w all
th e t ran sposit ion . Th e p eriadven t it ial layer is cleared from th e
u sing a ru n n ing su t u re. Th e in it ial an ch oring sut u re is passed
CCA at th e plan n ed site of an astom osis. Th e VA is occluded proxi
from outside to in side, th en in side to out side so th at th e fin al
m ally at its origin u sing Weck clips an d dist ally as it en ters th e
kn ot lies outside th e ar terial lum en . Th e an astom osis proceeds
t ran sverse foram en u sing a tem p orar y clip. Th e VA is th en t ran
by first sut uring th e m ore difficult back w all w h ile view ing from
sected above th e Weck clip s an d th e lu m en flu sh ed w ith h epa
in side th e vessels. Upon reach ing th e toe en d of t h e an astom osis,
rin ized salin e. An en dar terectom y m ay occasion ally be requ ired
th e su t u re is t ied to it self. On ce th e back w all h as been su t u red, a
if t h e lu m en is sten osed by an at h erosclerot ic p laqu e. If t h e VA
n ew an ch oring sut ure is placed an d th e fron t w all is th en su
is too sh or t to reach t h e CCA, it m ay be n ecessar y to liberate
t u red in a sim ilar m an n er w h ile view ing th e ou ter su rface of th e
t h e ar ter y from th e t ran sverse foram en of C6. Th e proxim al 1 cm
vessels. Th e lu m en of both arteries is filled w ith h ep arin ized sa
of t h e VA is st r ip p ed of it s p er iadven t it ial layer an d t h en cu t
lin e an d backbleeding allow ed p rior to com p let ion of th e fin al
obliqu ely an d sligh t ly fish m ou t h ed on it s lateral cor n er. Th is
st itch . Th e clam ps are th en rem oved an d t h e su t u re lin e obser ved
in creases t h e cross sect ion al area available for t h e byp ass an d
for bleeding. Sligh t oozing u sually stops w ith Su rgicel (Joh n son &
p rovid es redu n dan cy of th e VA w all, t h ereby m in im izing t h e
Joh n son ) an d gen t le p ressu re w ith a cot ton oid. Occasion ally it
possibilit y of sten osis at th e site of an astom osis. Th e p at ien t is
m ay be n ecessar y to p lace an addit ion al in terr u pted su t u re if th e
h eparin ized w ith an in t raven ous dose of 3,000 to 5,000 IU, de
bleeding does n ot term in ate w ith ligh t pressure. A suct ion drain
pen ding on th e pat ien t’s w eigh t , to p reven t in t ravascu lar th rom
is placed an d th e w oun d closed in layers after reapproxim at ion
bosis during th e period of tem porar y occlusion . Neu roprotect ion
of th e clavicular h ead of th e stern ocleidom astoid m u scle. Th e
is ach ieved w it h in d u ced m od erate hyp er ten sion (30% above
fin al result is sch em at ized in Fig. 23.3.
baselin e) an d m odest hyp oth erm ia.
Five m in utes after h ep arin adm in ist rat ion , th e CCA is cross
clam p ed at t h e selected level an d rot ated to expose th e p ostero
Vertebral Artery-to-Subclavian Artery or -Thyrocervical
lateral w all of the artery. A 4 or 5 m m circular arteriotom y based
Trunk Reimplantation
on th e size of th e ver tebral ar ter y is th en m ade using an ellipt ical
aor t ic pu n ch . Th e ver tebral ar ter y is m obilized an d an astom osed An altern at ive to VA–CCA t ran sposit ion is reim plan tat ion of th e
to th e carot id ar ter y using a 7 0 m on ofilam en t sut ure. Th e an as VA to eith er th e su bclavian ar ter y (Fig. 23.4) or th e thyrocer vical
tom osis can be perform ed in m any w ays (see below for tech t ru n k. Th is is par t icu larly u sefu l in sit u at ion s in w h ich th e CCA is

Fig. 23.3 Reimplantation of left V1 in left com m on carotid artery. Fig. 23.4 Reimplantation of left V1 in left subclavian artery.

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23 Surgical Treatment of Vertebrobasilar Insufficiency 303

eith er sten ot ic or occlu d ed. An oth er advan t age of th is tech n iqu e


is avoidan ce of th e isch em ic risks associated w ith carot id cross
clam p ing. It sh ou ld be n oted th at reim p lan t at ion in to th e su bcla
vian ar ter y is gen erally p erform ed d ist al to th e origin of th e VA in
th e region of th e an terior scalen e m uscle.

Vertebral Artery Interposition Grafts


An in terposit ion graft m ay be used in sit u at ion s w h ere th e VA is
too sh or t to perm it t ran sposit ion . Th e graft can be an astom osed
to eith er th e subclavian ar ter y or th e CCA in an en d to side fash
ion an d t h en to th e VA in an en d to en d fash ion . Th ere are sev
eral graft possibilit ies in cluding autologous ven ous an d ar terial
graft s (su ch as t h e sap h en ou s an d in ter n al iliac vein s an d in
ter n al m am m ar y an d rad ial ar ter ies) or syn t h et ic graft s su ch as
polyethylen e tereph th alate (Dacron ) or p olytet raflu oroethylen e
(PTFE). Th e disadvan tage of in terposit ion grafts is th at th ey are
t im e con su m in g d u e to t h e n eed for t w o an astom oses, as w ell
as th e t im e related to h ar vest ing th e graft if an au tologou s graft
is used. Fu r t h erm ore, th ere is th e risk of isch em ic com plicat ion s
related to carot id cross clam p in g if t h e CCA is u sed as a site of
an astom osis. A CCA–sap h en ou s vein –VA in ter p osit ion graft is
sch em at ized in Fig. 23.5. A clin ical case of su bclavian ar ter y ex
posure an d sap h en ou s vein im plan tat ion is sh ow n in Fig. 23.6.

Vertebral Artery Origin Endarterectomy


Curren tly, w ith th e availabilit y of safer an d sim p ler en dovascu lar
tech n iques, ver tebral en dar terectom y is rarely perform ed. Th e Fig. 23.5 Interposition venous graft: com m on carotid artery-vein-V1.

Fig. 23.6a,b Use of subclavian artery (SA) as a donor. (a) Exposure and
control of SA through supraclavicular approach. (b) Postoperative angio-
gram after saphenous vein implantation in SA. b

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304 III Ischemic Stroke and Vascular Insufficiency

procedu re m ay st ill be con sidered in rare cases of VA origin ste Decompression of the V1 Segment
n osis an d sim ultan eous subclavian ar ter y occlusion in pat ien ts
Occasion ally a cer vical fibrou s ban d from th e ten don of th e an te
w h o can not u n dergo radial or brach ial en dovascu lar access. Th e
rior scalen e or longu s colli m u scle m ay com p ress th e p roxim al
exp osu re is th rough a su p raclavicu lar ap proach as described
VA. Th is m ay becom e clin ically sign ifican t in cases w h ere flow
above. The su bclavian ar ter y both proxim al an d dist al to th e VA
th rough th e con t ralateral VA is eith er occlu ded or severely re
origin m ust be exposed. It is n ot n ecessar y to dissect th e VA to it s
stricted. Patients t ypically com plain of vertebrobasilar sym ptom s
en t ran ce in to th e t ran sverse foram en . Th e thyrocer vical an d in
w ith t urn ing of th e h ead. Dyn am ic cer vical ver tebral angiogra
tern al m am m ar y ar teries m ust be dissected an d tem porarily oc
phy, first w ith th e p at ien t’s h ead in a n eu t ral p osit ion an d th en
clu ded. Th e p at ien t is given a bolu s of h ep arin . A tem p orar y clip
w ith th e h ead t urn ed, w ill dem on st rate vertebral ar ter y com pro
is app lied to th e VA above th e p laque an d vascu lar clam ps ap
m ise only in the lat ter position. Surgical decom pression is accom
plied to th e su bclavian ar ter y on eith er side of th e VA origin .
plish ed after exp osu re of th e VA from its origin to th e t ran sverse
Rem oval of th e p laqu e can be perform ed in t w o w ays. Th e
foram en of C6 by excising th e overlying con st rict ing ligam en ts,
first techn ique is th rough a longit u din al in cision along th e an
m u scles, an d ban d s. Occasion ally t h e sym p at h et ic gan glia or
terosu perior w all of th e su bclavian ar ter y just in ferior to th e ver
n er ve fibers m ay com press th e VA. Division of th e stellate ganglia
tebral ar ter y origin (Fig. 23.7). Dissect ion of th e p laqu e begin s in
u su ally result s in a m ild ipsilateral Horn er’s syn drom e. How ever,
th e su bclavian ar ter y an d p roceeds in to th e ver tebral ar ter y. Th e
occasion ally it m ay be n ecessar y to excise th e ganglia to relieve
plaque rarely exten ds m ore th an 1 cm in to th e ver tebral ar ter y. It
VA com pression . In su ch sit u at ion s, an altern at ive to excising th e
m ay be necessar y to place an in t im al tacking sut ure in th e sub
ganglia, w h ich w ould resu lt in a m ore sign ifican t Horn er’s syn
clavian arter y dist ally at th e m argin of th e en dar terectom y. Th e
drom e, is division of th e VA an d rean astom osis in an en d to en d
secon d tech n iqu e is th rough a ver t ical in cision in th e ver tebral
fash ion .
ar ter y that exten ds in to th e su bclavian ar ter y (Fig. 23.8). Th is
en ables visu alizat ion of th e dist al ver tebral ar ter y p laqu e. We
favor th e lat ter tech n iqu e. Surgery of the Second Vertebral (V2) Segment
After th e plaque h as been rem oved, th e ar teriotom y is closed
Exposure of the V2 Segment of the Vertebral Artery
using a 6 0 m onofilam ent suture. A patch (vein or syn thetic) m ay
be u sed in th e lat ter tech n iqu e (ver t ical in cision ) to avoid sten o Th e V2 segm en t st art s from th e t ran sverse foram en of C6 an d
sis of th e ver tebral ar ter y origin . Th e ver tebral ar ter y is allow ed goes to th e t ran sverse foram en of C1. Exposure of V2 is ach ieved
to backbleed prior to com plet ion of th e fin al st itch . Fin ally th e th rough an an terior ap proach . In rare cases, V2 is in adver ten tly
dist al an d p roxim al su bclavian ar ter y clam p s are rem oved fol injured du ring cer vical diskectom y procedu res if disk excision /
low ed by rem oval of th e tem porar y clip off th e ver tebral ar ter y. curet t ing is too lateral. Th e pat ien t is posit ion ed supin e w ith th e

a b

Fig. 23.7a–c Left V1 endarterectomy, longitudinal variant. (a) Transverse


incision in subclavian artery just below V1 origin. (b) The atherom a is dis-
sected off the origin of the V1. (c) The endarterectomy is completed and
c the arteriotomy is sutured.

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23 Surgical Treatment of Vertebrobasilar Insufficiency 305

a b

Fig. 23.8a–c Left V1 endarterectomy, vertical variant. (a) Vertical incision


in V1 origin. (b) Atherom a dissected off origin of V1. (c) Endarterectomy
completed and arteriotomy closed with a vascular patch to prevent early/
c delayed stenosis.

n eck sligh tly exten ded by placing an in terscapular roll to facili postop erat ive n u m bn ess in th e an terior n eck, w h ich t yp ically
tate th e deep exposu re. A large m outh guard sh ould be avoided disap pears w ith in 6 m on th s as th e n er ve regen erates. Th e dis
to m axim ize th e available subm an dibular space. Th is is par t icu sect ion is th en carried along th e an terior asp ect of th e stern o
larly im p or tan t for exposu re of th e distal V2 segm en t at C1–2. cleidom astoid m uscle. Self retaining retractor blades m ust always
Th e skin in cision is m ade eith er t ran sversely or longit u din ally be kept su perficial on th e m edial side to preven t ret ract ion in
dep en ding on th e n u m ber of levels n eeded to be exp osed. A jur y to th e lar yngeal n er ves, but m ay be placed m ore deeply on
t ran sverse in cision along a skin crease exten ding from th e m id th e lateral side. Excessive ret ract ion sh ou ld be avoided as th is
lin e to ju st p ast th e an terior border of th e stern om astoid m u scle m ay result in st retch injur y of th e spin al accessor y n er ve. It is
is adequ ate for on e or t w o level d isease. A longit u din al in cision im port an t to rem em ber th at th e sp in al accessor y n er ve pen e
along th e an terior border of th e stern om astoid m uscle exten ding t rates th e m edial border of th e stern ocleidom astoid m u scle at
from ap p roxim ately t w o fingerbreadth s above th e clavicle to ap th e ju n ct ion of its u pper th ird an d m iddle th ird. Th e su bsequen t
proxim ately t w o fingerbreadth s below th e angle of th e m an d ible plan e of dissect ion w ill var y depen ding on th e level of th e V2
is n eed ed for disease involving th ree or m ore levels. Exposure of segm en t n eeded for exposure.
th e dist al V2 segm en t at C1–2 requ ires fu r th er rost ral exp osu re
an d exten sion of th e u p p er en d of t h e in cision backw ard in a
Exposure of V2 at the Level of C6
gen tle cur ve tow ard th e m astoid process to avoid injur y of th e
m an dibular bran ch of th e facial n er ve. Th is becom es th e “an tero Su rgical exp osu re of th e VA at th e t ran sverse process of C6 is
lateral” ap proach develop ed by Bern ard George.51 It sh ou ld be sim ilar to th e exp osu re of th e V1 segm en t described above. Th e
n oted th at th e length an d level of th e skin in cision sh ou ld be carot id sh eath is en tered an d th e in tern al jugu lar vein ret racted
adju sted ap p rop r iately based on t h e locat ion of t h e p at h ology. laterally an d t h e CCA m edially. Th e d issect ion is con t in u ed in
A cer vical X ray can be u sed to d efin e t h e level of in terest prior t h e deep fascial layer. Th e an terior (carot id) t u bercle of th e C6
to in cision an d sh ould be repeated to con firm th e proper level t ran sverse p rocess is p alpated an d th en th e in ser t ion s of th e sca
in t raoperat ively. len e an d longu s colli m u scle d issected in a su bp eriosteal fash ion .
Th e p lat ysm a is t h en in cised sh arp ly w h ile avoiding inju r y to Th e d issect ion can be carried m ore rost rally to exp ose th e C5
th e great au ricu lar n er ve, w h ich ru n s ju st ben eath th e m uscle at t ran sverse p rocess if n ecessar y. Th e t ran sverse foram en is th en
t h e u p p er m ost asp ect of t h e in cision . It is n ot u n com m on to u n roofed u sing a h igh sp eed d rill, preferably a diam on d bit for
en cou n ter t h e t ran sverse cer vical cu t an eou s n er ve as it crosses safet y, Kerrison rongeu rs, an d cu ret tes to expose th e un derlying
th e m id belly of th e stern ocleidom astoid m u scle. Tran sect ion of VA. Th e ven ou s p lexu s th at invest s th e VA is carefu lly coagu lated
th is n er ve m ay be n ecessar y for exposu re an d resu lts in t ran sien t an d dissected from th e ar ter y.

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306 III Ischemic Stroke and Vascular Insufficiency

Exposure of V2 at the Level of C2–C5 Sym ptom s are frequen tly in term it ten t an d precipitated by h ead
t urn ing. Dyn am ic angiography togeth er w ith CT or CTA can es
Exp osu re of th e m id V2 segm en t is ach ieved by carr ying th e dis
tablish the diagnosis. Managem ent consists of surgical rem oval of
sect ion bet w een th e st rap m u scles, thyroid, t rach ea, an d esoph a
the offending com pressive lesion. Th e t ransverse processes above
gu s m edially an d th e stern om astoid m uscle an d carot id sh eath
an d below th e level of sten osis are exposed. Th e t ran sverse fo
laterally. Th e prever tebral fascia is op en ed an d th e un derlying
ram in a are u n roofed an d t h e ven ou s p lexu s invest in g t h e VA
anterior longitudinal ligam ent and longus colli m uscle identified.
coagulated an d dissected off of th e ar ter y. Th e VA is m obilized
Th e ip silateral lon gu s colli m u scles are t h en d issected off t h e
laterally exposing th e osteophyte origin at ing from th e un cover
an terolateral surface of th e ver tebral bodies an d t ran sverse pro
tebral joint. The osteophyte is subsequently rem oved using a high
cesses at th e target levels. Th e sym path et ic t ru n k lies on th e lat
speed drill an d cu ret tes. Con st rict ing fibrous ban ds or adh esion s
eral aspect of th e longus colli m uscle an d m ust be preser ved.
sh ou ld also be released . Th e VA sh ou ld exp an d to it s n orm al cali
Sim ilarly, cau t ion sh ou ld be exercised w h en dissect ing th e m u s
ber at th e en d of th e procedu re.
cle lateral to th e an terior t u bercle of th e t ran sverse processes to
avoid injur y to th e exit ing cer vical n er ves, w h ich lie im m ediately
lateral and posterior. The transverse foram ina, located m edial and Revascularization of the V2 Segment
deep to th e an terior t u bercle, are su bsequ en tly u n roofed using a Revascu larizat ion of th e V2 segm en t can be perform ed in th e
h igh speed drill, Kerrison rongeurs, an d cu ret tes to expose th e set t ing of p roxim al VA occlu sion p rovided th at paten cy of th e
u n derlying VA. Th e ven ou s plexu s th at invest s th e VA is carefu lly dist al VA can be dem on st rated by DSA. Th e distal VA is frequ en tly
coagulated an d dissected from th e ar ter y. It is ext rem ely im por recon st it u ted via m u scu lar collaterals from t h e ascen d ing cer
tan t to preser ve th e radiculom edu llar y bran ch es of th e VA to vical an d occipit al ar teries. Revascu larizat ion of th e V2 segm en t
preven t an isch em ic inju r y to th e spin al cord. can be perform ed u sing t ran sp osit ion tech n iqu es or w ith in ter
posit ion grafts.
Exposure of V2 at the Level of C1–2
Exp osu re of th e d ist al V2 segm en t at C1–2 is id eal for revascu lar Transposition Techniques
izat ion procedu res. Th e ap proach requ ires a h igh exposu re. Th e
Several t ran sposit ion opt ion s exist . Th e ECA or on e of it s bran ch es
pat ien t is posit ion ed su p in e w ith th e h ead rot ated to th e con t ra
can be t ran sp osed to th e V2 segm en t p rovided th at th e ECA
lateral side. As m en t ion ed above, th e in cision is star ted along th e
t ru n k is long en ough an d th e carot id ar ter y bifu rcat ion is free
an terior border of th e stern ocleidom astoid m uscle to a poin t ap
of ath erosclerot ic disease. Th e carot id bifurcat ion is exposed an d
proxim ately t w o fingerbreadth s below th e angle of th e m an d ible
th e ECA skeleton ized. All th e ECA bran ch es are dou bly ligated
an d th en exten ded backw ard in a gen tle cur ve tow ard th e m as
an d divided. Th e occipit al ar ter y is gen erally left in tact , part icu
toid process to avoid inju r y of th e m an dibular bran ch of th e fa
larly if it con st it u tes a m ajor sou rce of collateral su p ply to th e VA.
cial n er ve. Several m an euvers can facilitate th e h igh exposure.
Th e VA is th en exposed at th e C1–2 level an d th e ar ter y cleared
Nasal en dotracheal in tubat ion and avoiding placem ent of a m outh
of it s periadven t ial t issue at th e proposed site of an astom osis.
guard sh ould m axim ize th e available subm an dibular space. Sim
Th e ECA is cu t at an app rop riate length to reach th e V2 segm en t
ilarly, in ext rem ely rare circu m stan ces, it m ay be n ecessar y to
w ith out ten sion . Th e distal 1 cm of th e ar ter y is th en st ripped of
dislocate th e tem p orom an dibu lar join t , divide th e stern ocleido
its periadven t it ial layer, fish m outh ed, an d an astom osed to th e
m astoid m u scle or divide th e m an dibu lar ram u s. Th e au ricu lar
VA in an en d to side or en d to en d fash ion u sing an 8 0 m on o
n er ve, w h ich ru n s just ben eath th e plat ysm a at th e upperm ost
filam en t su t u re. Alter n at ively, t h e VA can be t ran sp osed an d
aspect of th e in cision , m ay n eed to be t ran sected. Th e low er pole
an astom osed to th e ICA, ECA, or CCA in an en d to side fash ion .
of th e parot id glan d is reflected rost ro an teriorly.
Th e carot id sh eath is en tered an d th e in tern al jugu lar vein
iden t ified . Th e plan e of dissect ion is carried bet w een th e in ter Interposition Grafts
n al jugu lar vein m edially an d th e stern om astoid m u scle laterally. In terposit ion graft s can be used in sit uat ion s w h ere a t ran sp osi
The spinal accessor y ner ve is identified and protected as it courses t ion can n ot be perform ed du e to in su fficien t length of th e ECA
posteriorly beneath the sternocleidom astoid m uscle. Distal expo t ru n k or its bran ch es. Graft ch oices in clu de au tologou s (ven ou s
su re can be facilit ated by ret ract ing th e digast ric m u scle rost ro or ar terial) or syn th et ic graft s (Dacron or PTFE). Th e VA is ex
anteriorly w ith fishhooks, and occasionally, dividing the digastric posed at th e level C1–2 an d th e ar ter y cleared of it s periadven t i
m uscle. Th e C1 an d C2 t ubercles are palpated an d con firm ed by t ial t issu e at th e proposed site of an astom osis. Possible don or
in t raop erat ive fluoroscopy. Th e levator scapu lae m u scle, w h ich sites in clu de th e CCA, ICA, or ECA, alth ough th e lat ter is p referred
originates from the posterior tubercles of the transverse processes to avoid cerebral isch em ia du ring th e period of tem porar y occlu
of C1–4, is in cised to expose th e an terior ram us of th e C2 n er ve sion . Fig. 23.9 dem on st rates a sch em at ic of a CCA saph en ous V2
root . Cut t ing th e C2 n er ve root laterally exposes th e VA bet w een in terp osit ion graft .
C1 an d C2. Fu r th er exposu re can be ach ieved by liberat ing th e VA
from th e transverse foram en of C1. The ven ous plexus that invests
th e VA is th en carefully coagu lated an d d issected off th e ar ter y. Surgery of the Third Vertebral (V3) Segment
Exposure of the V3 Segment of the Vertebral Artery
Decompression of the V2 Segment
Th e V3 segm en t st art s from th e t ran sverse foram en of C1 an d
Extern al com pression of th e V2 segm en t , du e to cer vical spon dy en d s at th e p oin t w h ere th e ar ter y pierces t h e du ra. Exp osu re of
lot ic d isease or fibrou s ad h esion s w it h in or bet w een t h e t ran s th e V3 segm en t is easily ach ieved via a posterior m idlin e ap
verse p rocesses, can resu lt in sym ptom at ic VA com p rom ise. proach . Th e pat ien t is p laced in a lateral decu bit u s posit ion w ith

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23 Surgical Treatment of Vertebrobasilar Insufficiency 307

Fig. 23.10 Surgical view of a right far-lateral approach including m idline


suboccipital exposure. Note the dissected and isolated right occipital artery
and V3 segm ent at sulcus arteriosus. The patient is in the three-quarter
prone position.

flow th rough th e ext racran ial VA associated w ith h ead m ove


m en t s. Th e con dit ion is depen den t on th e existen ce of an iso
lated posterior circulation w ith hypoplasia, stenosis, or occlusion
of th e con t ralateral VA an d m in im al collaterals from th e an terior
circulat ion . Bow h un ter’s syn drom e t ypically occurs at th e at
lan toaxial level as a resu lt of im m obilizat ion of th e VA at th e
Fig. 23.9 Interposition venous graft: common carotid artery-vein-V2. Note
the opening of foramen transversarium at C3 in this case.
t ran sverse foram in a of C1 an d C2 an d along th e su lcu s ar teriosu s
to it s dural en t r y. As w e h ave m en t ion ed above, com prom ise of
VA blood flow associated w ith h ead an d n eck rot at ion can also
th e h ead t u rn ed to th e con t ralateral side. A h ockey st ick in cision occur at oth er levels as a result of fibrous ban ds, m uscular ten
is th en m ade. Th e in cision start s in th e m idlin e app roxim ately at d on s, or sp on dylot ic sp u rs. Dyn am ic an giograp hy is t h e gold
th e level of th e sp in ou s p rocess of C3 an d exten ds su periorly to st an dard im agin g test . Su rgical t reat m en t opt ion s for bow
~ 2 cm above th e su perior n uch al lin e. Th e in cision is th en cur ved h u n ter’s syn drom e in clu de C1–2 fusion or surgical decom pres
laterally p arallel to t h e su p er ior n u ch al lin e to a p oin t im m ed i sion of th e VA.53–55
ately su p er ior to t h e m astoid p rocess. Fin ally, th e in cision is
cur ved in feriorly to en d just in ferior to th e m astoid process. Care Revascularization of the V3 Segment
sh ou ld be taken to p reser ve th e OA if it is to be u sed for a byp ass
(see Occipital Ar ter y Bypass, page 309). Th e suboccipital fascia A byp ass to t h e V3 segm en t can be p er for m ed in t h e set t ing
an d m uscles are in cised, leaving a m uscular cuff at t ach ed to th e of proxim al VA occlu sion . DSAs m ust dem on st rate recon st it ut ion
su p erior n u ch al lin e for later reat t ach m en t . Th e m u scu lat u re is of th e distal VA th rough m uscular collaterals from th e ascen ding
th en sw ept laterally to exp ose t h e occip u t as far laterally as th e cer vical or occip it al ar ter ies. In m ost cases t h e OA is u sed for
m astoid process, as w ell as th e lam in a of C1 an d C2. Th e verte t h e bypass. How ever, it sh ou ld be n oted th at if th e OA already
bral ar ter y is iden t ified w ith in th e sulcus ar teriosus of C1. Th e rep resen t s a m ajor source of collateral su pply, perform ing an OA
su rrou n ding ven ou s p lexu s is carefu lly coagu lated an d dissected bypass m igh t n ot provide any su bst an t ial blood flow to th e VA
from th e ar ter y. Resect ion of th e p osterior arch of C1 usu ally pro beyond w hat is already present. In such situations it m ay be m ore
vides access to a 1 to 1.5 cm h orizon tal segm en t of th e ar ter y. pr u den t to p erform an in terp osit ion graft bet w een th e VA an d
Th e t ran sverse foram en of C1 can be d r illed to liberate t h e VA th e ECA or CCA.
if a longer segm en t is n eed. Fig. 23.10 represen t s a clin ical case After h ar vest ing th e OA an d exposing th e V3 segm en t, th e VA
w ith a righ t far lateral approach , an d dem on st rates th e exposure is liberated from th e C1 t ran sverse foram en . Th e OA is cut at an
of th e V3 segm en t at th e sulcus ar teriosu s, as w ell as th e dissec appropriate length an d th e distal en d st ripped of its periadven t i
t ion of th e righ t occip it al ar ter y. t ia an d fish m ou th ed. Th e pat ien t is given a dose of in t raven ou s
h eparin an d th e blood pressure is elevated. Th e VA segm en t in
ten ded for th e an astom osis is th en isolated bet w een tem porar y
Decompression of the V3 Segment
clips. Th e bypass is su bsequ en t ly perform ed in an en d to side
Bow h u n ter’s st roke (syn d rom e), first coin ed by Soren sen 52 in fash ion using a 8 0 or 9 0 m on ofilam en t (th e tech n ique is dis
1978, is ch aracterized by VBI secon dar y to com prom ised blood cussed below ).

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308 III Ischemic Stroke and Vascular Insufficiency

from u n dern eath th e scalp flap . We prefer to first iden t ify th e


■ Intracranial Procedures STA distally an d th en p roceed w ith th e dissect ion proxim ally, so
Extracranial-to -Intracranial Bypass th at if th e ar ter y is in adver ten tly inju red early in th e dissect ion ,
th ere is st ill en ough ar ter y length to p erform th e byp ass. Th e
Th e in d icat ion s for EC–IC byp ass in th e set t ing of VBI are lim ited. ar ter y is dissected out from th e galeal t issu e, leaving a cuff of soft
To date, th ere are n o prospect ive or ran dom ized st udies validat t issu e su rroun ding th e ar ter y. Side bran ch es are coagulated an d
ing th e efficacy of th e p rocedu re. Th e classic EC–IC bypass st udy, sect ion ed a few m illim eters aw ay from th e m ain ar ter y to avoid
pu blish ed in 1985, failed to sh ow ben efit for STA–m iddle cere th erm al inju r y. Th e skin in cision sh ould exten d ~ 5 m m below
bral ar ter y (MCA) bypass in pat ien ts w ith sym ptom at ic ICA or th e root of th e zygom a. Th e length of th e STA n eeded for a SCA or
MCA ath erosclerot ic disease n ot am en able to carot id en dar ter PCA bypass is 8 to 10 cm . Th e dissected ar ter y is w rapped in a
ectom y. Th e st udy w as h eavily crit icized for th e lack of h em ody papaverin e soaked cot ton oid to relieve sp asm related to vessel
n am ic select ion criteria. More recen tly, th e results of th e Carot id m an ipulat ion an d is left in con t in u it y u n t il just before it is re
Occlusion Surgery Study (COSS) have been published.56 The study qu ired for th e an astom osis. Altern at ively, th e dist al ar ter y can be
ran dom ized pat ien ts w ith recen t (< 120 days) t ran sien t isch em ic divided an d th e lu m en flu sh ed w ith h eparin ized salin e after a
at tack or h em isp h eric isch em ic st roke in th e territor y of an oc tem porar y clip h as been placed on th e proxim al STA.
clu ded carot id ar ter y an d eviden ce of h em odyn am ic im p airm en t The tem poralis fascia and m uscle can be incised in one of three
on PET to m edical therapy or surgical intervention w ith STA–MCA w ays: (1) lin ear fash ion along th e skin in cision ; (2) T-sh ap ed
bypass. Th e st udy w as prem at u rely h alted based on an in terim fashion, leaving a m uscular cuff along the superior tem poral line;
fu t ilit y an alysis. Th e 2 year p rim ar y ou tcom e rates (all st rokes or (3) C sh ap ed fash ion , based an teriorly leaving a m u scu lar cu ff
an d death s w ith in 30 days of surger y an d ipsilateral isch em ic along th e superior tem poral lin e. We favor th e lat ter. Th e m uscle
st roke w ith in 2 years) w ere n ot st at ist ically sign ifican tly differ is th en dissected off th e squam ou s tem poral bon e in a subperios
en t (21% in th e su rgical grou p an d 22.7% in th e m ed ical grou p), teal fash ion an d ret racted w ith fish h ooks. A stan dard tem poral
prim arily in view of a 15% perioperat ive m orbidit y th at w as too bon e flap for a subtem poral exposu re is perform ed. It is im por
h igh to be overcom e by t h e ben efit of d ecreased su bsequ en t tan t to drill any rem ain ing overh ang of th e squam ous tem poral
st roke rate an d im p roved circu lator y reser ve. It is n ot to be for bon e so t h at t h e cran iotom y is flu sh w it h t h e floor of t h e m id
got ten , h ow ever, th at th e st roke rate in th e surgical group, on ce d le cran ial fossa. Th e dura is th en open ed in a C sh aped fash ion
th e perioperat ive period w as over, decreased sign ifican tly (2.5 based in feriorly an d ret racted w ith 4 0 Nurolon sut ures (Med
fold) com p ared w it h th e m ed ical grou p . Th e su rgical grou p lin e In dust ries, Mun delein , IL).
sh ow ed im provem en t in th eir PET assessed perfusion. Un for t u At th is stage in th e procedure 25 to 50 cc of CSF are released
n ately, th e m edical grou p did n ot h ave repeat PET scan n ing after th ough th e lu m bar drain to ach ieve brain relaxat ion . Un der m i
ran dom izat ion .57 Based on th ese resu lts, EC–IC bypass for p oste croscopic m agn ificat ion th e tem poral lobe is elevated an d bridg
rior circu lat ion isch em ia is h igh ly con t roversial. It sh ou ld on ly be ing vein s from th e in ferior su rface of th e tem poral lobe to th e
con sidered in p at ien t s w ith persisten t h em odyn am ic VBI sym p ten tor iu m are coagu lated an d sacr ificed as n ecessar y. Th e d is
tom s despite m axim al m edical th erapy an d in w h om en dovascu sect ion is con t in u ed u n t il t h e free edge of th e ten tor iu m is
lar th erapy is n ot an opt ion . reach ed. A brain ret ractor m ain t ain s th e su btem poral exposure.
Th e arach n oid of th e am bien t cistern is th en op en ed an d th e SCA
an d PCA iden t ified. It m ay be n ecessar y to divide an d ret ract th e
Superficial Temporal Artery (STA) Bypass
ten torium beh in d th e en t r y of th e t roch lear n er ve in to it s free
Th e STA can be u sed as a don or an d an astom osed to th e SCA or edge to gain access to th e SCA. Th e recip ien t ar ter y is th en d is
PCA. A subtem poral exposure is used. A righ t sided approach is sected to iden t ify a p erforator free zon e for th e an astom osis. A
gen erally preferred to avoid tem poral lobe com plicat ion s on th e rubber dam is th en placed deep to th e dissected segm en t . A m i
dom in ant hem isphere. The patient is positioned lateral or supine crom alleable self suct ion device is placed in th e vicin it y of th e
w ith a sh oulder roll on th e ipsilateral side. Th e h ead is secured in an astom osis to drain CSF an d blood. Th e STA–PCA or STA–SCA
a th ree pin h ead h older an d posit ion ed w ith t w o m ovem en t s: byp ass is t h en p er for m ed in an en d to sid e m an n er as w ill be
(1) con t ralateral rotat ion , so th at th e tem poral region is parallel discu ssed below.
to th e floor; an d (2) dow nw ard t ilt ing of th e ver tex, to allow th e After com plet ion of th e bypass, th e w oun d is closed in layers.
tem p oral lobe to fall aw ay from th e ten torium w ith gravit y. A A slit is created in th e du ra to accom m odate p assage of th e STA.
lu m bar drain facilitates brain relaxat ion an d m in im izes com pli Th e du ra is th en loosely t acked w ith 4–0 Nu rolon st itch es. A
cat ion s related to tem p oral lobe ret ract ion . Th e scalp is sh aved sh eet of DuraGen (In tegra Life Scien ces, Plain sboro, NJ) is placed
an d a por t able Dopp ler p robe is th en u sed to iden t ify th e course over th e dural open ing. A sm all open ing is m ade in th e bon e flap
of th e m ain STA t ru n k n ear th e root of th e zygom a as w ell as th e to en able un com prom ised passage of th e STA. Th e bon e flap is
fron tal an d pariet al bran ch es. th en replaced an d fixed w ith m in iplates an d screw s. Th e w ou n d
Dissect ion of th e STA can be perform ed w ith eith er m icro is cop iou sly ir r igated w it h an t ibiot ic solu t ion . Th e m u scle is
scopic or lou pe m agn ificat ion ; h ow ever, in ou r op in ion , lou p e loosely reapproxim ated w ith 2 0 Vicr yl st itch es, m aking sure n ot
m agn ificat ion is su fficien t an d m ore efficien t . Th e skin in cision to com prom ise th e STA. Th e rost ral par t of th e skin in cision is
is m ade th rough th e epiderm is an d derm is directly over th e ar closed in t w o layers u sing 2 0 inver ted Vicr yl st itch es follow ed
ter y. In cases w h ere th e an terior bran ch w ill be u sed, an altern a by a 3 0 r un n ing locking Prolen e sut ure. Th e caudal par t of th e
t ive to cu t t ing directly over th e ar ter y, w h ich frequen tly resu lts in cision over th e STA is carefu lly closed in on e layer w ith in ter
in th e in cision exten ding in fron t of th e h airlin e, is m aking a cu r r u pted ver t ical m at t ress 3 0 Prolen e su t u re to avoid inju r y or
vilin ear in cision beh in d t h e h airlin e an d d issect in g t h e ar ter y ten sion on th e STA. Su t u res are left in p lace for 2 w eeks. Th e

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23 Surgical Treatment of Vertebrobasilar Insufficiency 309

p at ien t is given an aspirin (325 m g) suppositor y in th e operat ing Occipital Artery Bypass
room prior to ext u bat ion .
Fig. 23.11 sh ow s th e steps of a righ t STA–SCA bypass via a Th e OA can be u sed as a don or an d an astom osed to th e PICA
su btem poral ap proach . Fig. 23.12 sh ow s th e steps of a righ t STA or less com m on ly th e AICA. A lateral suboccipital (ret rosigm oid,
PCA bypass for basilar ar ter y occlu sion . w it h exp osu re of m id lin e at foram en m agn u m ) ap p roach is

a b

c d

Fig. 23.11a–j Surgical steps in a right superficial temporal artery (STA)–


superior cerebellar artery (SCA) bypass. (a) The parietal branch of STA is
dissected, leaving a protective periadventitial fascial cuff. (b) Temporalis
m uscle is retracted anteriorly, the parietal branch of STA is kept in situ
under sponge, and a temporal bone flap is initiated. (c) Intradural subtem -
poral approach, with preservation of vein of Labbé complex (lum bar drain
already placed with cerebrospinal fluid egress). (d) Mobilization of SCA in
the am bient cistern. (e) Placement of background m aterial behind SCA in
e preparation for suturing. (continued on page 310)
(text cont inues on page 313)

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310 III Ischemic Stroke and Vascular Insufficiency

f g

h i

Fig. 23.11a–j (continued ) (f) Longitudinal arteriotomy is placed in SCA,


m easuring 2× the size of the diam eter of the donor vessel. (g) Meticulous
preparation of the distal end of STA, including fish-m outhing on one side.
(h) STA and SCA placed side by side to exactly match the length of the wall
appositions. (i) Following continuous suturing of the back wall with 10-0
Ethilon, the lum en and integrit y of the endothelial surface of the vessel is
inspected prior to suturing the front wall. (j) Completed anastom osis; all
temporary clips are rem oved. The bypass is patent. j

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23 Surgical Treatment of Vertebrobasilar Insufficiency 311

a b

c d

Fig . 23.12a–j A 52-year-old m an with stereot ypical frequent hem ody-


nam ic transient ischem ic at tack (TIAs) in the basilar artery distribution.
(a) Right vertebral artery (RVA) angiogram , anteroposterior view. The RVA
ends in the posterior inferior cerebellar artery (PICA). (b) RVA angiogram ,
lateral view. (c) Left vertebral artery (LVA) angiogram , AP view. The LVA
ends in a very sm all PICA. (d) LVA angiogram , lateral view. (e) Right internal
carotid artery (RICA) angiogram , lateral view. A sm all right posterior com -
m unicating artery (PCoA) fills the top of the basilar artery. (continued on
e page 312)

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312 III Ischemic Stroke and Vascular Insufficiency

Fig. 23.12a–j (continued ) (f) Left internal carotid artery (LICA) angiogram,
lateral view. (g) Surgery: a right temporal craniotomy is garnished. The su-
perficial temporal artery (STA) is divided and isolated. (h) Completed right
STA–posterior cerebral artery anastom osis is demonstrated. (i) Initiation of
dural closure around a completed bypass. (j) Postoperative computed to-
m ography angiogram dem onstrating a patent bypass. j

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23 Surgical Treatment of Vertebrobasilar Insufficiency 313

gen erally u sed, alth ough a far lateral exposu re m ay be n ecessar y th eir origin from t h e OA t r u n k. It is im p or t an t to dissect th e ar
for access to th e AICA. Th e pat ien t is eith er placed pron e or m ore ter y as far proxim ally as th e occipit al groove to en sure adequate
com m on ly in a th ree qu ar ter p ron e or lateral posit ion . Th e h ead lengt h of t h e graft . Th e lengt h of t h e OA n eed ed for a PICA by
is secu red in a th ree pin h ead h older. Pin placem en t is crucial as p ass is ~ 6 cm an d sligh tly longer for an AICA bypass. A tem po
it m ay h in der th e p rocedure if p erform ed im properly. Th e p in s rar y clip is th en placed on th e OA p roxim ally at th e level of th e
are placed so th at th e single pin is 2 cm su perior an d an terior to occipital groove. Th e distal tem porar y clip is th en rem oved an d
th e ear ipsilateral to th e d on or OA. Th e p aired pin s are p osit ion ed th e lu m en flu sh ed w ith h eparin ized salin e. Th e OA is w rap p ed in
so th at th e p osterior p in is 2 cm above th e con t ralateral ear a papaverin e soaked cot ton oid to relieve spasm related to vessel
p in n a. Th e h ead is p osit ion ed above t h e level of t h e h ear t to m an ip u lat ion an d is left u n t il ju st before it is requ ired for t h e
red u ce cerebral ven ou s congest ion . In t h e t h ree qu ar ter p ron e an astom osis.
p osit ion th e h ead is p osit ion ed w it h fou r m ovem en t s: (1) flex An ipsilateral suboccipital cran iotom y exten ding just across
ion w ith sligh t dist ract ion , to u n cover th e suboccipit al region ; th e m idlin e an d a C1 lam in ectom y are p erform ed. Th e cran iot
(2) con t ralateral rotat ion , to bring th e ipsilateral side u pperm ost; om y m ay be exten ded to a far-lateral/par t ial t ran scon dylar ap -
(3) con t ralateral ben d ing, to gain su rgical sp ace bet w een t h e proach by exposu re of th e sigm oid sin u s an d resect ion of th e
ip silateral sh ou lder an d th e su boccipital region ; an d (4) u pw ard posterior m edial th ird of th e occipit al con dyle if n ecessar y. Any
t ran slat ion , to par t ially an d su btly su blu x th e ipsilateral atlan to open ed m astoid air cells m u st be th orough ly sealed w ith bon e
occipit al join t an d facilitate possible con dylar drilling. On th e w ax to avoid postop erat ive CSF leaks. Th e du ra is open ed in th e
oth er h an d, if th e p ron e p osit ion is u sed, th e h ead is posit ion ed m idlin e at th e level of C1 an d exten ded in a cur vilin ear fash ion to
w it h t w o m ovem en t s: (1) flexion w it h sligh t d ist ract ion , to op th e su perolateral exten t of th e exp osu re. An addit ion al in cision
t im ize access to th e posterior fossa; an d (2) sligh t ip silateral ro is m ade from th e cen ter of th e previously m ade dural in cision to
tat ion , to bring th e ip silateral side u pp erm ost . the superom edial extent of the exposure. The dural flaps are then
Th e scalp h air is clipp ed an d a p or t able Dopp ler p robe is th en sut ured to th e su rrou n ding t issu es w ith 4 0 Nurolon su t ures.
u sed to iden t ify th e cou rse of th e OA over th e scalp, from th e Under the operative m icroscope, the ipsilateral cerebellar ton
m astoid to ~ 4 cm above th e superior n uch al lin e. Scalp in filt ra sil is ret racted su perolaterally an d th e cau dal loop of th e PICA
t ion solu t ion s con t ain ing vasocon st rict ive agen ts sh ou ld n ot be id en t ified . We gen erally t r y to avoid u sin g brain ret ractors, as
u sed. A h ockey st ick in cision is th en m ade. Th e in cision st arts t h ey m ay act u ally h in d er t h e su rgical exp osu re. How ever, if re
approxim ately at th e level of th e spin ous process of C3 an d ex t ract ion is n ecessar y, t h en a t ap ered self ret ain in g ret ractor
ten ds superiorly in th e avascular m idlin e plan e to ~ 2 cm above sh ou ld be u sed. Th e cau dal loop is carefu lly dissected by sh arply
th e su p erior n u ch al lin e. Th e in cision is th en t u rn ed laterally dividing th e arach n oidal ad h esion s an ch oring th e ar ter y to th e
parallel to th e su p erior n u ch al lin e. As th is lim b of th e in cision dorsal su rface of th e m edu lla. A bran ch free zon e along th e ar
approach es th e poin t at w h ich th e distal OA crosses th e in cision , ter y is iden t ified an d a r ubber dam is th en placed deep to th e
a cur ved h em ostat is u sed to dissect over an d protect th e OA. Th e dissected cau dal loop of th e PICA. A m icrom alleable self su ct ion
in cision is th en con t in u ed over th e OA to a p oin t im m ediately device is p laced in th e vicin it y of th e an astom osis to drain CSF
sup erior to th e m astoid p rocess. Fin ally, th e in cision is cu r ved an d blood. Th e OA–PICA bypass is th en perform ed in an en d to
in feriorly to en d ju st in ferior to t h e m astoid p rocess. Th e distal side m an n er as w ill be discussed below.
OA is th en iden t ified an d t ran sected bet w een a tem porar y clip If an OA–AICA bypass is the goal, then a retrosigm oid approach
placed on th e proxim al en d an d a Weck clip p laced on th e dist al to th e CPA is n ecessar y. Addit ion al drilling of th e ret rolabyrin
en d . Th e su boccip it al fascia an d m u scles are in cised, leaving a th in e bon e, if n eeded, m ay facilit ate for w ard ing m obilizat ion of
m uscular cuff at tach ed to th e superior n uch al lin e. Th is facili th e sigm oid sin u s, affording m ore room for th e su t u ring to th e
tates t igh t m uscle closure at th e en d of th e procedure as a w ater AICA. Th e occasion al case m ay requ ire a fu ll com bin ed ret rolaby
t igh t du ral closu re is n ot p ossible becau se of th e n ecessit y of rin th in e presigm oid p et rosal ap p roach for p rop er access to th e
creat ing an open ing for th e passage of th e OA. Th e suboccipit al AICA. A conven ien t p erforator free segm en t of th e AICA is iden t i
fascia an d m uscles are th en dissected along th e avascular m id fied an d used as a recipien t for th e OA as described below.
lin e p lan e. Th e su boccip ital m u scu lat u re is sw ept laterally in a After com plet ion of th e bypass th e w oun d is closed in layers.
su bp eriosteal fash ion to exp ose th e occip u t as far laterally as th e Th e du ra is closed w ith or w ith ou t a du ral graft . As previou sly
m astoid process, as w ell as th e arch of C1. Th e skin an d m uscle m en t ion ed , a w ater t igh t d u ral closu re is n ot p ossible becau se
flap are retracted inferolaterally and held in position by fish hooks. of th e n ecessit y of creat ing an open ing for passage of th e OA. A
Th e OA is th en dissected in a dist al to p roxim ally m an n er in sh eet of Du raGen is placed over th e du ral op en ing. A sm all open
its m u scu lar plan e from u n dern eath th e flap . Alth ough th is m ay in g is m ad e in t h e bon e flap to allow u n com p rom ised p assage
be perform ed un der th e operat ive m icroscope, in our opin ion of th e occipit al ar ter y. Th e bon e flap is th en replaced an d fixed
lou pe m agn ificat ion is su fficien t an d m ore efficien t . Dissect ion w ith m in iplates an d screw s. Th e w oun d is copiously irrigated
of th e OA is gen erally th e m ost difficult par t of th e procedu re w ith an t ibiot ic solu tion . Th e m uscle is reapproxim ated to th e
d u e to t h e tor t u osit y an d adh eren ce of t h e ar ter y to t h e su r m uscle cuff along th e superior n u ch al lin e. A m ult ilayer m et icu
rou n d in g t issu es. Th e OA is t yp ically su r rou n d ed by a ven ou s lous closure of th e m uscle an d fascia is cru cial to avoid CSF leaks
p lexu s an d r u n s w it h t h e occip it al n er ve in a fascial sh eath . A and m ay be facilitated by taking the patient out of the flexed posi
gen erou s cu ff of p eriadven t it ial t issu e is left aroun d th e ar ter y. tion . The skin is closed in t w o layers using 2 0 inverted Vicr yl
Sm all side bran ch es are carefu lly coagu lated u sing low cu rren t st itch es follow ed by a 3 0 ru n n ing locking Prolen e su t u re. Su
bipolar forceps, so as n ot to cause th erm al injur y to th e paren t t u res are left in place for 2 w eeks. Th e pat ien t is given an aspirin
ar ter y. Th e side bran ch es are th en sect ion ed at a dist an ce from (325 m g) su ppositor y in th e operat ing room prior to ext u bat ion .

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314 III Ischemic Stroke and Vascular Insufficiency

recipien t ar ter y is also m easured an d gives an in dicat ion of th e


am ou n t of flow t h at is desirable to rep lace or augm en t . On ce
t h e an astom osis h as been com p leted, flow th rough th e don or
ar ter y is m easu red again using a m icrovascular ult rason ic flow
probe (Ch arbel Micro Flow probe, Tran son ic System s, In c., Ith aca,
NY); t h is is kn ow n as t h e “byp ass flow .” Th is m easu rem en t rep
resen ts flow th rough th e bypass an d provides im m ediate verifi
cat ion of bypass paten cy an d adequ acy. Th e rat io of th e bypass
flow m easurem en t to th e cut flow m easu rem en t is kn ow n as th e
cut flow in dex, as in dicated by Ch arbel an d collaborators. Valu es
greater th an 0.5 h ave been foun d to be a sen sit ive predictor for
postoperat ive bypass paten cy.59
Th e recipien t ar ter y is th en prep ared for th e an astom osis.
Min iat u re tem p orar y clips are p laced on eith er side of th e seg
m en t selected for th e an astom osis. Th e pat ien t’s blood pressu re
is raised by 20 to 30%above baselin e du ring th e period of tem po
rary occlu sion . An arteriotom y is in it iated by using a 27 gauge
n eedle or beaver blade an d subsequen tly exten ded using m icro
Fig. 23.13 Right far-lateral approach for a completed occipital artery-to-
posterior inferior cerebellar artery anastom osis. scissors. Heparin ized salin e is u sed to irrigate th e lu m en th rough
ou t t h e cou rse of t h e an astom osis, an d is d elivered t h rough a
syringe t ipped w ith a 25 gauge angiocath eter.
Fig. 23.13 sh ow s th e fin al product of a righ t OA PICA an asto Th e an astom osis m ay be perform ed in several w ays. We pre
m osis via a far lateral ap proach . fer to an ch or t h e h eel (th e fish m ou th ed corn er) of th e d ist al en d
of th e don or ar ter y to on e en d of th e recipien t arteriotom y. On
the other hand, som e surgeons prefer to anchor the toe (th e non–
General Technique of Intracranial End-to -Side
fish m ou th ed corn er) of th e dist al en d of th e don or. Th is allow s
Anastomosis
th e su rgeon to exten d th e fish m ou th ed corn er of th e don or ves
Th e don or vessel (STA or OA) is p repared for th e an astom osis. sel if t h e recip ien t vessel ar ter iotom y h as been m ad e too lon g.
Th e ar ter y is cut distally at an appropriate length for th e bypass. An altern at ive m eth od is to an ch or both th e h eel an d toe of th e
It is crit ical to let th e ar ter y fin d its ow n n at ural con tour after distal en d of th e don or. Th is m eth od is u sefu l as it p reven t s er
dissect ing it , to avoid forcing an u n n at u ral kin k th at m igh t resu lt rors during su t u ring related to un equal dist an ces bet w een su
in graft occlu sion . Th e distal 1 cm of th e arter y is th en st rip ped t ure th row s. Despite th is advan t age, w e prefer n ot to an ch or both
of its periadven t it ial layer. Th ere are several w ays th at th e don or en ds as it decreases th e space available bet w een th e don or an d
vessel can be cut .58 Th e th ree m ost com m on tech n iqu es are (1) a recipien t vessel w alls an d th erefore m akes visualizat ion of th e
st raigh t 90 degree cu t; (2) an angled 45 d egree cu t; an d (3) a in dividual vessel w alls du ring sut u ring difficult .
straigh t 90 degree cut, w ith a single fish m outh on one side w ith Th e an astom osis m ay be perform ed u sing in terr upted st itch es
a length equal to half th e circu m feren ce of th e don or vessel (or, or a con t in u ou s su t u re. Alt h ough in ter r u pted st itch es h ave a
sim ply, th e length of th e “flat ten ed” diam eter of th e collapsed th eoret ical advan t age of allow ing fu t u re en largem en t an d m at u
vessel). We favor th e lat ter tech n iqu e becau se it in creases th e rat ion of th e bypass, w e do n ot believe th is is a pract ical con cern
cross sect ion al area (t w o t im es as com pared w ith a 45 degree u n less th e vessels are p ar t icu larly sm all. Fur th erm ore, w e sut ure
cut , an d four t im es as com pared w ith a 90 degree cut w ith out th e back an d fron t w all of t h e an astom osis sep arately an d th ereby
fish m outh ing) available for th e an astom osis an d provides re allow som e en largem en t of th e byp ass over t im e.
dun dan cy of d on or ar ter y w all. Th is m in im izes th e possibilit y of Th e in it ial an ch oring sut ure is passed from outside to in side
sten osis at th e site of an astom osis. In ou r op in ion , th e en d to the vessel, th en inside to outside the oth er vessel, so th at th e final
side an astom oses gen erally fare bet ter if an “elep h an t foot” de kn ot lies outside of th e arterial lum en . Th e an astom osis proceeds
sign is ach ieved, w ith th e redu n dan t edges of th e don or allow ing by first su t u ring th e m ore d ifficu lt back w all. Care is t aken to
a flaring of th e com pleted an astom osis an d a reduced risk of ste avoid grasping th e vessel w all as it m ay dam age th e in t im a. Th e
n osis or occlu sion . Fu r t h er m ore, t h e obliqu it y of t h e resu lt ing forceps sh ould be used to gen tly an ch or th e ar ter y as th e n eedle
con st r u ct allow s flow to be p referen t ially d irected p roxim ally is passed th rough th e vessel w all. Th e su t ure is kept loose be
tow ard th e basilar ar ter y. In addit ion to fish m ou th ing, w e often t w een st itch es like th e sp iral bin ding of a book u n t il th e en t ire
“roun d” or sligh tly excise th e sh arp corn ers of th e 90 degree back w all of the anastom osis has been sutured. The suture is then
fish m outh angles to facilitate run n ing th e su t ure, as w e w ill de t igh ten ed on e loop at a t im e using t w o forceps st ar t ing from th e
scribe below. in it ial an ch oring su t u re. Th e fin al loop is th en t ied dow n . On ce
Follow ing th e lead of Ch arbel et al,50 w e rout in ely m ake de th e back w all h as been su t u red, th e don or ar ter y is flip ped to
t ailed m easu rem en t s of blood flow in don or an d recip ien t ar expose th e fron t w all. On e t akes th is op port u n it y to in sp ect th e
ter ies during bypass surgeries. Th e “cu t flow,” or th e m axim al en dolum in al in tegrit y of th e com pleted sut ure lin e. A n ew an
flow car r yin g cap acit y of t h e d on or in t h e absen ce of d ow n ch oring su t u re is p laced an d th e fron t w all is t h en su t u red in a
st ream resist an ce, is first m easu red . Th e baselin e flow in t h e sim ilar m an n er. Th e lu m en of th e recipien t is filled w ith h ep a

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23 Surgical Treatment of Vertebrobasilar Insufficiency 315

rin ized salin e prior to com plet ion of th e fin al st itch . Th e an asto m obilized tow ard each oth er. Blood flow th rough both ar teries is
m osis is perform ed using a 10 0 m on ofilam en t sut ure. We prefer m easu red u sing a m icrovascu lar u lt rason ic flow p robe (Ch arbel
a BV or V t ype t aper poin t n eedle, n um bered 70 3 or 75 3 (Eth i Micro Flow p robe) A sm all p iece of Gelfoam an d a r u bber dam
con , Joh n son & Joh n son , New Br u n sw ick, NJ). Th e n eedle form s are p assed ben eath th e PICA loop s to gen tly elevate th e ar teries.
th ree eigh th s of a circle an d th erefore m in im izes th e degree of Min i tem porar y clips are applied proxim al an d distal to th e
w rist rotat ion requ ired during sut uring as com pared w ith n ee site of an astom osis. Th e p at ien t’s blood p ressu re is raised by 20
dles form ing on e h alf of a circle. to 30% above baselin e d u r ing t h e p er iod of tem p orar y occlu
Blood flow is restored after com p let ion of t h e an astom osis sion . An ar teriotom y is in it ially m ade using a 27 gauge n eedle or
by first rem ovin g t h e tem p orar y clip s on t h e recip ien t ar ter y beaver blade an d subsequ en tly exten ded u sing m icroscissors.
follow ed by th e don or ar ter y. Sligh t oozing along th e sut ure lin e Th e length of th e ar teriotom y sh ou ld be at least t w o to th ree
u sually stops w ith a single layer of Surgicel an d gen tle pressu re t im es th e diam eter of th e PICA vessel. Fu r th erm ore, if on e im ag
w ith a cot ton oid ap plied over th e ar teriotom y. Occasion ally it in es both vessels side by side in cross sect ion sim u lat ing th e
m ay be n ecessar y to place an addit ion al sut ure if th e bleeding faces of t w o clocks, th e an astom osis is m ore easily perform ed if
d oes n ot ter m in ate w ith ligh t p ressu re. A fin al assessm en t of th e ar teriotom y is m ad e at th e 1:30 o’clock an d 10:30 o’clock
vessel paten cy is m ade w ith a h an d h eld Doppler probe, or pref position s, as op posed to th e 3 o’clock an d 9 o’clock p osit ion s, or
erably a qu an t it at ive flow p robe. In t raoperat ive angiography or th e 12 o’clock posit ion s (Fig. 23.14). Hep arin ized salin e is u sed
in docyan in e green videoangiograp hy m ay also be u sed. to irrigate th e lum en th rough ou t th e course of th e an astom osis,
an d is delivered th rough a syringe t ipped w ith a 25 gauge angio
cath eter. Th e an astom osis is p erform ed u sing a ru n n ing 10 0
Intracranial-to -Intracranial Bypass m on ofilam en t sut ure. First th e back w all of th e an astom osis is
su t u red. An an ch oring su t u re is m ade at th e cran ial apex of th e
This m ethod applies to the PICA–PICA and the very rare PCA–SCA
ar teriotom y. As alw ays, it goes ou t in (in on e vessel, gen erally th e
byp ass. We discu ss th e form er.
righ t PICA for a righ t h an ded su rgeon ), th en in ou t (in th e oth er
vessel, th e left PICA for a righ t h an ded surgeon ), result ing in th e
kn ot being m ade on th e outside. Th e n eedle is th en passed u n
PICA–PICA (Side -to -Side) Bypass
dern eath th e kn ot an d brough t in to th e sp ace bet w een th e t w o
A PICA–PICA bypass can be perform ed for VBI in th e rare sit u a vessels. Th e r un n ing sut ure is th en begu n by passing th e n eedle
t ion th at on e VA is occlu d ed p roxim al to t h e PICA an d t h e con from ou t in th rough on e ar ter y (again th e left PICA for th e righ t
t ralateral VA en ds in th e PICA. Preoperat ive im aging is u sed to h an ded surgeon ) an d th en in out th rough th e oth er. Th e loops
determ in e th e d ist an ce bet w een both PICAs. Th e m in im al dis are th erefore form ed on e after an oth er un t il th e 6 o’clock apex is
tan ce bet w een th e righ t an d left PICA sh ou ld ideally be less th at reach ed. Th ere th e n eedle is passed from in out on on e side an d
4 to 5 m m to perm it safe m obilizat ion of th e PICAs w ith out ex th en ou t in on t h e oth er, an d t h en a fin al t im e in ou t on th e fron t
cessive t ract ion on th e m ain ar ter y or its perforat ing bran ch es. w all. Th e loop s of th e ru n n ing su t u re are th en serially t igh ten ed
Th e procedu re is p erform ed th rough a m idlin e su boccip it al cra from th e in it ial an ch oring kn ot as w e described previously. Th e
n iotom y an d C1 lam in ectom y. Th e du ra is open ed in a Y-sh aped final loop is then tied, keeping the knot on the outside. The lum en
fash ion . Follow ing a th orough arach n oidal dissect ion , th e righ t in flush ed w ith salin e an d in spected. Th is is th e last ch an ce to
an d left cerebellar ton sils are gen tly elevated an d th e exposure correct any im p erfect ion s in th e su t u re lin e. A n ew an ch oring
m ain tain ed w ith self retain ing ret ractors. Th e ton sillom edu llar y su t u re is th en p laced at th e 12 o’clock p osit ion at th e fron t w all
and telovelotonsillar segm ents of the PICA are then dissected and an d th e easier fron t w alls are th en sut ured in a sim ilar m an n er
in spected for a p erforator free zon e. Th e arteries are th en gen tly (Fig. 23.15).

Fig. 23.14 Conceptual explanation of the ideal placement


of arteriotom ies in a side-to-side anastom osis. If both ves-
sels are im agined in cross section as representing the
faces of t wo clocks, the arteriotom ies should be placed at
1:30 (on the left) and 10:30 (on the right). This is the best
comprom ise bet ween the best view (yet worse wall ap-
position) of the 12–12 o’clock position, and the best wall
apposition (yet worse view) of the 3–9 o’clock position.

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316 III Ischemic Stroke and Vascular Insufficiency

Fig . 23.15a– d Idealized schem atic of a side-to-side


anastom osis. (a) Initial apical stitch placed (out-in-in-out
sequence) at a 12 o’clock im aginary position (clock im ag-
ined facing the surgeon). (b) Initial apical stitch tied, and
then—a critical step—the needle is passed behind the
completed tie to initiate the running of the back wall. A
right-handed surgeon would start on the left wall (out-in)
just below the apical stitch. (c) Completed running of the
back wall. The suture is tied to itself at the 6 o’clock posi-
tion. (d) Easier running of the front wall, with a new suture
started at the 12 o’clock position again, going toward to
6 o’clock position.

a b

c d

Th e tem porary clips are first rem oved distal and th en proxim al by coagulat ing an d rem oving th e surroun ding ven ous plexus. An
to th e anastom osis. A fin al assessm en t of vessel p aten cy is m ade ipsilateral suboccipital craniotom y and a C1 lam inectom y are then
w ith a h an d h eld Doppler probe, quan t itat ive flow probe, in t ra perform ed. Th e cran iotom y sh ou ld exten d from ju st beyon d th e
operat ive angiograp hy, or in docyan in e green videoangiography. m idline to the sigm oid sinus and include rem oval of the posterior
Fig. 23.16 sh ow s th e steps of a PICA–PICA side to side bypass rim of th e foram en m agn u m an d p ossibly th e m ed ial th ird of th e
perform ed in the m idline bet ween the telovelotonsillar segm ents ipsilateral occipit al con dyle. Th e du ra is op en ed in a C sh aped
of both PICAs. fash ion based tow ard th e sigm oid sin us an d cen tered at th e level
of the foram en m agnum . The ipsilateral cerebellar tonsil is ele
vated, exposing th e in t racran ial VA an d low er cran ial n er ves. Sec
Intracranial Vertebral Endarterectomy t ion ing th e first t w o den tate ligam en ts an d lateral m obilizat ion
Th e in d icat ion s for in t racran ial ver tebral en dar terectom y are of th e spin al accessor y n er ve facilitate exposure of th e VA. Tem
ext rem ely lim ited in view of cu rren tly available en d ovascu lar porary occlusion of the involved VA segm ent is then perform ed. The
tech n iques. How ever, th e procedure m ay st ill be con sidered for proxim al clip m ay be ap p lied ext ra or in t radu rally an d th e distal
in t racran ial VA sten osis p roxim al to th e PICA in cases th at are n ot clip is ap plied ju st p roxim al to th e PICA. An ar teriotom y is th en
am en able to en dovascular th erapy. perform ed an d th e p laque dissected from th e w all of th e ar ter y.
Th e procedu re is p erform ed via a far lateral ap p roach an d a Th e ar teriotom y is th en closed u sing an 8 0 or 9 0 m on ofilam en t
h ockey st ick in cision (see above). Th e VA is exposed ext radurally sut ure after en su ring th at all in t im al tags h ave been rem oved.

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a b

e
f

Fig. 23.16a–g A posterior inferior cerebellar artery (PICA)–PICA side-to-


side bypass. (a) Through a m idline suboccipital craniotomy, the right and
left telovelotonsillar loops of both PICAs are m obilized and prepared for
side-to-side anastom osis. (b) Planned arteriotomy sites are m arked with
ink on both sides, with a length about 2× the size of the PICA diam eter.
(c) Four temporary clips are placed as distant as possible from the anasto-
m osis site, without comprom ising the perforators. (d) Back wall suturing is
alm ost complete. Individual loops are left loose on purpose to be tightened
prior to t ying the suture to itself. (e) Back wall suturing is com pleted.
(f) Front wall suturing is alm ost complete. Note that the loose continuous
loops (prior to tightening) resem ble the spiral binding of a notebook.
(g ) Anastom osis is com pleted, and all clips are rem oved. The bypass is
g patent.

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318 III Ischemic Stroke and Vascular Insufficiency

recen t fin dings of th e SAMMPRIS t rial dem on st rat ing t h at in t ra


■ Conclusion cran ial sten t ing is in ferior in both efficacy an d safet y com pared
Today su rgical t reat m en t of VBI m ay be con sid ered by m any to w ith best m edical th erapy. Credit sh ou ld be given to im proved
be a relic from a bygon e era. Its ut ilit y h as in deed con t in ued to ph arm acological m edical treatm ent for atherosclerosis in general
dw in dle over th e years because of t w o m ain factors: th e un cer over th e past 20 years. Th e realm of surgical in dicat ion s h as in
tain role of revascu larizat ion in isch em ic disease in gen eral (for deed sh ru n k bu t n ot disap peared. Sp ecialized cerebrovascu lar
both an terior an d posterior circu lat ion ), as w ell as th e adven t of m icrosurgeon s w ith in tellect ual an d tech n ical skills to recogn ize
a m uch easier an d safer m eth od to accom plish th e goal w h en an d operate on th is pat ien t group are st ill n eeded. We h ope th at
in dicated, n am ely th rough th e en dovascu lar route. Th ere w ill re th is review of su rgical tech n iqu es w ill h elp th e in terested reader
m ain the occasional patient, how ever, w hose vertebrobasilar dis st ay cu rren t on w h at h as been don e in th e p ast an d can st ill be
ease process is such th at surger y is sim ply th e t reat m en t m eth od don e today, w ith addit ion al im provem en t s an d m odern t w ist s.
of last resor t . Th is is of p ar t icu lar sign ifican ce in view of t h e

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24 Endovascular Treatment of
Vertebrobasilar Insufficiency
Ram sey Ashour and Moham m ad Ali Aziz-Sultan

cien cy, leads to ar terial n arrow ing th at m ay progress to h em o


■ Pathophysiology and Natural History dyn am ically sign ifican t sten osis, leading to superim posed in sit u
Ver tebrobasilar in su fficien cy is a clin ical syn d rom e resu lt ing th rom bosis, or resu lt in dist al em boli, any of w h ich , alon e or in
from posterior circu lat ion isch em ia du e to n u m erou s p oten t ial com bin at ion , m ay be exp ressed clin ically as p osterior circu lat ion
cau ses (see text box). t ran sien t isch em ic at t acks (TIAs) or st roke.3 Microath erom atou s
occlusion of sm all perforat ing arteries m ay also occur, par t icu
larly in th e set t ing of ch ron ic hyper ten sion , result ing in lacun ar
Pathophysiology of Vertebrobasilar Ischemia brain stem in farct ion .4 Less com m on bu t w ell recogn ized cau ses
of ver tebrobasilar in su fficien cy in clu d e ver tebral ar ter y d issec
Embolic source t ion ,5 ext r in sic ver tebral ar ter y com p ression (e.g., by sp in al os
• Heart teop hytes),6 h igh flow ar ter ioven ou s fist u las,7 an d su bclavian
• Aortic arch steal syn drom e,8 w h ereby blood is sh un ted aw ay from th e poste
• Subclavian artery rior circu lat ion ret rograde dow n th e ver tebral ar ter y to provide
• Vertebral artery flow to th e upper ext rem it y in th e face of subclavian arter y ste
Large-vessel atherosclerosis n osis sit u ated proxim al to th e vertebral ar ter y origin .
• In situ thrombosis Alth ough posterior circulat ion st rokes accoun t for 30% of all
• Flow-limiting stenosis isch em ic st rokes in large regist ries,1,9,10 th e n at u ral h istor y of
Small-vessel microatheromatous occlusion sym ptom at ic ver tebrobasilar ath erosclerosis is n ot as w ell st u d
• Lacunar infarction ied or u n derstood as com p ared w ith an terior circulat ion (i.e., ca
Vertebral artery dissection rot id) disease. In th e Warfarin Aspirin Sym ptom at ic In t racran ial
• Spontaneous Disease (WASID) t rial,11 th e largest p rospect ive st u dy to date
• Traumatic evalu at ing m edical th erapy for in t racran ial ath erosclerosis, th e
Vertebral artery compression rate of ver tebrobasilar st roke in p at ien ts w ith in t racran ial verte
• Spinal osteophytes brobasilar disease w as 8.7% per year. In addit ion to th is prospec
• Soft tissue bands t ive t rial, variou s ret rospect ive st u dies in dicate th at th e rates of
• Bow-hunter’s syndrome isch em ic st roke in pat ien t s w ith sym ptom at ic in t racran ial ver te
Vascular steal syndrom e brobasilar ath erosclerosis are com parable to th ose in pat ien t s
• Subclavian stenosis/occlusion proximal to vertebral artery w ith sym ptom at ic in t racran ial an terior circulat ion disease.12–14
origin On th e oth er h an d, n eu rologic m orbidit y an d m or talit y appear
• High-flow arteriovenous fistulas involving the vertebral h igh er after posterior circulat ion st roke as com pared w ith an te
artery rior circu lat ion st roke,11,15 reflect ing th e vit al im p or t an ce of th e
Others brain stem an d it s vascular sup ply.
• Vasculitis/inflammatory disorders As w ith int racranial disease, the nat ural histor y of extracran ial
• Fibromuscular dysplasia ver tebral ar ter y ath erosclerosis requires fur th er st udy. Ext racra
• Orthostatic hypotension n ial ver tebral ar ter y ath erosclerosis often involves th e origin or
proxim al aspect of th e vessel an d is th e secon d m ost com m on
site of sten osis after th e carot id bifu rcat ion in isch em ic st roke
Posterior circu lat ion st rokes m ost com m on ly result from em boli p at ien t s.16 Un like cer vical carot id at h erosclerosis, at h eroscle
that arise from th e h ear t , aor t ic arch , su bclavian ar ter y, or proxi rot ic plaques h ave been rep or ted to be sm oot h er an d less pron e
m al ver tebral ar ter y.1 Not ably, becau se th e basilar ar ter y is larger to ulcerat ion in th e set t ing of ext racran ial ver tebral ar ter y dis
th an eith er ver tebral ar ter y alon e, an em bolu s th at is able to t ra ease.16,17 In th e New Englan d Medical Cen ter Posterior Circu la
verse th e ver tebral arter y ten d s to m ake it all th e w ay u p to an d t ion Regist r y, ext racran ial ver tebral ar ter y at h erosclerosis w as
becom e lodged at th e top of th e basilar arter y.2 In t racran ial ath con sid ered a con t r ibu t in g factor in 10 to 20%of p oster ior circu
erosclerosis, an ot h er com m on cau se of ver tebrobasilar in su ffi lat ion st rokes 1 ; h ow ever, in th e largest prospect ive ran dom ized

320

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24 Endovascular Treatm ent of Vertebrobasilar Insufficiency 321

t rial com p aring en dovascu lar versu s m edical th erapy for sym p
tom atic vertebral stenosis, the Carotid And Vertebral Arter y Trans
lum in al Angioplast y St u dy (CAVATAS) invest igators reported n o
ver tebrobasilar st rokes in eith er group over a m ean follow up
of 4.7 years.18 Fu r th erm ore, th e largest ret rospect ive n at u ral h is
tor y st udy of pat ien ts w ith proxim al ver tebral ar ter y sten osis
yielded a posterior circu lat ion st roke rate of on ly 0.4%per year.19
Alth ough it is clear th at th ese p at ien t s are at h igh er risk for st roke
in gen eral d ue to con com itan t carot id territor y disease, th e n at u
ral h istor y an d best m an agem en t of ext racran ial vertebral arter y
ath erosclerot ic sten osis rem ain to be defin ed.

■ Relevant Anatomy
Th e left an d righ t ver tebral ar teries t yp ically arise as th e first
bran ch of th eir respect ive subclavian ar teries; un com m on but
w ell recogn ized variat ion s m ay occur, su ch as a direct aort ic arch
origin of th e left ver tebral ar ter y or a com m on origin of th e righ t
ver tebral an d righ t com m on carot id ar teries. Each vertebral ar
ter y th en courses superom edially to approach an d en ter th e C6
t ran sverse foram en (V1 segm en t), ascen ds ver t ically th rough th e
cer vical t ran sverse foram in a (V2 segm en t), exits th e C2 t ran s
verse foram en , ascen d s t h rough t h e C1 t ran sverse foram en ,
cu r vin g first p oster iorly alon g t h e C1 ver tebral arch an d t h en
an teriorly an d superiorly tow ard th e foram en m agn um (V3 seg
m en t), an d pierces th e du ra as it con t in ues for w ard in t racran i
ally (V4 segm en t) to un ite w ith th e con t ralateral ver tebral ar ter y
at th e p on tom edu llar y ju n ct ion , form ing th e basilar ar ter y (Fig.
24.1). A ch aracterist ic tor t uosit y com posed of t w o righ t angle
t u rn s as th e ver tebral ar ter y t ravels bet w een C2 an d C1 (Fig.
24.2) en ables vessel redun dan cy to accom m odate h ead t urn ing
an d m akes angiop last y an d sten t in g t argeted to t h is sp ecific re
gion m ore challenging. Extradural branches of the vertebral arter y
in clude th e posterior m en ingeal arter y, w h ich t ypically arises
from t h e V3 segm en t , an d m u lt iple sm all cer vical segm en t al
(e.g., m uscular) bran ch es, w h ich origin ate from th e V2 segm en t .
In th e face of ext racran ial occlusive ver tebral ar ter y disease,
th ese an d oth er ext radu ral bran ch es becom e p oten t ial rou tes for
collateral blood flow bet w een th e extern al carot id an d ver tebro
basilar circu lat ion s. In t radural bran ch es of th e ver tebral ar ter y
in clu de t h e posterior in ferior cerebellar arter y (PICA), th e an te
rior sp in al ar ter y (ASA), an d th e posterior sp in al ar ter y (PSA)
(Fig. 24.3). Th e left ver tebral ar ter y is con sidered “dom in an t” in
50% of cases; oth er w ise, th e righ t ver tebral ar ter y is dom in an t
(25%) or codom in an t ver tebral ar teries are presen t (25%).16 Oc-
casion ally, on e ver tebral ar ter y m ay term in ate in a n orm al sized Fig . 24.1 The cervical vertebral arteries each t ypically arise from their
PICA or it m ay be hyp op last ic t h rough ou t it s cou rse. In su ch respective subclavian artery (SCL) and travel superom edially to enter the
cases, w h en on e ver tebral ar ter y con st it u tes t h e sole su p p ly to transverse foram ina of the cervical spine. V1 is the initial extraforam inal
th e basilar circu lat ion , it s p ath ological or iat rogen ic occlu sion segm ent running from the subclavian artery up to the transverse foram en
of C6, V2 is the foram inal segm ent bet ween C6 and C2, and V3 begins as
often carries devastat ing con sequen ces.
the artery exits the C2 transverse foram en and ends as the artery pierces
Th e basilar ar ter y ascen ds in fron t of an d su p plies th e pon s the dura to becom e the intracranial V4 segment. BA, basilar artery; PICA,
an d m idbrain via m ultiple param edian an d sh or t circum ferent ial posterior inferior cerebellar artery; SCL, subclavian artery. (Courtesy of Bar-
perforators. Long circu m feren t ial bran ch es su p ply th e brain stem row Neurological Institute.)

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322 III Ischemic Stroke and Vascular Insufficiency

Fig. 24.2 The vertebral artery runs posteriorly along the


arch of C1 and through the suboccipital triangle before
curving anteriorly and superiorly to enter the foram en
m agnum . CN, cranial nerve; VA, vertebral artery. (Cour-
tesy of Barrow Neurological Institute.)

as w ell as th e cerebellum an d in clude th e paired an terior in ferior im portan t su p p ly to t h e rost ral m id brain an d m ed ial d ien cep h
cerebellar ar teries (AICAs) at th e m idpon t in e level as w ell as th e alon . Th e posterior com m un icat ing ar teries (PCoAs) con n ect to
paired su perior cerebellar ar teries (SCAs) at th e p on tom esen ce th e PCAs in fron t of th e cerebral p edu n cles, an d in th e face of
phalic junction. The basilar artery bifurcates at the level of the in ver tebrobasilar occlusive disease th ey can ser ve as im por tan t
terpedun cular cistern in to th e paired posterior cerebral ar teries sou rces of collateral flow eith er p roxim ally dow n th e basilar ar
(PCAs). Th e p oster ior t h alam op er forators ar ise from t h e top of ter y in a ret rograde fash ion or distally to th e su praten torial PCA
t h e basilar ar ter y as w ell as t h e p roxim al PCAs an d con t r ibu te territories.

a b

Fig. 24.3a,b (a) The intracranial vertebral arteries unite at the pontomed- AICA, anterior inferior cerebellar artery; ASA, anterior spinal artery; BA,
ullary junction to form the basilar artery, which ascends along the pons, giv- basilar artery; CN III, oculom otor nerve; CN IV, trochlear nerve; ICA, internal
ing off m ultiple param edian and short circum ferential perforators as well as carotid artery; MCA, m iddle cerebral artery; PCA, posterior cerebral artery;
t wo nam ed long circumferential branches: the anterior inferior cerebellar PCoA, posterior com m unicating artery; PICA, posterior inferior cerebellar
and superior cerebellar arteries. (b) The basilar artery bifurcates into the artery; PSA, posterior spinal artery; SCA, superior cerebellar artery; VA, ver-
bilateral posterior cerebral arteries at the level of the interpeduncular cis- tebral artery. (Courtesy of Barrow Neurological Institute.)
tern. ACA, anterior cerebral artery; ACoA, anterior comm unicating artery;

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24 Endovascular Treatm ent of Vertebrobasilar Insufficiency 323

■ Clinical Presentation • Neuromuscular disease


• Tumor
Ver tebrobasilar in sufficien cy produces m ult iple sym ptom s an d
• Paraneoplastic syndrome
sign s dep en ding on th e locat ion of th e offen ding path ology (see
• Cavernous sinus pathology (e.g., carotid-cavernous fistula,
text box).
Tolosa-Hunt syndrom e)
• Ocular pathology (e.g., Graves’ disease)
Vertebrobasilar Ischemic Symptoms and Signs • Infection (e.g., syphilis, tuberculosis)

• Decreased consciousness
• Syncope W h en t ran sien t sym ptom s occu r over t im e, especially vagu e
• Nausea/vomiting sym ptom s such as syncope or dizziness, th e diagn osis of vertebro
• Visual field deficit basilar insufficiency is m ore difficult to m ake as com pared w ith
• Pupillary abnorm alities th e acu te, dram at ic set t ing of a st roke. Sp ecial at ten t ion sh ou ld
• Diplopia/ophthalmoparesis be given to th e t im e an d rapidit y of sym ptom on set , clin ical pro
• Facial numbness/weakness gression or im provem en t , t reat m en t s at tem pted, cardiovascu lar
• Vertigo/dizziness risk factors, gen eral m edical con dit ion , baselin e cogn it ive an d
• Hearing loss n eurologic fu n ct ion , su rgical h istor y, bleeding problem s, h istor y
• Horner’s syndrome of t raum a, illicit drug u se, an d oth er relevan t factors.
• Dysarthria/dysphonia In p at ien t s p resen t ing acu tely w it h a su sp ected isch em ic
• Dysphagia n eu rologic deficit , a n on con t rast com puted tom ography (CT)
• Dysgeusia scan of th e brain is first p erform ed p rim arily to exclu de h em or
• Gait/limb ataxia rh age. Addit ion al fin dings to n ote on th e in it ial CT scan in clude
• Extremit y weakness/num bness ver tebrobasilar dolich oect asia, vessel calcificat ion s, ch ron ic en
cephalom alacia, generalized atrophy, hyperdense basilar sign sug
gest ive of acute th rom bus, an d hypoden se in farcted brain t issue
Dizzin ess, ver t igo, h eadach e, vision loss, dou ble vision , n u m b in delayed cases (> 6 h ours). After con sid erat ion of several fac
n ess, w eakn ess, in coordin at ion , slurred speech , sw allow ing dif tors, intravenous recom binant tissue t ype plasm in ogen activator
ficult y, an d loss of con sciou sn ess are am ong th e m ost com m on (r t PA) m ay or m ay n ot be adm in istered prior to fur th er radio
clin ical m an ifest at ion s. Fu r th erm ore, bilateral m otor or sen sor y graph ic evaluat ion .
loss, cerebellar sym ptom s/sign s, an d crossed long t ract an d cra After th e in it ial CT scan , m agn et ic reson an ce im aging/angiog
n ial n er ve dysfun ct ion are all h allm arks of ver tebrobasilar isch raphy (MRI/MRA) is th en p erform ed to bet ter evaluate for st roke
em ia. Mu lt ip le eponym ou s ver tebrobasilar st roke syn drom es are an d to assess th e paten cy of th e relevan t vasculat ure. Due to th e
w ell recognized by neurologic specialists and h ave been review ed con fin ed an atom y of t h e p oster ior fossa, p er fu sion MRI is less
elsew h ere 20 ; h ow ever, pat ien ts rarely p resen t w ith th e pu re con h elpful for dem on st rat ing diffusion –perfusion m ism atch in ver
stellat ion of fin dings for a given syn drom e. Dep en ding on th e tebrobasilar as op p osed to an ter ior circu lat ion isch em ia; t h u s
et iology, sym ptom s m ay be t ran sien t or perm an en t , fluct uat ing blood flow m easurem en t via quan t it at ive MRA is curren tly being
or progressive (t ypically in a stepw ise fash ion ), m ild or severe, st u d ied as an alter n at ive m et h od to evalu ate ver tebrobasilar
but alw ays su dden an d episodic, reflect ing th e “vascular” n at ure isch em ia.21 In cases of acu te large vessel occlu sion , th e decision
of th e problem . to perform cerebral angiography an d possible en dovascular re
vascu larizat ion is based on several factors in cluding th e clin ical
st at u s of th e p at ien t , size an d locat ion of th e st roke, locat ion an d
m orph ological feat u res of th e occluded vessel, t im e sin ce sym p
■ Perioperative Evaluation tom on set , an d oth er relevan t factors.
W h en p at ien t s presen t w ith rep et it ive ver tebrobasilar TIAs or
In pat ien t s presen t ing w ith sym ptom s an d sign s of posterior cir
a st roke outside of th e acute ph ase, m an agem en t is cen tered on
culat ion isch em ia, a det ailed h istor y an d physical exam in at ion
preven t ing fu t u re st rokes. A m ore th orough evalu at ion is often
often en able an atom ic localizat ion of th e problem to th e ver te
u n der t aken in clu ding m edical w orku p , cardiac test ing, vest ibu
brobasilar territor y an d facilit ate n arrow ing dow n an oth er w ise
lar testing, neck u ltrasoun d, tran scran ial Doppler, cerebral perfu
broad differen t ial of poten t ial n on isch em ic causes (see text box).
sion im aging (e.g., single photon em ission com puted tom ography
[SPECT], p osit ron em ission tom ograp hy [PET]), an d oth ers. On ce
Differential Diagnosis of Vertebrobasilar Insufficiency the diagnosis of vertebrobasilar in sufficiency is firm ly establish ed
an d ch aracterized radiograp h ically, en dovascu lar m an agem en t
• Labyrinthitis is t ypically reser ved for p at ien t s w h o fail “best” m edical th erapy,
• Vestibular neuronitis w h ich is a con t roversial topic in an d of it self.
• Meniere’s disease
• Benign paroxysmal positional vertigo
• Vestibular schwannoma
• Migraine ■ Treatment Options
• Cardiogenic syncope
• Demyelinating disease Th e en dovascu lar t reat m en t opt ion s for ver tebrobasilar in su ffi
cien cy depen d on th e t im ing an d cause of sym ptom s. For acute

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324 III Ischemic Stroke and Vascular Insufficiency

st roke, in t ra ar terial t PA an d m ech an ical th rom bolysis u sing fluoroscopic m arkers to en sure opt im al posit ion across th e ste
a variet y of devices are th e m ain en dovascular tools used to n osis (Fig. 24.4). Th e sten t sh ou ld exten d at least 3 m m p roxim al
ach ieve recan alizat ion of an occluded vessel, an d are discussed an d d ist al to t h e sten osis, an d it s d iam eter sh ou ld be ch osen to
elsew h ere in th e text . Here w e focu s on en dovascu lar opt ion s for m atch t h e n or m al vessel caliber adjacen t to th e sten osed seg
treating vertebrobasilar insufficiency due to atherosclerosis caus m en t . Th e sten t is carefu lly d ep loyed by stead ily u n sh eat h in g it .
ing (1) in t racran ial basilar or ver tebral ar ter y sten osis, (2) ext ra Post sten t balloon angioplast y sh ould be con sidered if th ere re
cranial vertebral arter y stenosis, and (3) subclavian steal. We also m ain s sign ifican t sten osis after sten t ing. After fin al angiograph ic
briefly discuss th e in frequen t role of en dovascular in ter ven t ion run s are obt ain ed, all cath eters an d w ires are rem oved, an d a
for (4) ver tebral ar ter y d issect ion an d (5) h igh flow ar ter iove percu tan eou s closu re device is u sed to close th e fem oral ar teri
n ou s fist u las. otom y at th e con clusion of th e procedu re.
In addit ion to th e st an dard risks of angiography, balloon an
gioplast y an d sten t ing in pat ien ts w ith ath erosclerot ic basilar
Endovascular Techniques stenosis carries the added risks of procedure related em boli, stent
t h rom bosis/occlu sion , vessel d issect ion or r u pt u re (Fig. 24.5),
Balloon Angioplasty and Stenting : Basilar Artery Stenosis
occlu sion of basilar p er forators by d isp lacem en t of at h eroscle
We in it iate du al an t ip latelet th erapy by p rescribing asp irin (325 rot ic m ater ial d u r in g an giop last y/sten t in g (“sn ow p low in g” ef
m g) an d Plavix (75 m g) by m ou th daily for at least 5 days p rior to fect), an d reperfu sion h em orrh age, am ong oth ers. Th e text box
sten t ing. Con sciou s sedat ion m ay be con sidered for cooperat ive below lists avoidan ce m easu res for various com plicat ion s en
pat ien ts an d offers th e advan tage of allow ing for in t raprocedu ral cou n tered du ring en dovascu lar in ter ven t ion for ver tebrobasilar
n eu rologic exam in at ion ; h ow ever, gen eral an est h esia en ables disease.
ph arm acological p aralysis, w h ich en sures excellen t fluoroscopic
visualizat ion an d elim in ates p at ien t m ovem en t .
Th e p at ien t is p osit ion ed su p in e w it h t h e h ead secu red in
n eu t ral posit ion . Th e left an d righ t groin are asept ically prepared Endovascular Intervention for Vertebrobasilar
an d draped allow ing for bilateral percutan eou s fem oral access if Insufficiency—Complication Types and
n eeded. All cath eters an d sh eath s are con n ected to a con t in u ous Avoidance Measures
flu sh of h eparin ized salin e. A 6 Fren ch (F) vascular sh eath is first Procedure-related emboli
n avigated in to th e descen ding th oracic aor t a an d t arget su bcla • Initiate systemic anticoagulation upon insertion of vascular
vian arter y via a st an dard percu t an eou s t ran sfem oral approach . sheath.
System ic an t icoagulat ion is in it iated using in t raven ous h eparin • Confirm therapeutic heparinization (activated clot ting time
to ach ieve an d m ain tain an act ivated clot t ing t im e of 250 to 300 250 to 300 seconds) prior to intervention and hourly
secon d s th rough ou t th e proced u re. A 6F gu ide cath eter is th en thereafter.
in t rodu ced th rough th e sh eath an d m an euvered in to th e target • Consider continuing intravenous heparin drip 12 to 24
cer vical ver tebral ar ter y, an d w orking angiograph ic view s are hours postprocedure.
obtain ed . Altern at ively, diagn ost ic angiograp hy can first be per Stent throm bosis
form ed u sing 5F cath eters, par t icularly if th e decision to perform • Dual antiplatelet therapy should be started at least 5 days
an interven tion has n ot been firm ly established preprocedure; 6F prior to stenting.
cath eters can th en be in t rodu ced for in ter ven t ion as n eeded. • If early stent thrombosis is detected during procedure,
A m icrocath eter is in troduced th rough th e 6F guide cath eter consider intra-arterial infusion of platelet aggregation
an d carefu lly n avigated over a m icrow ire in to th e basilar ar ter y inhibitor (e.g., abcixim ab).
an d across t h e sten osis u n d er su bt racted road m ap gu idan ce. Iatrogenic vessel dissection
On ce t h e m icrocat h eter is p osit ion ed d ist al to t h e sten osis, an • Use over-the-wire technique under subtracted roadmap
exch ange length m icrow ire is in t rodu ced an d u sed to m ain t ain guidance for selective vertebral artery catheterization.
w ire access to th e t arget vessel distal to th e sten osis. Th e m icro • Perform subclavian artery angiogram to evaluate vertebral
cath eter is th en carefu lly rem oved . Th e exch ange length w ire artery origin prior to selective catheterization.
n ow ser ves as th e con duit over w h ich an angioplast y balloon or Vessel rupture/perforation
a sten t can be in t rodu ced across th e sten osis. • Undersize angioplast y balloon to 80% of vessel diameter.
Pre sten t balloon angiop last y sh ou ld be perform ed if th e ste • Device insertion and rem oval over an exchange-length
n osis is so severe th at it w ould oth er w ise m ake it difficult for th e wire is a t wo-person technique requiring good
sten t it self to cross th e sten osis. Th e Gatew ay balloon (Boston com m unication.
Scien t ific, Marlborough , MA) sh ou ld be un dersized to 80% of th e • Prior to device insertion/removal over exchange-length
target vessel diam eter, as recom m en ded by th e m an ufact urer, to wire, release forward tension in the system to prevent wire
lessen th e risk of vessel w all inju r y or p erforat ion . Th e balloon is from jum ping forward.
navigated across the stenosis, carefully inflated under fluoroscopic Hemorrhage
visu alizat ion u sing an in su fflator prim ed w ith 70:30 con t rast/ • Ensure blood pressure control during and after procedure.
salin e m ixt ure, m aintained in position for a few secon ds, and then • Keep protamine immediately available during procedure
slow ly deflated . Follow u p angiograp hy is th en p erform ed an d for heparin reversal in the event of vessel perforation.
angiop last y repeated as n ecessar y. • Consider temporary flow arrest via balloon inflation across
After rem oval of t h e balloon , t h e W ingsp an sten t (Boston perforation.
Scien t ific) is in t rodu ced over th e exch ange length w ire u sing it s

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24 Endovascular Treatm ent of Vertebrobasilar Insufficiency 325
Fig. 24.4a–d (a) Angiographic im age in a patient with
vertebrobasilar transient ischem ic at tacks showing severe
basilar stenosis. (b) Lateral intraprocedural angiographic
image illustrating the exchange-length wire positioned
distally within the superior cerebellar artery. Fluoroscopic
markers (arrows) indicate the position of a balloon that
has been introduced over the wire across the stenosis to
perform angioplast y prior to stent deployment. Im m edi-
ate (c) and 6-m onth follow-up (d) angiographic im ages
dem onstrate resolution of the stenosis, and the stent it-
self can also be seen (arrows).

a b

c d

Patient Outcomes
Th e Sten t ing versu s Aggressive Medical Man agem en t for Pre
ven t ing Recurren t st roke in In t racran ial Sten osis (SAMMPRIS) 22
st u dy w as a ran dom ized con t rolled t rial com paring aggressive
m edical th erapy an d angioplast y/sten t ing for severe (70–99%)
sym ptom at ic in t racran ial ath erosclerot ic sten osis. Th e t rial w as
stop p ed early after en rollm en t of 451 p at ien t s becau se th e 30
day st roke or d eath rate in th e sten ted grou p w as 14.7% as com
pared w ith 5.8%in the m edically treated group (p = 0.002). Beyon d
30 days, th e st roke rate in th e affected territor y w as equivalen t
bet w een th e t w o groups at 1 year follow u p. Th e auth ors n oted
th at periprocedu ral st roke rates in t h e sten ted grou p w ere h igh er
than previously reported in the pretrial regist ries 23,24 ; in addition,
the st roke rates w ere low er than expected in the m edically treated
group as com p ared, for exam ple, w ith th e WASID t rial.11
As exp ected , con cern s h ave been raised in th e literat u re to
explain th e “n egat ive” resu lt of SAMMPRIS.25,26 Never th eless, in
ligh t of th e dat a, m om en t u m h as sign ifican tly sh ifted aw ay from
sten t in g for in t racran ial at h erosclerot ic d isease. As h as been
poin ted ou t ,26 th e fact th at 12.2%of m edically t reated p at ien t s at
1 year m et th e prim ar y en d poin t (any st roke/death w ith in 30
days or affected territor y st roke after 30 days) suggest s th ere is
sign ifican t room for im provem en t in th e m an agem en t of in t ra
Fig. 24.5 Left vertebral artery angiogram im m ediately after deploym ent
cran ial ath erosclerot ic disease. As n ew er gen erat ion devices are of a stent in the presence of severe basilar artery atherosclerosis. There is
develop ed, p ar t icu larly devices w ith a single step deliver y sys diffuse extravasation of contrast consistent with catastrophic intraproce-
tem th at do n ot require th e use of an exch ange length w ire, it is dural rupture of the basilar artery secondary to oversizing of the stent.

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326 III Ischemic Stroke and Vascular Insufficiency

possible th at p erip rocedu ral m orbidit y cou ld be sign ifican tly re w ith in t racran ial ath erosclerot ic or ext racran ial ver tebral sten o
duced. Nevertheless, at this point in tim e, stenting for sym ptom atic sis. In th e su bset of pat ien ts w ith ext racran ial ver tebral ar ter y
in t racranial ath erosclerot ic disease sh ou ld be reser ved for th ose sten osis (n = 18), th e st roke rate at 1 year after t reat m en t w as
pat ien ts w ith severe sten osis for w h om m edical th erapy fails. 11%, an d th e resten osis rate at 6 m on th s w as 43%; for ver tebral
ost ial lesion s, th e resten osis rate w as 67%. How ever, th e m ajorit y
of pat ien ts w ith resten osis rem ain ed clin ically asym ptom at ic.
Balloon-Mounted Stent: Vertebral Artery Origin Stenosis
Th e CAVATAS st udy in corporated th ree separate ran dom ized
Th e set u p an d tech n iqu e for ext racran ial vertebral ar ter y sten t t rials, on e of w h ich ran dom ized pat ien t s w ith sym ptom at ic ver
ing are sim ilar to th ose described for in t racran ial sten t ing. Pre tebral ar ter y sten osis (n = 16) to receive eith er en dovascular or
t reat m en t w ith du al an t ip latelet th erapy is u t ilized. Th e n eed for m edical t reat m en t .18 Of eigh t p at ien t s t reated en dovascularly,
gen eral an esth esia an d ph arm acological paralysis is less w ith six u n der w en t angioplast y alon e an d on ly t w o u n der w en t sten t
ext racranial as com pared w ith intracran ial stenting, and our pref placem en t . No pat ien t in eith er grou p exp erien ced a vertebro
eren ce is to p erform th ese p rocedu res u t ilizing con sciou s seda basilar territor y st roke at m ean follow up of 4.7 years; h ow ever,
t ion . After p lacem en t of a 6F gu id in g cat h eter in to t h e t arget th e st udy w as clearly un derpow ered to dem on st rate a ben efit of
su bclavian ar ter y, a m icrocath eter is n avigated over a m icrow ire t reat m en t .
across th e sten osis an d in to th e dist al cer vical ver tebral ar ter y. Alt h ough ext racran ial ver tebral ar ter y sten osis is clearly a
Th e m icrow ire is rem oved, an d an exch ange length m icrow ire is m arker for in creased st roke r isk d u e to carot id ar ter y d isease,
in t rodu ced to m ain t ain access across th e sten osis as th e m icro it s relat ion sh ip to ver tebrobasilar ter r itor y st roke is less evi
cath eter is t h en carefu lly rem oved . A balloon m ou n ted sten t is d en t 1,19,29 ; t h u s, en dovascu lar t reat m en t sh ou ld be reser ved for
th en in t rodu ced over th e w ire across th e sten osis. Th e sten t di sym ptom at ic p at ien t s w ith severe sten osis w h o fail m edical
am eter sh ould be ch osen to m atch th e n orm al vessel diam eter th erapy, par t icularly th ose in w h om th e involved ver tebral ar
adjacen t to th e sten osis; h ow ever, sligh t oversizing of th e sten t is ter y con stit utes th e sole m ajor supply to th e posterior circula
preferable to en su re adequ ate vessel w all ap posit ion an d to ac t ion . Su rgical opt ion s (e.g., ver tebral carot id t ran sposit ion ) for
com m odate par t ial sten t recoil. Th e sten t is dep loyed by in flat ing ext racran ial ver tebral ar ter y sten osis are m ore du rable bu t also
th e balloon for 15 to 30 secon ds an d th en deflat ing it; rep eat m ore invasive th an angioplast y an d sten t ing; th ey h ave been ut i
angioplast y can be perform ed as n eeded (Fig. 24.6). In cases of lized w ith su ccess in w ell selected pat ien t s 30–32 an d are review ed
ver tebral origin sten osis w ith con com itan t severe ath erosclero elsew h ere in th e text .
sis of th e su bclavian ar ter y itself, th e sten t sh ou ld be sized an d
dep loyed su ch th at it s p roxim al en d p rot ru des sligh tly in to th e
Angioplasty and Stenting : Subclavian Steal
lu m en of t h e su bclavian ar ter y, to avoid p roxim al occlu sion of
th e sten t .27 In p at ien t s w ith su bclavian ar ter y sten osis, if a st an dard p ercu
t an eou s t ran sfem oral ap p roach to t h e lesion is n ot feasible, a
ret rograd e t ran srad ial ar ter y ap p roach can be u sed . Pre sten t
Patient Outcomes
angiop last y is t yp ically requ ired w h en t h e sten osis is severe
Th e Sten t in g of Sym ptom at ic At h erosclerot ic Lesion s in t h e en ough to h ave cau sed sym ptom s, an d occasion ally angiop last y
Ver tebral or In t racran ial Ar teries (SSYLVIA) st udy 28 w as a n on - u sing a sm aller balloon m u st first be perform ed sim ply to allow
ran dom ized, m ult icen ter, p rospect ive safet y an d feasibilit y st u dy th e lesion to be crossed by a larger balloon , sized to th e n orm al
evalu at ing t h e NEUROLINK (Gu idan t Cor p ., Men lo Park, CA) vessel diam eter. Both balloon m ounted and self expanding stents
balloon m oun ted sten t system for use in sym ptom at ic pat ien ts h ave been used w ith success to t reat subclavian sten osis; n eith er

a b c

Fig. 24.6a–c Left (a) and right (b) subclavian artery angiogram s dem on- infarction. (c) Final postprocedure angiographic im age after angioplast y
strating severe left vertebral artery origin stenosis and right vertebral ar- and balloon-m ounted stent deploym ent dem onstrating resolution of the
tery occlusion, respectively, in a patient presenting with right cerebellar stenosis. Arrows depict the position of the stent.

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24 Endovascular Treatm ent of Vertebrobasilar Insufficiency 327

t ype h as been clearly sh ow n su perior to th e oth er.33 Alth ough


balloon m ou n ted sten ts are perh aps easier to deploy and exh ibit
vir t u ally n o foresh or ten ing, self expan ding sten t s are m ore flex
ible by design an d are w ell suited for use in com m on ly tort u ous
su bclavian an atom y. Ver tebral ar ter y p rotect ion , for exam ple by
using a filter device, h as been don e du ring proxim al su bclavian
ar ter y angiop last y/sten t in g to red u ce t h e p roced u ral em bolic
risk 34,35 ; h ow ever, th e u t ilit y of th is m an euver rem ain s to be es
tablish ed. In deed, ver tebral ar ter y flow reversal follow ing angio
plast y for su bclavian steal h as been sh ow n to occu r in a delayed
fash ion , often t akin g several m in u tes, w h ich ser ves to red u ce a b
t h e im m ed iate risk of em boli reach ing th e posterior circu lat ion
after in ter ven t ion .36 Com plete subclavian occlusion m ay also be
t reated en dovascu larly via m ech an ical th rom bectom y follow ed
by angioplast y an d sten t ing (Fig. 24.7) 37 ; h ow ever, difficult y t ra
versing th e occlusion is reflected in low er rates of t reat m en t suc
cess as com p ared w ith p aten t bu t sten otic lesion s.38,39

Patient Outcomes
Angioplast y alon e for subclavian sten osis is associated w ith h igh
rates of clin ical im provem en t bu t also w ith h igh rates of long c d
term resten osis; h ow ever, radiograph ic resten osis is often clin i
cally silen t . Th e addit ion of sten t ing im p roves th e du rabilit y of
t reat m en t w h ile adding m in im al m orbidit y an d is often th e first
lin e t reat m en t . Alth ough overall 5 year p aten cy rates after an
gioplast y an d sten t ing are low er th an th ose reported for open
surgical bypass (70% vs 96%, respect ively),40–42 surgical m orbidit y
(6–28.9%) an d m or t alit y (0–2.2%) rem ain h igh er th an en dovas
cular m orbidit y (2–11.4%) an d m or talit y (0–1%).33

Vertebral Artery Dissection


e f
Ver tebral ar ter y dissect ion , w h eth er t raum at ic or spon tan eous,
is t ypically t reated m edically via an t icoagu lat ion or an t iplatelet
agents to prevent em bolic ischem ic even ts. Balloon m ounted and
self expan dable sten ts h ave been u sed relat ively in frequ en tly to
t reat ext racran ial ver tebral ar ter y d issect ion , w ith good tech n i
cal resu lt s an d low p roced u re related com p licat ion rates.43–47
Given th e sm all n um ber of pat ien t s t reated, th e role of sten t ing
for ver tebral dissect ion rem ain s to be defin ed, an d sh ou ld be re
ser ved for pat ien ts in w h om m edical th erapy is in effect ive or
con t rain dicated or w h en th e dissect ion cau ses flow lim it ing ste
n osis an d th e involved ver tebral ar ter y is th e sole m ajor supply g h
to th e posterior circu lat ion .
Fig. 24.7a–h (a) Angiogram dem onstrating near-complete left subcla-
vian artery occlusion proximal to the origin of the left vertebral artery in a
High-Flow Arteriovenous Fistulas Involving the wom an presenting with vertebrobasilar insufficiency and arm claudication.
Vertebral Artery Right vertebral artery early cervical (b), intracranial (c), and delayed cervi-
cal (d) angiographic runs demonstrate antegrade flow up the right verte-
High flow ar terioven ou s fist u las th at involve on e or both verte bral artery followed by retrograde flow down the left vertebral artery into
bral ar teries can produce vascular steal aw ay from th e posterior the left subclavian artery. Arrows depict the direction of flow, consistent
circulat ion , resu lt ing in isch em ia an d m ay be congen ital, t rau with subclavian steal. Fluoroscopic im ages demonstrate the pre-stent an-
m at ic, iat rogen ic, or idiopath ic acquired lesion s (Fig. 24.8). Al- gioplast y balloon fully inflated (e), the post-stent angioplast y balloon fully
th ough th ese fist u las are an u n com m on cau se of ver tebrobasilar inflated (f), and the final position of the self-expanding stent that was
deployed (g) (arrows). (h) Final postprocedure angiographic im age dem -
in sufficien cy, th ey are im por tan t to recogn ize, because clin ical
onstrates resolution of the stenosis and norm alization of antegrade flow
im provem en t after su ccessful th erapy is often rapid an d st riking. within the left vertebral artery. Arrows depict the final position of the stent.
Sp ecific en dovascu lar t reat m en t opt ion s in clu de (1) t ran sar terial
or t ran sven ous em bolizat ion to obliterate th e fist ula, w h ich w e
t ypically p erform using a liquid em bolic agen t; (2) vertebral ar
ter y sacrifice using coils deployed w ith in th e vessel lum en across

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328 III Ischemic Stroke and Vascular Insufficiency

Fig . 24.8a– d Early- (a) and late-phase (b) right verte-


bral artery angiogram s dem onstrating a recurrent, high-
flow arteriovenous fistula involving the left vertebral artery
draining into a dilated posterior cervical venous pouch.
The patient originally presented with vertebrobasilar in-
sufficiency and had undergone m ultiple previous trans-
arterial em bolizations. After direct puncture and em boli-
zation through the venous pouch (c), the fistula rem ained
obliterated on the 6-m onth follow-up angiogram (d).

a b

c d

th e fist u lou s p oin t; an d (3) deploym en t of a covered sten t w ith in am eliorate the offending stenosis in patients w ith atherosclerosis.
th e vertebral arter y across th e fist u lou s p oin t to ach ieve flow Less com m on set t ings th at occasion ally w arran t en dovascular
d iversion aw ay from t h e fist u la w h ile p reser ving th e p aren t th erapy in clu de ver tebral ar ter y dissect ion or h igh flow arterio
ar ter y. Th e decision to u se an en dovascu lar, op en surgical, or ven ou s fist ulas involving th e ver tebral ar ter y causing posterior
com bin ed ap p roach dep en ds on several factors, discu ssed m ore circulation ischem ia. The procedural techniques, stents used, bal
fu lly elsew h ere in th e text , in clu ding th e locat ion , size, m orph ol loon s used, ou tcom es, an d com plicat ion risks differ som ew h at
ogy, an d com p lexit y of th e fist u la in addit ion to th e clin ical sta depending on the site of inter vention (int racranial vertebrobasilar
t u s of th e pat ien t . Close longit u din al radiograph ic follow u p is vs extracranial vertebral vs subclavian); n evertheless, endovascu
n ecessar y after t reat m en t to detect lesion recu rren ce, w h ich is lar treatm en t of vertebrobasilar in sufficien cy sh ould be reser ved
n ot u n com m on after en dovascu lar in ter ven t ion alon e. for sym ptom at ic p at ien t s in w h om m a xim al m ed ical th erapy is
ineffective w ith rare exception, regardless of the offending pathol
ogy. Even in the face of im proving m edical th erapy, as reflected by
the SAMMPRIS trial, endovascular in ter vention continues to re
m ain a usefu l tool in a su bset of w ell selected pat ien t s an d sh ould
■ Conclusion n ot be aban don ed. How ever, fut ure endovascular techn iques an d
En dovascu lar t reat m en t of ver tebrobasilar in su fficien cy cen ters devices m ust be rigorously st udied and scrut inized to define their
u pon balloon angioplast y u sed in com bin at ion w ith sten t ing to role in th e sch em e of th erapy for vertebrobasilar disease.

References
1. Caplan LR, Wit yk RJ, Glass TA, et al. New Englan d Medical Cen ter Posterior 6. Hard in CA, W illiam son W P, Steegm an n AT. Ver tebral ar ter y in su ffi
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2626 8. Fish er CM. A n ew vascular syndrom e—th e subclavian steal. N Engl J Med
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10. Moulin T, Tat u L, Vuillier F, Berger E, Ch avot D, Rum bach L. Role of a st roke 29. St aym an AN, Nogueira RG, Gu pt a R. A system at ic review of sten t ing an d
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com e of 1,776 con secut ive pat ien t s from the Besan çon st roke regist r y. 2011;42:2212–2216
Cerebrovasc Dis 2000;10:261–271 30. Berguer R, Feldm an AJ. Surgical recon st r uct ion of th e ver tebral ar ter y.
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and aspirin for sym ptom at ic in t racran ial ar terial sten osis. N Engl J Med brobasilar in sufficien cy. Par t 1: Microsurgical t reat m en t of ext racran ial
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595–601 31(1 Pt 1):9–18
13. Qureshi AI, Ziai WC, Yah ia AM, et al. St roke free su r vival an d it s deter 33. Aiello F, Mor r issey NJ. Op en an d en dovascu lar m an agem en t of su bcla
m in an t s in pat ien t s w ith sym ptom at ic ver tebrobasilar sten osis: a m u lt i vian an d in n om in ate ar terial path ology. Sem in Vasc Surg 2011;24:31–35
cen ter st udy. Neurosurger y 2003;52:1033–1039, discu ssion 1039–1040 34. Mich ael TT, Ban erjee S, Brilakis E. Subclavian ar ter y in ter ven t ion w ith
14. Moufarrij NA, Lit tle JR, Furlan AJ, Leath erm an JR, William s GW. Basilar vertebral em bolic protect ion . Cath eter Cardiovasc Inter v 2009;74:22–25
an d dist al vertebral arter y sten osis: long term follow up . St roke 1986;17: 35. St iefel MF, Park MS, McDougall CG, Albuqu erque FC. En dovascular t reat
938–942 m en t of in n om in ate arter y occlusion w ith sim ult an eous ver tebral an d
15. De Marchis GM, Koh ler A, Ren z N, et al. Posterior versus an terior circula carot id ar ter y dist al protect ion : case repor t . Neurosurger y 2010;66:E843–
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ist ics. J Neurol Neurosurg Psychiat r y 2011;82:33–37 36. Ringelstein EB, Zeum er H. Delayed reversal of ver tebral ar ter y blood flow
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n osis. QJM 2003;96:27–54 drom e. Neu roradiology 1984;26:189–198
17. Im parato AM, Riles TS, Kim GE. Cer vical ver tebral angioplast y for brain 37. Dayam a A, Riesen m an PJ, Ch eek RA, Kasirajan K. En dovascular m an age
stem isch em ia. Su rger y 1981;90:842–852 m en t of aor t ic arch vessel occlusion : successful revascu larizat ion of in
18. Cow ard LJ, McCabe DJ, Ederle J, Feath erstone RL, Clifton A, Brow n MM; n om in ate an d left subclavian arteries. Vasc En dovascu lar Surg 2012;46:
CAVATAS Invest igators. Long term outcom e after angioplast y an d sten t 273–276
ing for sym ptom at ic vertebral arter y sten osis com pared w ith m edical 38. Sixt S, Rast an A, Sch w arzw älder U, et al. Result s after balloon angioplast y
t reat m en t in th e Carot id An d Ver tebral Ar ter y Tran slum in al Angioplast y or sten t ing of ath erosclerot ic subclavian ar ter y obst ru ct ion . Cath eter Car
Study (CAVATAS): a ran dom ized trial. Stroke 2007;38:1526–1530 diovasc In ter v 2009;73:395–403
19. Moufarrij NA, Lit tle JR, Furlan AJ, William s G, Marzew ski DJ. Ver tebral ar 39. Lin n i K, Ugurluoglu A, Mader N, Hit zl W, Magom et sch n igg H, Hölzenbein
ter y stenosis: long term follow up. St roke 1984;15:260–263 TJ. En d ovascu lar m an agem en t versu s su rger y for proxim al su bclavian ar
20. Wolf JK. The Classical Brain stem Syn drom es. Springfield, IL: Ch arles C ter y lesions. An n Vasc Surg 2008;22:769–775
Th om as; 1971 40. AbuRah m a AF, Bates MC, Ston e PA, et al. Angioplast y an d sten t ing versus
21. Am in Hanjan i S, Rose Fin nell L, Rich ardson D, et al; VERiTAS St udy Group. carot id subclavian bypass for th e t reat m en t of isolated subclavian ar ter y
Ver tebrobasilar Flow Evaluat ion an d Risk of Tran sient Isch aem ic At t ack disease. J En dovasc Th er 2007;14:698–704
an d St roke st u dy (VERiTAS): rat ion ale an d design . In t J St roke 2010;5:499– 41. Palch ik E, Bakken AM, Wolford HY, Saad W E, Davies MG. Su bclavian ar
505 ter y revascu larizat ion : an outcom e an alysis based on m ode of th erapy
22. Ch im ow it z MI, Lyn n MJ, Derdeyn CP, et al; SAMMPRIS Trial Invest igators. an d presen t ing sym ptom s. Ann Vasc Surg 2008;22:70–78
Sten t ing versu s aggressive m ed ical th erapy for in t racran ial ar terial sten o- 42. Modarai B, Ali T, Dourado R, Reidy JF, Taylor PR, Burn an d KG. Com parison
sis. N Engl J Med 2011;365:993–1003 of ext ra an atom ic bypass graft ing w ith angioplast y for ath erosclerot ic
23. Zaidat OO, Kluczn ik R, Alexan der MJ, et al; NIH Mult i cen ter Wingspan disease of th e supra aort ic t r un ks. Br J Surg 2004;91:1453–1457
In t racran ial Stent Regist r y St udy Group. Th e NIH regist r y on use of the 43. Coh en JE, Gom ori JM, Um an sky F. En dovascular m anagem en t of sym p
Wingspan stent for sym ptom at ic 70 99% in t racran ial arterial sten osis. tom at ic vertebral ar ter y dissect ion ach ieved using sten t angioplast y and
Neurology 2008;70:1518–1524 em boli protect ion device. Neurol Res 2003;25:418–422
24. Bose A, Har t m an n M, Hen kes H, et al. A n ovel, self expan ding, n it in ol 44. Coh en JE, Gom ori JM, Um an sky F. En dovascular m an agem en t of spon t a
sten t in m ed ically refractor y in t racran ial ath erosclerot ic sten oses: th e n eous bilateral sym ptom at ic ver tebral ar ter y dissect ion s. AJNR Am J Neu
Wingspan st udy. St roke 2007;38:1531–1537 roradiol 2003;24:2052–2056
25. Abou Ch ebl A, Stein m et z H. Crit ique of “Sten t ing versus aggressive m edi 45. Lee YJ, Ah n JY, Han IB, Ch ung YS, Hong CK, Joo JY. Th erapeut ic en dovascu
cal th erapy for int racran ial arterial sten osis” by Ch im ow it z et al in th e lar t reat m en t s for t raum at ic vertebral ar ter y injuries. J Traum a 2007;62:
new Englan d Jou rn al of Medicin e. St roke 2012;43:616–620 886–891
26. Marks MP. Is th ere a fu t ure for en dovascular t reat m en t of in t racran ial ath 46. Price RF, Sellar R, Leung C, O’Su llivan MJ. Traum at ic ver tebral ar terial dis
erosclerot ic disease after Sten t ing an d Aggressive Medical Man agem en t sect ion an d ver tebrobasilar ar terial throm bosis successfully t reated w ith
for Preven t ing Recurren t St roke an d Int racranial Sten osis (SAMMPRIS)? en dovascular th rom bolysis an d sten t ing. AJNR Am J Neuroradiol 1998;
St roke 2012;43:580–584 19:1677–1680
27. Cloud GC, Craw ley F, Clifton A, McCabe DJ, Brow n MM, Markus HS. Ver te 47. Ph am MH, Rah m e RJ, Arn aou t O, et al. En dovascular sten t ing of ext ra
bral arter y origin angioplast y an d prim ar y sten t ing: safet y an d resten osis cran ial carot id an d ver tebral arter y dissect ion s: a system at ic review of
rates in a prospect ive series. J Neurol Neurosurg Psych iat r y 2003;74:586– th e literat u re. Neu rosu rger y 2011;68:856–866, discu ssion 866
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28. SSYLVIA St udy Invest igators. Sten t ing of Sym ptom at ic Ath erosclerot ic Le
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St roke 2004;35:1388–1392

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25 Medical Management of Intracranial
Athero -Occlusive Disease
Shakeel A. Chow dhry and Peter Nak aji

Sten o-occlu sive disease of th e in t racran ial ar teries rep resen ts a fin d in g t h at is con sisten t w it h dat a from t h e War far in -Asp ir in
sign ifican t sou rce of m orbidit y both in th e Un ited St ates an d Sym ptom at ic In t racran ial Disease (WASID) t rial an d ot h er p ro -
w orldw ide. Th e u n derlying p ath ophysiology is varied; th e m ain spect ive t rials (Fig. 25.1).17
cau ses in clu de ath erosclerot ic disease, ar terial dissect ion , m oya- Th e risk of st roke in th e sam e vascu lar dist ribu t ion as a sym p -
m oya angiopathy, an d em bolic disease. Th is ch apter discu sses tom at ic IA sten osis is 11% in th e first year overall, bu t n early
th e m edical m an agem en t of in t racran ial ath erosclerot ic disease. t w ice as h igh if th e sym ptom at ic sten osis is greater th an 70%.20
Th ese n u m bers suggest a m u ch h igh er st roke risk th an p rior pro-
spect ive st udies, such as th e ext racran ial to in t racran ial (EC–IC)
bypass t rial of th e EC/IC Bypass St udy Group, w h ich foun d th at
pat ien ts w ith carot id sip h on an d m idd le cerebral ar ter y (MCA)
■ History and Pathophysiology sten osis receiving m edical t reat m en t w ith m odificat ion of risk
St roke is th e th ird leading cau se of death in th e Un ited States an d factors an d 1,300 m g p er day of asp ir in h ave an an n u al st roke
th e leading cau se of disabilit y. Isch em ic st roke accou n ts for 85% r isk of 8 to 10%.21 Th e p revalen ce of coexisten t asym ptom at ic
of all cerebrovascular acciden ts, an d in t racran ial ath erosclerot ic IA in pat ien ts w ith sym ptom at ic IA is fairly h igh , w ith a 19%
sten osis is believed to accou n t for 8 to 10%of isch em ic st rokes in prevalen ce by angiograp hy of asym ptom at ic IA w ith sten osis
th e Un ited St ates (resu lt ing in 60,000 st rokes p er year).1–6 Several m easuring > 50%. Speculat ion regarding cu m ulat ive st roke risk
st u d ies h ave provided d em ograph ic in form at ion on sym ptom - in pat ien ts w ith con com it an t asym ptom at ic IA is m ade in several
at ic in t racran ial ath erosclerot ic disease. Th e racial an d dem o- ret rospect ive st u dies, an d subset an alyses of prosp ect ive st udies
grap h ic dist ribu t ion is u n equ al, w ith in t racran ial ath erosclerosis suggest a low risk of st roke from asym ptom at ic in t racran ial ste-
accoun t ing for 6 to 29% of st rokes in blacks, 22 to 26% in Asian s, n osis com p ared w ith previou sly sym ptom at ic lesion s.22,23
an d up to 11% of st rokes in people of Hispan ic descen t . Accord- Subset analyses of data from the WASID trials and several other
ingly, in oth er region s of th e w orld, in t racran ial ath erosclerosis st udies fou n d th at pat ien t s at risk for sym ptom at ic in t racran ial
(IA) is believed to play a m ore sign ifican t role in isch em ic st roke stenosis share com m on cardiovascular risk factors including prior
t h an in th e Un ites St ates, accou n t in g for 30 to 50% of st rokes in cerebral isch em ic even t , prior cardiac isch em ic even t , hyper ten -
Asia.7–13 Alt h ough m en are m ore often affected , w om en w it h sion , d iabetes, hyp erlip idem ia, an d sm oking.20,24 Addit ion al risk
sym ptom at ic in t racran ial sten osis are at h igh er risk for recu rren t factors for st roke in clude exten t of in t racran ial sten osis, addi-
isch em ic st roke, alth ough dat a are con fou n ded by sign ifican t dif- t ion al presen ce of asym ptom at ic IA, p resen ce of a sym ptom at ic
feren ces in socioecon om ic stat u s.14 lesion (i.e., Nat ion al In st it u tes of Healt h St roke Scale [NIHSS]
Few data exist regarding the prevalence of asym ptom at ic in tra- score > 1), m et abolic syn d rom e, h em odyn am ically sign ifican t
cran ial ath erosclerot ic disease, an d th e m ajorit y of st u dies in th e sten osis, an d progressive MCA sten osis.20,25
literat ure involve subset s of pat ien t s w ith sym ptom at ic disease. How ever, th e m an agem en t of in t racran ial ath erosclerot ic dis-
Analysis of th e North Am erican Sym ptom atic Carotid En darterec- ease varies from cardiac disease due to fun dam en t al differen ces
tom y Trial (NASCET) data revealed eviden ce of m ild in t racran ial in toleran ce of th e en d organ an d key h istological an d an atom ic
at h erosclerot ic d isease (d efin ed as w all ir regu lar it ies w it h ou t differen ces bet w een cran ial an d coron ar y ar teries. Th e cerebral
sten osis) in 26.9% of p at ien t s, m od erate d isease w ith sten osis ar ter y, in addit ion to it s sm aller caliber an d th in n er w alls, h as n o
m easuring less th an 50%in 5.8%of pat ien ts, an d greater th an 50% extern al elast ic lam in a, less adven t it ia, an d relat ively m ore t u -
sten osis in 0.5% of pat ien t s.15 A st u dy in Sp ain fou n d a 9% preva- nica m edia. Th ese ch aracteristics in part m ay predispose cerebral
len ce of asym ptom at ic IA am ong pat ien t s w ith m oderate to h igh ar teries to a h igh er risk of vasospasm an d rupt u re th an coron ar y
vascu lar risk.16 Based on dat a from st u dies of sym ptom at ic p a- vascu lat ure.
t ien ts, h alf of ath erosclerot ic plaqu es are fou n d in th e in t racra- Intracranial atherosclerotic disease m ay lead to ischem ic events
n ial in tern al carot id ar teries. th rough on e of several p rocesses: (1) hyp op erfu sion , (2) th rom -
Th e n at u ral h istor y of IA disease rem ain s poorly u n d erstood. bus form at ion at th e site of sten osis, (3) th rom boem bolism , or
Studies involving IA m onitoring, m ostly through transcranial Dop - (4) occlu sion of p er forat ing ar ter ies. Em bolic even t s are p u n c-
pler ult rason ograp hy or conven t ion al angiography, h ave sh ow n t u ated by su d d en on set of a (relat ively) fixed d eficit . Hyp op er-
th at in t racran ial sten oses m ay u n dergo p rogression , rem ain st a- fu sion , h ow ever, is associated w it h flu ct u at ing sym ptom s t h at
ble, or even undergo regression .1,17,18 A m eta-an alysis suggests im prove w ith in creased blood pressu re. In p ract ice, sym ptom
th at th e an n u al ip silateral st roke risk for p at ien t s w ith IA ranges m an ifest at ion m ay involve m ore th an on e of th ese path ophysio-
from 3.1 to 8.1%.19 Th e risk of st roke for p osterior circu lat ion IA logical pathways. Unstable plaque m orphology m ay m anifest w ith
does n ot ap pear to be h igh er th an for an terior circu lat ion IA, a th rom bosis at th e site of sten osis or th rom boem bolism .

330

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25 Medical Management of Intracranial Athero-Occlusive Disease 331

(COSS) u t ilized PET to m easu re oxygen ext ract ion fract ion to
assess cerebral reser ve.29

■ Medical Management: Data and Trials


Historically, w arfarin w as th e m ain st ay for t reat m en t of sym p -
tom at ic in t racran ial vascular disease. Th is paradigm w as sup -
por ted by several ret rosp ect ive st u dies suggest ing a ben efit of
w arfarin over an t ip latelet m edicat ion .30,31 How ever, th e WASID
t rial, a large ret rospect ive st u dy, ch allenged th ese fin dings, an d
th e su bsequ en t Nat ion al In st it u tes of Health (NIH)-fu n ded, ran -
dom ized, prosp ect ive, dou ble-blin d, m u lt icen ter US st u dy (com -
paring w arfarin an d aspirin for sym ptom atic in t racran ial ar terial
sten osis) p roved th at w arfarin w as n ot sup erior to asp irin for
sym ptom atic intracranial atherosclerotic disease.3,32 In this study,
569 pat ien ts w ere en rolled an d severe sten osis w as defin ed as
greater th an 50%. Pat ien t s w ere ran dom ized to h igh -dose asp irin
th erapy (650 m g t w ice a day) or w arfarin th erapy (goal in tern a-
t ion al n orm alized rat io [INR] 2–3). No sign ifican t differen ce in
th e rate of cerebrovascu lar even t s w as fou n d bet w een t h e h igh -
dose aspirin group and the w arfarin group. The 2-year stroke risk
w as 19.7% in th e asp irin grou p an d 17.2% in th e w arfarin grou p .
Th e st u dy w as h alted early du e to a sign ifican t differen ce in
m ajor ext racran ial h em orrh age (8.3% in th e w arfarin group ver-
su s 3.2%in th e asp irin grou p ). A stat ist ically sign ifican t in creased
Fig . 25.1 Annual death and stroke rates for intracranial atherosclerosis
based on distribution. This graph dem onstrates the annual death and risk of death , m ajor h em orrh age, an d m yocardial in farct ion (MI)
stroke rates (isotopic stroke and any stroke) for patient s with internal ca- or sudden death in pat ien ts taking w arfarin w as foun d com pared
rotid artery, vertebrobasilar, and m iddle cerebral artery (MCA) stenosis. w it h t h ose t aking h igh -d ose asp ir in . Ad d it ion al an alyses in a
Data compiled from previously published studies.17,56–65 (Courtesy of Bar- m u lt ivar iable m od el adju sted for age, sex, an d race fou n d t h at
row Neurological Institute.)
t h e r isk of st roke w it h in th e vascu lar ter r itor y of sten osis w as
h igh est in p at ien t s w it h severe sten osis (> 70%) an d th ose en -
rolled early after th eir qualifying even t (< 17 days).20
No p u blish ed dat a are available in th e m edical literat u re es-
t ablish ing eith er t h e equ ivalen ce or su p eriorit y of any ot h er
■ Radiographic Evaluation an tiplatelet agen t over aspirin for secon dar y st roke preven t ion
Digit al su bt ract ion angiograp hy rem ain s t h e gold st an dard . in pat ien ts w ith in t racran ial sten osis. A ran dom ized, open -label,
Com pu ted tom ograp hy (CT) angiography h as im p roved con sid- blinded en d-poin t t rial com paring aspirin plu s Plavix versus as-
erably, an d its sen sit ivit y con t in u es to im p rove. Magn et ic reso- pirin alon e for pat ien ts w ith sym ptom at ic in t racran ial in tern al
n an ce angiography an d t ran scran ial Doppler ult rason ography carot id ar ter y (ICA) or MCA sten osis fou n d t h at com bin at ion
bot h h ave h igh n egat ive p red ict ive valu e bu t low p osit ive p re- th erapy w as m ore effect ive th an m on oth erapy for redu cing m i-
d ict ive valu e n oted in t h e St roke Ou tcom es an d Neu roim aging croem bolic sign als on t ran scran ial Doppler st udies.33 Oth er an t i-
of In t racran ial At h erosclerosis (SONIA) t r ial, a su bset an alysis of platelet agents, clopidogrel and aspirin-dipyridam ole, were found
t h e WASID st udy.26 Th erefore, th ese lat ter m odalit ies are u seful to h ave sim ilar st roke recu r ren ce rates in t h e Preven t ion Regi-
m ain ly as screen ing tools to exclude th e p resen ce of in t racran ial m en for Effect ively Avoid in g Secon d St rokes (PRoFESS) st u dy,
ath erosclerosis. Neith er m odalit y can reliably est im ate th e ex- w h ich in cluded any pat ien ts w ith prior st roke.34 A m u lt icen ter,
ten t of sten osis, part icu larly w h en evalu at ing severe sten osis. dou ble-blin d, placebo-con t rolled t rial of cilostazol an d asp irin
Perfusion studies are useful to determ ine flow -related changes versus aspirin alon e in pat ien t s w ith sym ptom at ic M1 segm en t
due to in t racran ial ath erosclerot ic disease. Perfu sion st u dies en - or basilar sten osis foun d suggest ion of regression of sten osis in
able in direct assessm en t of a pat ien t’s abilit y to m eet dem an d in pat ien ts receiving cilostazol.35 How ever, in a su bsequ en t st u dy of
a par t icular vascular dist ribut ion . Curren t m odalit ies ut ilized in - cilost azol plus aspirin versus Plavix plus aspirin , cilost azol w as
clu de p osit ron em ission tom ograp hy (PET), single p h oton em is- n ot fou n d to h ave a su p er ior ben efit in p reven t ing p rogression
sion com p u ted tom ograp hy (SPECT), CT p er fu sion , xen on CT of sym ptom at ic IA.35,36 Su bset an alyses from th is st u dy fou n d
p er fu sion , an d m agn et ic reson an ce (MR) p er fu sion . Per fu sion that h igh -densit y lipoprotein (HDL) cholesterol elevation, coupled
st u dies h ave been sh ow n in a ret rospect ive st u dy to h elp iden t ify w ith rem n an t lipoprotein ch olesterol reduct ion an d low apoli-
pat ien ts w ith flow ch anges th at m ay ben efit from aggressive in - pop rotein B/A-I, w as associated w ith absen ce of angiograp h ic
ter ven t ion .27 Th e Japan ese EC-IC bypass Trial (JET) ut ilized SPECT progression of sym ptom at ic IA.37
to id en t ify pat ien t s w it h sign ifican t flow -related sten osis for A subsequen t m ult icen ter prospect ive st udy evaluat ing sym p -
con siderat ion for byp ass.28 Th e Carot id Occlusion Surger y St udy tom at ic in t racran ial sten osis, 25% of w h ich w as located in th e

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332 III Ischemic Stroke and Vascular Insufficiency

in tern al carot id ar ter y an d n early 50% of w h ich w as located in IA, an d th e pooled result s do n ot suggest ben efit over m edical
th e p osterior circu lat ion , fou n d a h igh rate of recu rren t even t s at th erapy.41,42 At th is t im e, surger y rem ain s an opt ion for a select
2 years despite m edical th erapy, w ith a n early 2-fold in creased subpopulat ion of p at ien ts w ith sym ptom at ic IA disease.
stroke risk w hen hem odynam ically significant stenosis was pres- Th e h igh rate of st roke in p at ien t s w it h sym ptom at ic in t ra-
en t .38 Th is an d ot h er sim ilar st u dies n ot ing th e h igh risk of recu r- cran ial sten osis prom pted evolut ion of en dovascular th erapy to
ren t st roke in pat ien ts w ith sym ptom at ic in t racran ial sten osis, redu ce th e st roke bu rden . In it ial st u dies dem on st rated tech n ical
despite m edical th erapy, h elped to drive d evelop m en t an d adop - feasibilit y of angioplast y an d in t racran ial sten t ing. Most data
t ion of add it ion al th erap eu t ic opt ion s. How ever, it is w or th n ot- w ere collected in th e form of regist ries an d ret rospect ive series.
ing th at subset an alyses of th e ran dom ized p rospect ive WASID Angioplast y w as associated w ith a relat ively h igh resten osis rate,
pat ien t pop u lat ion did n ot suggest th at p at ien t s w h o failed an t i- an d sten t ing w as added to m ain tain vessel paten cy, alth ough
th rom bot ic th erapy (i.e., an t ip latelet or an t icoagu lat ion ) w ere at som e st u dies h ave fou n d lim ited ben efit of sten t ing over angio-
h igh er risk for recu rren t st roke.39 p last y.43,44 Ot h ers advocated t h e u se d r ug-elu t in g sten t s to re-
Follow ing th e first ext racran ial to in t racran ial (EC–IC) ar terial du ce th e risk of in -sten t sten osis.45
bypass in 1967 by Mah m ut Gazi Yaşargil, EC–IC bypass gain ed In it ial Food an d Drug Adm in ist rat ion (FDA) approval of th e
popularit y as a treatm ent option for sym ptom atic carotid or MCA Wingspan sten t (Boston Scien t ific, Marlborough , MA; n ow part
sten osis. Th e In tern at ion al Cooperat ive St u dy of Ext racran ial/ of St r yker) w ith a h u m an itarian device exem pt ion in 2005 w as
In t racran ial Ar terial An astom osis began in 1977 to assess th e based on a prospect ive, single-arm st udy of 45 pat ien ts w h o un -
valu e of EC–IC byp ass for sym ptom at ic ath erosclerot ic lesion s of der w en t angiop last y w ith th e Gatew ay balloon cath eter follow ed
th e ICA an d MCA.40 Th e origin al EC–IC byp ass t rial did n ot dem - by placem en t of th e self-expan ding Wingspan sten t . Th e com -
onstrate a benefit of cerebrovascular bypass over m edical m anage- posite ip silateral st roke/d eath rate w as 4.5% at 30 days an d 7.0%
m en t in pat ien ts w ith sten o-occlusive carot id an d in t racran ial at 6 m on t h s.46 A sep arate m u lt icen ter p rosp ect ive regist r y of
disease.21 Th is st udy en rolled 1,495 pat ien ts w h o w ere ran dom - p at ien t s t reated w ith th e Gatew ay balloon an d Wingspan sten t ,
ized to m edical m an agem en t or su rgical in ter ven t ion , of w h ich also publish ed in 2007, repor ted a 6.1% rate of m ajor periproce-
118 w ere excluded by th e referring physician s w h o sen t th ose du ral n eu rologic com p licat ion s for p at ien ts w ith sym ptom at ic
patients directly for surgical intervention. An 18% stroke rate w as stenosis > 70%.47 Technical success in these studies exceeded 97%.
seen in th e m edical grou p w ith m ean follow -u p of 55.8 m on th s. How ever, as in t racran ial sten t ing for sten osis in creased, m eta-
In tot al, a 20% st roke rate w as seen in th e su rgical grou p. Th e an alyses fou n d a w ide range of periprocedural m orbidit y w ith
su bset of pat ien ts w ith severe MCA sten osis faired par t icu larly sten t ing for IA disease.48
poorly w ith su rgical in ter ven t ion . Th e absen ce of assessm en t of Th ese feasibilit y st u d ies, cou p led w it h t h e h igh st roke r isk
h em odynam ic fun ct ion , an d th e clear select ion bias w ere key for pat ien ts w ith sym ptom at ic sten osis greater th an 70% based
crit icism s of th e st udy. In abilit y to differen t iate pat ien t s at h igh on th e WASID dat a an d th e fin dings of th e EC–IC bypass t rial,
risk from th ose at low risk for recu rren t st roke w as believed by en cou raged m any to pu rsu e a m ore aggressive role for en dovas-
m any to con t ribute to th e n egat ive fin ding. St rat ificat ion by h e- cu lar th erapy in select pat ien t s. Ult im ately, a large prospect ive
m odyn am ic param eters w as perform ed in a ret rospect ive st udy ran dom ized t rial to com p are best m edical th erapy to best m edi-
w ith 88% of th e 65 pat ien ts experien cing n eu rologic im prove- cal t h erapy w it h sten t in g (Sten t in g versu s Aggressive Med ical
m en t .27 Th e JET st udy ut ilized acetazolam ide ch allenge w ith PET, Man agem en t for Preven t ing Recu rren t st roke in In t racran ial Ste-
SPECT, an d xen on - CT im aging to determ in e h em odyn am ically nosis [SAMMPRIS]) w as in itiated in Novem ber 2009. The trial w as
sign ifican t serial isch em ia. In th e JET st u dy, 206 pat ien ts w ere prem at u rely term in ated in Ap ril 2011 du e to safet y risks based
en rolled from 1998 to 2002 w ith sym ptom at ic ICA or MCA ste- on a h igh er th an expected periprocedural risk of en dovascular
n osis greater th an 70%. At 2 years, th e st roke recu rren ce rate an d th erapy. Th e 30-day com posite risk of st roke or death w ith per-
incidence of death were significantly lower for the surgical arm .28 cutan eou s t ran slum in al angioplast y an d sten t ing w ith aggres-
COSS sough t to evalu ate su p erficial tem p oral ar ter y to MCA by- sive m ed ical th erapy com p ared w ith aggressive m edical th erapy
pass p lu s m edical th erapy com p ared w ith m edical th erapy for alon e w as 14.7% an d 5.8%, respect ively (p = 0.002).49 Th e h igh er
sym ptom at ic atherosclerot ic ICA occlusion. PET im aging w as em - rate of periprocedural st roke an d death w ith sten t ing m ay be
ployed in COSS to assess h em odyn am ic fun ct ion . Medical th er- du e in par t to bias from th e regist ries an d ret rosp ective st u dies,
apy con sisted of an t ith rom bot ic t reat m en t at th e discret ion of m ore aggressive m on itoring of isch em ic even ts, an d earlier t im e
th e t reat ing physician , t arget blood p ressu re < 130/85 m m Hg, to in ter ven t ion from th e qualifying even t . Non eth eless, th e su b -
low -den sit y lipoprotein (LDL) < 100, t riglycerides < 150, an d h e- set of WASID p at ien ts w h o w ou ld h ave m et th e in clu sion criteria
m oglobin A1c < 7.0. A total of 195 pat ien ts w ere en rolled an d ran - for SAMMPRIS (age < 80 years, qualifying even ts w ithin 30 days
dom ized bet w een Ju n e 2002 an d Ju n e 2010 in th is p arallel grou p , of en rollm en t , an d sten osis greater th an 70%) h ad a h igh er pri-
ran dom ized, open -label, blin ded -adju dicat ion m ult icen ter t reat- m ar y ou tcom e even t rate (29%) th an th e overall WASID pat ien t
m en t t rial. Th e t rial w as term in ated p rem at u rely; su rger y p lu s sam ple.20,50 Th e sten t ing arm w as associated w ith a h igh er rate
m edical th erapy did n ot redu ce th e risk of recu rren t ip silateral of ipsilateral territor y st roke (10.3%vs 4.4%) an d a relat ively h igh
isch em ic st roke at 2 years (21.0%) com pared w ith m edical th er- rate of sym ptom at ic periprocedu ral h em orrh age (4.5%).
apy alon e (22.7%). Alth ough th e en dovascu lar m orbidit y w as h igh er th an an t ici-
Of n ote, the m ajorit y of ip silateral isch em ic even t s in th e sur- pated, th e rem arkably low rate of isch em ic even ts in th e m edi-
gical groups occurred w ithin the first 30 days (14.4%) as com pared cally t reated arm w as part icu larly su rprising. In th e SAMMPRIS
w ith th e m edical group (2.0%).29 Several sm all ret rosp ect ive se- st udy, aggressive risk factor m an agem en t in clu ded target blood
ries regarding u se of in direct revascu larizat ion for sym ptom at ic pressu re < 140/80 m m Hg (systolic < 130 if diabet ic) an d LDL

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25 Medical Management of Intracranial Athero-Occlusive Disease 333

< 70. Pat ien ts w ere provided w ith rosuvastat in (Crestor), m u lt i- for t iclopidin e. An oral load of clopidogrel (300–600 m g) can be
ple ant ihypertensive m edications, aspirin , and clopidogrel (Plavix) adm in istered, w h ich reduces platelet in h ibit ion t im e to 2 to 3
free of cost , w h ich likely aided com plian ce. Also, a life coach w as h ou rs. Most of th e data available for clopidogrel are fou n d in th e
provided th rough INTERx VENT Can ada (Boston , On t ario, Can ada) cardiac literat u re w ith regard to angioplast y an d sten t ing. Clopi-
to en courage com plian ce an d suppor t lifest yle m odificat ion s of dogrel h as a bet ter safet y profile th an t iclop idin e w ith a m in im al
diet ar y im p rovem en t , sm oking cessat ion , st ress m an agem en t , risk of n eu t ropen ia. Polym orp h ism s w ith in th e h epat ic en zym es
an d exercise. Th ese in ter ven t ion s h elped to ach ieve 50% few er involved in th e m et abolism of clopidogrel (cytoch rom e P-450
outcom e even ts th an expected based on WASID dat a. [CYP]1A2, CYP3A4, CYP2C19) or w ith th e p latelet P2Y12 receptor
Data from th e m edical arm of th e SAMMPRIS t rials, p ar t icu - m ay affect t h e abilit y of clop id ogrel to in h ibit p latelet aggrega-
larly w h en com p ared w ith th e m edical arm of WASID, suggests t ion . At t h is t im e, rou t in e screen in g for resp on se to clop id ogrel
th at aggressive in ter ven t ion for m odifiable risk factors m ay sig- is n ot recom m en ded for pat ien t s receiving clopidogrel for sec-
n ifican tly low er st roke risk for pat ien t s w ith sym ptom at ic IA. on dar y st roke p reven t ion .17 In com p ar ison to asp ir in , clop id o-
It is im por t an t to n ote th at th e SAMMPRIS regim en is unproven . grel h as a sligh t ly h igh er frequ en cy of rash an d d iar rh ea, bu t
Th e dat a obt ain ed can be u t ilized as a coh or t st u dy w ith regard sligh t ly low er frequ en cy of gast ric irrit abilit y or gast roin test in al
to scien t ific im pact . Non eth eless, th e m arked differen ce in st roke bleeding.
rate bet w een th e m edical arm s of WASID an d SAMMPRIS sug-
gests th at m odificat ion of risk factors m ay play an im m en se role
is st roke risk redu ct ion . Th e relat ive im pact of each in ter ven t ion , Others
h ow ever, is curren tly un kn ow n , an d fur th er st udies w ould be re-
Dipyridam ole in h ibit s platelet act ivit y by in h ibit ing act ivit y of
qu ired to determ in e th e relat ive im pact of each m odificat ion .
aden osin e deam in ase an d ph osph odiesterase, th ereby in creas-
ing levels of cyclic aden osin e m on oph osph ate an d cyclic guan o-
sin e m on op h osp h ate. Dipyr idam ole h as a sh or t h alf-life an d
th erefore requ ires adm in ist rat ion ever y 8 h ou rs. An exten ded-
■ Antiplatelet Options release form en ables t w ice-a-day dosing. It is usu ally form ulated
Several an t ip latelet m ed icat ion s are available. Th e m ost com - w ith aspirin (200 m g dipyridam ole an d 25 m g aspirin ). Th e m ost
m on are discussed in th e follow ing subsect ion s. com m on side effect is h eadach e, w h ich is rep or ted in u p to 38%
of pat ien ts, possibly th rough vasodilat ion . It is sh ow n to be effec-
t ive w h en com bin ed w ith 25 m g of asp irin in secon dar y st roke
Salicylic Acid preven t ion in th e Eu ropean St roke Preven t ion St u dy-2 (ESPS-2)
Asp ir in , also kn ow n as acet ylsalicylic acid , is t h e sin gle m ost t rial.51
com m on ly u sed m edicat ion in th e w orld. An irreversible cyclo- Cilostazol is a ph osph odiesterase-3 in h ibitor th at is m ain ly
oxygen ase in h ibitor, asp ir in exh ibit s a greater effect on t h e u sed to t reat in term it ten t claudicat ion associated w ith periph -
COX-1 varian t of th e en zym e. In h ibit ion of th e cyclooxygen ase eral vascu lar d isease. Th e m ajor it y of st u d ies of cilost azol in
en zym e p reven t s p rodu ct ion of p rost aglan din an d th rom boxan e st roke t reat m en t w ere p er for m ed in Asia an d suggest efficacy
A2 . Aspirin h as a rapid effect , w ith an t i-aggregate act ivit y n oted in secon dar y st roke preven t ion sim ilar to aspirin .35 Triflu sal is an
w ith in 1 h our of adm in ist rat ion . Dosing rem ain s debated, but an t iplatelet agen t st ruct urally related to aspirin th at is available
low er doses are gen erally advocated, as th ey are associated w ith on ly in Eu rop e an d Lat in Am er ica. Use in t h e Un ited St ates is
less risk of bleeding. lim ited to invest igat ion al p urposes on ly at th is tim e.

Thienopyridine Derivatives:
Ticlopidine and Clopidogrel ■ Medical Management:
Ticlopidine has been approved for secondary prevention of stroke Current Recommendations
but is rarely prescribed due it s side-effect profile. A t ypical dos-
Cu r ren t recom m en dat ion s for m ed ical m an agem en t of sym p -
ing regim en is 500 m g t w ice a day. It decreases platelet aggrega-
tom at ic in t racran ial sten osis in clu d e aggressive cor rect ion of
t ion by in h ibit ing th e bin ding of aden osin e 5’-dip h osph ate (ADP)
m odifiable risk factors an d t reat m en t w ith a single an t iplatelet
receptor antagonists that inhibit ADP-induced fibrinogen binding
agen t .
to platelets. In addit ion to a h igh risk of diarrh ea (20%), t iclopi-
Modifiable risk factors for p at ien t s w ith sym ptom at ic in t ra-
d in e is associated w it h sign ifican t r isk of severe n eu t rop en ia
cran ial ath erosclerosis:
(~ 1%), w h ich often occurs in th e first 2 to 3 m on th s of t reat m en t .
Ticlop idin e also en t ails som e risk of th rom bot ic th rom bocytop e- • Diet
n ic purpura. For th ese reason s, pat ien ts are recom m en ded to ob - • Exercise
tain com plete blood coun t s ever y 2 w eeks for th e first 3 m on th s • Sm oking cessat ion
on t iclop idin e. • Con t rol of diabetes m ellit us (target h em oglobin A1c < 7.0)
Clopidogrel is st ruct u rally sim ilar to t iclopidin e w ith an ad- • Aggressive blood p ressu re con t rol (t arget BP < 130/80 m m Hg)
dit ion al carboxym ethyl side grou p . Sign ifican t p latelet in h ibition • Low -d en sit y lipop rotein redu ct ion (goal < 100), gen erally w ith
is seen w it h in 2 to 3 days, w it h m a xim al in h ibit ion occu r r ing st at in s
bet w een 4 to 7 days. A sim ilar platelet in h ibit ion profile is seen • Elevat ion of low HDL

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334 III Ischemic Stroke and Vascular Insufficiency

Recom m en dat ion s for m edical t reat m en t of sym ptom at ic in - com p licat ion s m ay ou t w eigh t h e ben efit s of long-term du al-an -
t racran ial ath erosclerosis: t iplatelet th erapy for recu rren t st roke.52,53 Rou t in e test ing of
platelet react ivit y is n ot recom m en ded bu t m ay be con sidered in
• An t icoagu lat ion is n ot recom m en ded pat ien ts w ith recurren t even ts on an t ip latelet th erapy.
• Sin gle an t ip latelet t h erapy, asp ir in , clop id ogrel, or asp ir in - St rict con t rol of blood pressu re is recom m en ded, as elevated
dipyridam ole blood pressure w as significantly associated w ith ischem ic stroke.54
• Sligh t ben efit of Plavix an d asp ir in -d ipyr idam ole based on
LDL redu ct ion , gen erally w ith 3-hydroxy-3-m ethylglu t ar yl co-
st u dies, but sign ifican t cost disadvan t age
en zym e A (HMG- CoA) in h ibitors (oth er w ise kn ow n as “st at in s”)
• Du al an t iplatelet th erapy for 3 m on th s follow ing an isch em ic is recom m en ded. Th e t arget LDL is 100, alth ough m ore aggres-
even t , follow ed by single an t iplatelet th erapy sive low ering m ay be ben eficial as suggested by th e SAMMPRIS
Recom m en dat ion s for m ed ical t reat m en t of asym ptom at ic dat a. Aggressive con t rol of d iabetes m ellit u s w ith a t arget h em o-
in t racranial ath erosclerosis: globin A1c of less t h an 7 is also recom m en d ed . Treat m en t of
m et abolic syn drom e, diet m odificat ion , exercise, an d sm oking
• Modificat ion of risk factors cessat ion are recom m en ded.55 Medical elevat ion of low HDL m ay
• An t iplatelet th erapy m ay be con sidered bu t can n ot be recom - be con sidered as subset an alyses from th e Trial of Cilost azol in
m en ded based on lim ited n at u ral h istor y dat a an d absen ce of Sym ptom at ic In t racran ial Ar terial Sten osis-II (TOSS-2) st udy
st u dies suggests th at HDL m ay be p rotect ive again st IA progression , al-
th ough im pact on th e st roke rate is u n clear.37
No st udy h as dem on st rated th e su periorit y of a single agen t
No con sen su s exist s for m an agem en t of asym ptom at ic in t ra-
over aspirin in secon dar y st roke preven t ion for sym ptom at ic in -
cran ial ath ero-occlusive disease. Aggressive adjust m en t of m odi-
t racran ial ath erosclerosis. Non eth eless, m any p hysician s u t ilize
fiable risk factors is appropriate, but th e role of an t ith rom bot ic
clop idogrel in lieu of or in conju n ct ion w ith asp irin . Based on th e
m edicat ion is un clear based on lim ited n at u ral h istor y dat a.
available dat a, con sid erat ion for clop id ogrel 75 m g on ce daily
as m on oth erapy or asp irin -dipyridam ole 25 m g/200 m g t w ice a
day m ay be con sidered in lieu of asp irin alon e as in it ial t reat-
m en t . These m edicat ion s appear to exten d a m odest advan t age
over aspirin in secon dar y st roke preven t ion , but th is is offset by
■ Conclusion
a significant cost disadvantage. At the tim e this chapter w as w rit- In t racran ial ath ero-occlu sive disease is a m ult ifactorial process
ten , clopidogrel w as sligh tly ch eaper th an aspirin -dipyridam ole, w it h a sign ifican t m orbid it y an d m or t alit y p rofile. Alt h ough
an d both w ere over 14 t im es as expen sive as aspirin . su rgical an d en dovascular th erapies h ave sough t to revascularize
Many vascu lar n eu rologist s in th e Un ited St ates add a secon d territories at risk for isch em ia, th e curren t dat a suggest th at ag-
an t iplatelet agen t if a p at ien t experien ces an even t w h ile on sin - gressive m edical m an agem en t cou pled w ith lifest yle m odifica-
gle an t iplatelet th erapy. Ut ilit y of du al-an t ip latelet th erapy for t ion s provide th e m ost robu st m ean s of m in im izing m orbidit y in
several m on th s follow ing an acu te even t in pat ien ts w ith sym p - th ese p at ien t s. As m ore effect ive en dovascu lar tools are devel-
tom at ic large-vessel in t racran ial disease is likely ben eficial based oped, en dovascular th erapy m ay becom e an adju n ct or altern a-
on SAMMPRIS data, but several st udies suggest th at h em orrh agic t ive to m edical th erapy.

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Lung, and Blood In st it ute Scien t ific St atem en t . Circulat ion 2005;112: 46. Bose A, Har t m an n M, Hen kes H, et al. A n ovel, self-expan ding, n it in ol
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55. Hussain MS, Fraser JF, Abru zzo T, et al; Societ y for NeuroIn ter ven t ion al sten osis. St roke 1984;15:237–241
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h istor y of isolated carot id siph on sten osis. J Vasc Surg 1984;1:744–749 dle an d dist al segm en t s. Neu rology 1987;37:1742–1746

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26 Medical Management and Thrombolytic
Therapy for Acute Ischemic Stroke
W. David Freem an and Thom as G. Brot t

St roke h as declin ed from th e secon d lead ing cau se of death in St roke Scale (NIHSS) or Los Angeles Preh osp it al St roke Screen
th e Un ited St ates prior to 1939, bu t du e to im p rovem en t s in sys- (LAPSS) are often used. Th ese screen ing exam in at ion s are n ot
tem s of st roke care, th rom bolyt ic th erapy, an d m edical m an age- com plete neurologic exam inations, but they do save precious tim e
m en t it h as declin ed to th e th ird leading cause of death reported in acu te st roke m an agem en t . Th e NIHSS an d LAPSS are h elp ful in
in 2011.1 New or recu rren t st rokes n ow affect 780,000 p at ien t s gauging th e severit y of th e st roke deficits, w h ich m ay correlate
per year in th e Un ited St ates,2 an d th e prevalen ce is 5.8 m illion w ith isch em ic/in farct brain volu m e.
pat ien ts p er year. St roke also cau ses sign ifican t m orbidit y 1–5 Isch em ic st roke can n ot be differen t iated from acute in t racra-
am ong those patients w ho sur vive. Intravenous (IV) recom binant n ial h em orrh age on clin ical fin dings alon e; acu te n euroim aging
t issu e-t ype plasm in ogen act ivator (r t-PA) rem ain s th e on ly Food su ch as com p u ted tom ography (CT) or m agn et ic reson an ce im -
an d Dr ug Adm in ist rat ion (FDA)-approved drug to t reat acute aging (MRI) is also n eed ed . Th is asser t ion is su p p or ted by t h e
isch em ic st roke (AIS) pat ien t s, if t reat m en t begin s w ith in 3 h ou rs fact t h at t h e Nat ion al In st it u te of Neu rological Disord ers an d
of st roke on set .3,6,7 St roke (NINDS) t reat m en t t rial for IV r t-PA requ ires a baselin e
Th is ch apter first review s th e decision m aking for u sing acu te n on con t rast CT of th e h ead before in st it ut ing t reat m en t w ith
th rom bolyt ics an d m edical m an agem en t of AIS pat ien t s. It is th rom bolysis.6 To evalu ate pat ien ts rapidly, it is crit ical th at th e
w rit ten as a pract ical guide for m edical providers w h o care for ED or h osp it al est ablish a st roke p rotocol to h elp st ream lin e ef-
an AIS pat ien t during th e first h ours to first w eek. Th e first pri- ficien t care of st roke p at ien t s.
orit ies in m edical m an agem en t of th e acute st roke pat ien t are to Fig. 26.1 dem on st rates an over view of th e flow of th e acu te
determ in e IV r t-PA eligibilit y an d to ach ieve stabilizat ion . Th u s, st roke p at ien t s from ou t side th e h osp it al w ith th e em ergen cy
th e ch apter focu ses on m edical m an agem en t of severe isch em ic m edical ser vice (EMS) to th e ED an d, after CT im aging classifica-
st roke an d th ose w h o receive IV r t-PA an d are adm it ted to t h e t ion , as eith er acute isch em ic st roke or in t racran ial h em orrh age.
in ten sive care un it (ICU). Secon d, th e ch apter discu sses m edical Table 26.1 outlin es sam ple “st roke protocol” orders for th e ED
m anagem ent in term s of physiological m anagem ent. Third, it dis- an d h ospitals th at sh ould be in st it uted as soon as th e st roke pa-
cusses topographic m anagem ent of stroke com plications; that is, t ien t arrives. Secon dar y orders, su ch as ech ocardiography or ca-
“in t racran ial” (n eck-up ) com plicat ion s an d “ext racran ial” (n eck- rot id u lt rasoun d, can be perform ed after th e in it ial evaluat ion .
dow n ) com plicat ion s are discu ssed for con cept u al pu rposes. Obt ain ing a h istor y from th e pat ien t , th e fam ily/caregiver (if
th e pat ien t is ap h asic or u n con sciou s), or t h e EMS p roviders is
crit ical to h elp w ith acu te m an agem en t decision s. Th e EMS pro-
vid ers m igh t also be able to d escr ibe t h e scen e in w h ich t h e
■ Initial Medical Management of the p at ien t w as collected or foun d, or provide n am es an d con tact
n um bers of eyew it n esses at th e scen e, if th e pat ien t w as foun d
Patient w ith Acute Ischemic Stroke on th e groun d an d is u n able to provid e h istor y. Param edics often
Th e in it ial ap proach to th e pat ien t w ith AIS is based on th e rap id obtain initial vital signs, LAPSS, and “finger check” serum glucose
clin ical diagn osis of isch em ic st roke, w h ich is often in t h e acu te to screen for hypoglycem ia. Som e cen ters are able to obt ain th e
h ospitalizat ion or em ergen cy depar t m en t (ED) set t ing. Pat ien ts pat ien t’s w eigh t on a floor w eigh t scale as th e st retch er is rolled
w ith AIS t ypically presen t w ith abr upt posit ive (h eadach e, visual in to th e ED. Once th e p at ien t is m oved off th e EMS st retch er, th e
h allucin at ion or display) or n egat ive (w eakn ess of face, arm , or w eigh t of th e pat ien t is deducted from th e subsequ en t EMS
leg; ataxia; diplopia) n eu rologic sym ptom s or sign s. AIS p at ien ts st retch er w eigh t . Get t ing th e pat ien t’s exact w eigh t qu ickly can
presen t ing in th e ED sh ou ld be rapidly evalu ated, ideally by a be usefu l if IV rt-PA dosing is ult im ately used because it is w eigh t
ded icated st roke team , to m ake th e evalu at ion of th ese p at ien ts based. Oth er opt ion s in clude ED or h ospit al beds th at can w eigh
as efficien t as possible. A st roke team t ypically com prises a first- th e p at ien t .
respon der p hysician , su ch as an ED p hysician , an d, if available, a Key aspect s of th e pat ien t h istor y to obtain from EMS, or from
n eu rologist , residen t , or st roke specialist . On e of th e m ost im por- th e p at ien t (if available or able to sp eak), in clu d e th e t im e of
tan t pieces of th e AIS p at ien t evalu at ion is th e in it ial h istor y an d on set (TOO) of th e st roke or if th e TOO is n ot clear th en th e last-
exam in at ion , w h ich can often be exp ed ited by eith er a n u rse or seen neurologic-n orm al (LSN) t im e for the patien t. These are crit i-
a param edic w h o obtain s as m u ch in form at ion as possible for cal p ieces of in form at ion th at can im pact m an agem en t . If t h is
th e team . A n eu rologic screen ing exam in at ion sh ou ld be don e as in form at ion is n ot obt ain able from th e pat ien t or EMS, th e n ext
soon as possible w h en evaluating acute stroke patients to provide step is to obt ain in form at ion from an eyew it n ess at th e scen e.
som e m easu rem en t of th e n eu rologic deficits. For exam p le, th e Som et im es th e p at ien t’s cell p h on e or oth er belongings (e.g., a
rapid-screen exam in at ion s of th e Nat ion al In st it utes of Health store receipt) h ave som e referen ce to a t im e th e pat ien t w as last

337

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338 III Ischemic Stroke and Vascular Insufficiency

eral capillar y oxygen sat u rat ion [Sp O2 ]) sh ou ld be m ain t ain ed at


> 92% to 95% in st roke p at ien t s because hypoxia can cau se sec-
on dar y injur y to already vuln erable brain t issu e.

Blood Pressure Management


Acu te st roke p at ien t s often d isp lay an acu te hyp er ten sive re-
sp on se,8 sim ilar to th e Cu sh ing reflex. Th is hyper ten sive re-
spon se is likely self-protect ive in AIS because in creasing blood
pressu re w ill in crease cerebral blood flow to inju red brain t issu e.
Th e basic p rem ise in m an aging th e AIS p at ien t is to allow “p er-
m issive hyperten sion .” How ever, recen t guidelin es suggest th at
th ere m ay be u pp er lim it s beyon d w h ich u n con t rolled hyp er ten -
sion can in crease th e risk of h em orrh agic t ran sform at ion in both
th rom bolyt ic an d n on th rom bolyt ic p at ien ts 3 (see text box).

Fig . 26.1 Acute stroke evaluation algorithm from outside the hospital to
within the em ergency departm ent based on initial com puted tom ography NINDS Thrombolysis Eligibility* (< 3 Hours) and
(CT) scan and testing. BP, blood pressure; EMS, emergency medical services; European Cooperative Acute Stroke Study III
ICH, intracranial hem orrhage; ICU, intensive care unit; IV t-PA, intravenous
(ECASS III) (3 to 4.5 Hours)
recombinant tissue plasminogen activator.
Inclusion
• Noncontrast CT study showing no intracranial hemorrhage
n orm al or to baselin e. Th e LSN an d TOO t im es are crit ical factors (ICH)
in d eter m in in g eligibilit y for IV r t -PA. Un for t u n ately, m any p a- • Measurable, clinically significant deficit (by NIHSS)
t ien t s p resen t ou t sid e th e IV r t -PA 3-h ou r w in d ow , bu t t h ey Exclusion (acronym AAA-PILGRIMS-GPS)
m ay st ill h ave large areas of brain t issu e at risk for su bsequ en t • Aneurysm or arteriovenous malformation (AVM)
isch em ia an d in farct ion . Th is is esp ecially p er t in en t if t h e ED • Anticoagulation (international normalized ratio [INR] > 1.7)
n on con t rast CT scan does n ot sh ow an in farct ion larger t h an • Any history suspicious for subarachnoid hemorrhage (SAH)
on e-th ird of th e m iddle cerebral ar ter y (MCA) or oth er vascular • Puncture at noncompressible site (or lumbar puncture)
territor y or early isch em ic ch anges. within 1 week
• ICH history
• Low platelets < 100,000 per µL
• Glucose < 50 or > 400 mg/dL
■ Stabilizing the Acute Stroke Patient • Rapid resolution or minor neurologic deficits
• Intracranial neoplasm
Acute stroke patients should be initially assessed in term s of their • Major surgery or serious bodily trauma < 2 weeks
overall m edical and neurologic stabilit y. Intubation should be per- • Stroke or serious head traum a within 3 months
form ed for obt un ded pat ien t s or com atose pat ien t s w ith a Glas- • Gastrointestinal/genitourinary tract hemorrhage within 21
gow Com a Scale score of 8 or less, th ose w ith out self-protect ive days
air w ay reflexes of cough or gag, or th ose w ith obvious bedside
assessm en t of hyp oxia or in su fficien cy. Pu lse oxim et r y (periph - (Box cont inued on next page)

Table 26.1 Initial Ischemic Stroke Protocol Orders for AIS Patients

Symptoms, Past Medical (Surgical) History, Medications, Time of Onset and


History Last-Seen Normal Time (Via Patient, Family, or Collateral Witness)

Exam Rapid NIH Stroke Scale (NIHSS) exam or Los Angeles Prehospital Stroke Screen (LAPSS)
Radiology Stat noncontrast head computed tomography (e.g., differentiate ischem ic stroke vs hemorrhage)
Electrocardiogram 12 lead—evaluate for ischem ia, arrhythmia
Laboratory (obtained stat) Complete blood count with differential and platelets
Prothrombin time (PT) and international normalized ratio (INR), especially if taking warfarin
Activated partial thromboplastin time (aPTT)
Serum glucose (detect hypoglycemia mimic, hyperglycemia > 250 mg/dL)
Electrolytes
Serum creatinine (e.g., calculate glom erular filtration rate [GFR]) and blood urea nitrogen (BUN)
Pregnancy test in females of child-bearing age
Drugs of abuse screen
Troponin (or isoenzyme of creatine kinase with muscle and brain subunits [CK-MB] if renal impairment)
Source: Data from Rosam ond et al.2

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 339

Th e ECASS III t rial invest igated giving IV r t-PA du ring an ex-


• blood Pressure > 180/110 mm Hg tended w in dow up to 3 to 4.5 h ours post–st roke on set .9 Th e
• Seizure at stroke onset ECASS II t rial h ad a prim ar y outcom e being defin ed as good
ECASS III Additional Exclusion Criteria 9 (m odified Ran kin Scale [m RS] score of 0 to 1), w h ich occurred in
• Age > 80 years 52% of r t-PA–t reated pat ien t s versus 45% of placebo-t reated pa-
• Baseline NIHSS score > 25 t ien ts (odds rat io [OR], 1.34; 95% con fiden ce in ter val [CI], 1.02–
• Oral anticoagulants regardless of INR 1.76; p = 0.04). Secon dar y ou tcom es in clu ded a global favorable
• Combination of a previous stroke and diabetes mellitus outcom e (m RS of 0 to 1, Bar th el In dex score > 95, an NIHSS score
*Dat a t aken from th e Nat ion al Inst it ute of Neurological Disorders an d of 0 to 1, an d a Glasgow Outcom e Scale score of 1). Sym ptom at ic
St roke r t-PA St roke St u dy Grou p .6 in t racerebral h em orrh age occurred in 2.4% of rt -PA pat ien t s ver-
su s 0.2% for p lacebo p at ien ts (OR, 9.85; 95% CI, 1.26–77.32; p =
0.008). Mor t alit y did n ot differ sign ifican tly, alth ough it w as
For p at ien t s w h o receive in t raven ou s th rom bolysis, systolic sligh tly h igh er am ong th e su bject s t reated w ith p lacebo com -
blood pressure (SBP) sh ould be allow ed to rise up to 180 m m Hg, pared w ith r t-PA (8.4% vs 7.7%, respect ively; p = 0.68). Based on
but be t reated w ith sh or t-act ing blood pressure m edicat ion s if th ese dat a, th e FDA h as n ot ap p roved r t-PA beyon d th e 3-h ou r
th e SBP is h igh er th an 185 m m Hg. Sim ilarly, th e u pper th resh old w in dow, but som e cen ters are t reat ing pat ien ts w ith th e ECASS
for n on lyt ic pat ien ts is h igh er, w ith an upper SBP param eter u p III t rial protocol.
to 220 m m Hg before begin n ing t reat m en t w ith sh or t-act ing Pat ien t s w h o receive IV th rom bolysis or in ter ven t ion al t reat-
agen t s su ch as labet alol or hydralazin e IV as in term it ten t pu sh es. m en t of st roke are t ypically adm it ted to th e ICU for at least 24
If th e in term it ten t pu sh es fail to con sisten tly low er th e blood h ours for obser vat ion an d frequen t blood pressu re an d n euro-
pressu re to w ith in th e desired p aram eter, an in t raven ou s drip , logic m on itoring. Pat ien ts w h o do n ot receive IV r t-PA or in ter-
su ch as n icardip in e (star t ing dose 5 m g/h ), can be used. On e can ven t ion al m an agem en t of st roke are t ypically n ot adm it ted to th e
select th e an t ihyper ten sive of ch oice based on th e kn ow n drug ICU un less they have severe neurologic deficits (NIHSS score > 24),
m ech an ism an d th e pat ien t’s vital sign s (e.g., esm olol if th e pa- com a, resp irator y com prom ise, or hyper ten sive em ergen cy re-
t ien t is tachycardic an d hyp er ten sive rath er th an n icardipin e). qu iring in t raven ou s in fu sion of m edicat ion to con t rol th e blood
pressu re. Pat ien ts w ith relat ively m in or deficits, th ose w h o are
n ot given IV r t-PA or in ter ven t ion al th erapy, an d th ose w h o are
w ith out respirator y com prom ise or h em odyn am ic fluct uation s
■ Acute Thrombolysis and are adm it ted to a regular (n on -ICU) h ospit al bed.
Interventional Decision Making
On e of th e m ost im por t an t decision s in evalu at ing an acute
st roke p at ien t is w h eth er or n ot th e p at ien t is eligible an d able ■ Medical Management of Stroke :
to receive in t raven ou s th rom bolysis w ith in th e 3-h ou r (p ossibly
4.5-h our) w in dow sin ce th e on set of st roke. If th e pat ien t is eli-
The Seven P’s of Pathophysiology
gible for IV rt-PA, th is t reat m en t sh ould be discussed w ith th e A basic un derstan ding of st roke path ophysiology is n ecessar y for
pat ien t (if p ossible) or h is/h er p roxy m edical decision m aker. opt im al pat ien t m an agem en t . Isch em ia in dicates a lack of suffi-
Th is discu ssion sh ou ld in clu de th e risks of bleeding associated cien t cerebral blood flow (CBF) to m ain t ain n orm al brain t issu e
w ith th rom bolysis. Th e in t racran ial risk w as foun d to be 6.6% in function , leading to either transien t ischem ia or perm anent dam -
th e NINDS t rial,6 w h ich evalu ated IV r t-PA at a dose of 0.9 m g/kg age called in farct ion . Isch em ia to th e brain m an ifests as n eu ro-
IV, w ith a m axim u m of 90 m g. Th e dr ug is dosed w ith 10% given logic deficits an d sym ptom s referable to th e vascu lar territor y of
as th e in it ial IV bolu s an d th e rem ain der given over th e rem ain - affected brain t issue. Isch em ia, if t ran sien t , can be reversible, but
ing h ou r to p at ient s presen t ing w ith AIS w ith in 3 h ours of sym p - after a period of t im e th e n euron al t issue becom es irreversibly
tom on set . Th e st udy w as a ran dom ized placebo-con t rolled t rial. dam aged or u n dergoes in farct ion .
Th e resu lt s of th e st u dy dem on st rate th at IV r t-PA, w h en given Th e brain is a st rictly aerobic organ an d relies on oxygen de-
w ith in 3 h ours of st roke on set in eligible pat ien t s, im proved th e liver y. Brain t issu e th at is deprived of oxygen an d glucose from
clin ical ou tcom es at 3 m on th s. Th e NINDS in clu sion an d exclu - reduced CBF quickly depletes intracellular adenosine triphosphate
sion criteria are listed in th e text box above; th e first au th or of (ATP). With ou t ATP, glucose is conver ted to lactate, w h ich pro-
t h is ch apter suggest s t h e acronym for m ed by t h e exclu sion cr i- du ces 2 ATP com pared w ith u p to 36 ATP from aerobic m etabo-
teria as sh ow n in th e box: AAA-PILGRIMS- GPS. Clin ician s are lism . Th e d im in ish ed ATP is in su fficien t for n eu ron al/ast rocyt ic
recom m en ded to keep th ese in clu sion /exclu sion s as a “p ocket” in t racellular fu n ct ion , an d th is result s in in t racellular acidosis
referen ce or posted som ew h ere in th e ED. Th e eligibilit y for rt-PA an d a cascade of even t s leading to cell death . Isch em ic in farct ion
at 3 h ou rs is discu ssed below, as w ell as eligibilit y for th e Eu ro- is th e fin al com m on path w ay regardless of th e m ech an ism of ar-
pean Coop erat ive Acu te St roke St u dy (ECASS) III t rial,9 w h ich h as terial occlu sion or reduced CBF (e.g., em bolism or ath eroth rom -
expanded th e treatm ent w indow in som e patients up to 4.5 hours bosis). Th erefore, th e durat ion of t im e th at th e brain is exposed
sin ce the t im e of on set. Further, several throm bolytic studies have to reduced CBF (t ypically less th an 10 to 20 m L/100 g/m in ) is
been com pleted, an d a recen t m eta-an alysis dem on st rates th at propor t ion ate to th e degree of t issu e in farct ion .11,12 Th is rela-
the sooner th e m edication is adm inistered to eligible patien ts, th e t ion sh ip h as been quan t ified as “t im e is brain .”
m ore likely th e pat ien t w ill h ave a bet ter outcom e; h em orrh age Un for t un ately, th e m ajorit y of pat ien ts w h o present w ith AIS
risk in creases th e fu r th er ou t r t -PA is given from t im e of on set .10 do so outside th e 3-h our IV rt-PA reperfusion w in dow.3 Th erefore,

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340 III Ischemic Stroke and Vascular Insufficiency

su bsequ en t m edical an d p hysiological m an agem en t of isch em ic Table 26.2 The 7 Physiological (P’s) Strategies for Acute Ischemic
st roke is fu n dam en t al to ach ievin g opt im al p at ien t ou tcom es. Stroke Management
In th is ch apter, w e divide m edical m an agem en t of th e AIS pa-
1. Pipes Stroke mechanism of the arterial occlusion
t ien t in to physiological an d topograph ical issu es for con cept u al 2. Pressure Mean arterial pressure and cerebral perfusion
m an agem en t purposes. Seven physiological m an agem en t st rate- pressure (CPP)
gies (“7 P’s”) of t h e AIS p at ien t are d iscu ssed below (Table 3. Perfusion Cerebral blood flow (CBF)
26.2). These st rategies are m odified an d expan ded from th e pre- 4. Pump Cardiac output (CO = SV × HR)
viou s excellen t con cept u al w ork of Row ley 13 an d Felberg an d 5. Penumbra Potential salvageable area of brain tissue that is at
Naidech .14 risk for becoming infarcted within a finite period
of time, and reduced in CBF compared with
normal
Pipes 6. Prevent Prevention of stroke complications such as aspiration
Th e m ost com m on m ech an ism of brain isch em ia in AIS is a pneumonia, deep venous throm bosis, pulm onary
“blocked -p ip e” m ech an ism cau sin g isch em ia to d ow n st ream em bolus, and secondary stroke
brain tissue. Therefore, the consideration of a “pipe-buster agen t” 7. Pyknosis Protecting against secondary brain injury through
like IV rt-PA is th e m ost fu n dam en tal p hysiological step . In t ra- awareness of penumbral brain tissue peri-infarct
depolarization, future neuroprotective strategies,
ar terial m an agem en t can be con sidered if th ere is a viable region
and preventing/treating fever and major
of brain , called a p en u m bra, t h at cou ld be rescu ed by rep er fu -
hypotension
sion . Fu r t h er, t h e d iscover y of ar ter ial vascu lar occlu sion can
sh ed ligh t on th e m ech an ism s resp on sible for isch em ia. For ex- Abbreviations: SV, stroke volume; HR, heart rate.
Sources: Modified and expanded from Rowley13 and Felberg and Naidech.14
am ple, iden t ifying occlusion as cardioem bolic, ar ter y to ar ter y
(e.g., from a carot id ath erosclerot ic plaque), or ar teriosclerot ic/
sm all vessel can in for m d ecision m aking an d in ter ven t ion . Ar- th rom bu s form at ion , occlu sion , em bolism , or h em orrh age. Neu -
ter ial d issect ion is an ot h er en t it y t h at can lead to st roke after rovascular im aging su ch as a CT angiogram of t h e h ead an d n eck
t rau m a an d , sp orad ically, w ith ou t t rau m a. Dissect ion occu rs vessels, MR angiogram , or u lt rasoun d can detect vascular (pipe)
w ith th e tearing of an in t ralum in al ar terial w all an d can lead to occlusion an d h elp drive m an agem en t .

Fig. 26.2 Acute blood pressure (BP) management in acute stroke. Caution nous; MAP, m ean arterial pressure; SBP, systolic blood pressure. (Adapted
is advised in discontinuing beta-blockers or clonidine (and other chronic from Qureshi AI. Acute hypertensive response in patient s with stroke:
oral antihypertensive m edications) in patients with underlying coronary pathophysiology and m anagem ent. Circulation 2008;118:176–187, with
disease or atrial fibrillation. However, avoiding hypotension is also impor- perm ission from Lippincot t William s and Wilkins/Wolters Kluwer Health:
tant. CPP, cerebral perfusion pressure; ICP, intracranial pressure; IV, intrave- the Am erican Heart Association. Copyright 2008.)

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 341

Pressure
Several key equ at ion s are im p or t an t to rem em ber w h en caring
for AIS pat ien t s. Th e first equat ion to con sider is blood pressure
(BP), w h ich is equal to cardiac out put (CO) t im es system ic vascu-
lar resistan ce (SVR):
BP = CO × SVR
Alt h ough CO an d SVR are t yp ically n ot m easu red w it h ou t
invasive devices, BP is an easily obtain able su rrogate of CO an d
SVR. Blood p ressu res can be obt ain ed at th e pat ien t’s bedside
w ith a n on invasive blood pressure (NIBP) cuff. Fu rth erm ore,
NIBP m on itoring in AIS p at ien t s, esp ecially after IV r t-PA, is t yp i-
cally frequ en t (ever y 15 m in u tes for th e first few h ou rs, an d th en
h ourly) 3 to h elp gu ide BP m an agem en t (Fig. 26.2).
An ot h er im p or t an t equ at ion for m ed ical p roviders is t h at
u sed to calcu late t h e m ean ar ter ial p ressu re (MAP), w h ich can
be calculated using th e pulse pressure (PP) (w h ich is th e systolic
pressu re m in u s th e d iastolic p ressu re) an d th e d iastolic blood Fig. 26.3 Graph of pulse pressure. P, pressure.
pressu re (DBP):
MAP = ⅓ PP + DBP
is h igh er in gray m at ter. Isch em ic brain t issu e becom es in farcted
MAP is th e driving pressu re th at th e organ s “feel,” w h ereas PP
(irreversibly dam aged or dead) if th is isch em ia (CBF < 20 m L/100
is th e w ater-h am m er effect of blood pressu re (Fig. 26.3). Fu r th er,
g/m in ) is n ot corrected in m inu tes. In large in t racran ial arter y
in t racranial pressu re (ICP) is th e “back” p ressu re to MAP an d is
m odels of isch em ic st roke, th e cen t ral area of in farct ion is term ed
described in th e n ext su bsect ion . Th erefore, MAP is th e driving
th e “core” region of in farct ion . Brain t issu e receiving m ore th an
pressu re an d ICP is th e resistan ce to MAP. W h en ICP app roach es
20 m L/100 g/m in bu t less th an 50 m L/100 g/m in CBF m ay be
MAP, th e cerebral p erfu sion pressu re (CPP) ap proach es 0. How -
term ed “oligem ic.” Oligem ic t issu e th at surroun ds th e core re-
ever, in norm al con dit ion s in AIS, ICP sh ould be n orm al an d CPP
gion of isch em ia is term ed th e pen um bra. How ever, th e pen um -
sh ou ld equ ate to MAP.15
bra can tolerate th is relat ively low am oun t of CBF for on ly a fin ite
period of t im e before irreversible cellu lar inju r y an d death en su e.
Perfusion After brain t issue dies, th e t issue un dergoes cytotoxic edem a or
sw elling. Secon dar y ischem ia can occur from m assive hem ispheric
An oth er im por t an t equat ion to rem em ber is th e equat ion for ce-
in farct ion an d resu lt ing ed em a, leading to m ass effect an d m e-
rebral blood flow :
ch an ical occlu sion of ar terial (an d ven ou s) vessels. A viciou s
CBF = CPP/CVR “sn ow ball” p h en om en on m ay be in it iated ; m id-lin e sh ift an d ce-
Here, CVR is cerebral vascu lar resistan ce or th e ch ange in vas- rebral h ern iat ion syn drom es m ay follow (Figs. 26.5 an d 26.6).
cular react ivit y or vessel diam eter. CBF (Fig. 26.4) is depen den t
on CPP, w h ich can be calcu lated from th e MAP an d th e ICP: Pump
CPP = MAP – ICP
Th e h ear t is t h e pu m p t h at drives system ic blood flow. W h en
Brain isch em ia is d efin ed as t issu e w it h less t h an 20 m L/ heart function is com prom ised, a decrease occurs in blood flow to
100 g/m in of CBF. Norm al CBF is t ypically 50 m L/100 g/m in an d th e body’s organ s, in clu ding t h e brain . Th e brain receives at least

Fig . 26.4 Cerebral “pressure” autoregulation relation-


ship. The x-axis indicates cerebral perfusion pressure (CPP),
which is defined by the equation CPP = MAP – ICP, where
MAP is the m ean arterial pressure, or ⅓ PP + DBP, and ICP
is the intracranial pressure. PP is the pulse pressure, or the
difference bet ween SBP (systolic blood pressure) and DBP
(diastolic blood pressure). The y-axis indicates cerebral
blood flow (CBF), which is measured in m L/100 g/m in
unit s. Ischem ia can occur below 20 CBF unit s (dashed
red line). Infarction happens rapidly as CBF approaches
zero.11,12 (Reprinted from Rose JC, Mayer SA. Optim izing
blood pressure in neurological emergencies. Neurocrit Care
2004;1:287–299, with perm ission of Springer Science+
Business Media.)

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342 III Ischemic Stroke and Vascular Insufficiency

a b c

Fig. 26.5a–c Computed tom ography im ages of 72-year-old m an with an (b,c) Twelve days later, progressive swelling caused secondary ischemia to
acute ischem ic stroke of the right posterior and m iddle cerebral artery divi- deep perforators of the m idbrain, thalamus, and basal ganglia. The expand-
sions (a). His brain continued to swell, which caused progressive herniation. ing infarction resulted in the patient’s death.

15% of the cardiac ou t pu t of th e en t ire body, w h ich is dispropor- lip id - low e r in g age n t s, an d m an age m e n t of ot h e r r isk factors
t ion ately h igh con sidering it s m ass is on ly 3 p ou n ds (1500 g). sh ou ld be e n te r t ain e d .3 Preve n t ion of st roke com p licat ion s
Cardiac ou t p ut (Q) is exp ressed by th e follow ing equ at ion : su ch as asp irat ion p n e u m on ia , d e e p ve n ou s t h rom bosis, an d
p u lm on ar y e m bolu s are also p ivot al afte r AIS to e n su re op t i-
Q = SV × HR
m al ou t com es.
Here, SV sign ifies st roke volu m e m easu red in m illiliters an d
HR sign ifies h ear t rate in beat s per m in ute. In th e st roke pat ien t ,
opt im izing Q is im port an t . Th e p u m p is also w or thy of at ten t ion
as a poten t ial cause of th e st roke. Cardiac sources of st roke can
origin ate from a ven t ricu lar w all th rom bu s (after m yocardial in -
farct ion ) or from th e left at rial appen dage in a pat ien t w ith at rial
fibrillat ion .

Penumbra
Pen u m bra refers to oligem ic brain t issu e th at is poten t ially via-
ble w ith ret urn of n orm al blood flow, but is oth er w ise at risk for
cerebral in farct ion . In con t rast to pen um bral brain t issue, a core
area is defin ed in AIS pat ien t s as th at area of brain t issue th at is
n ot salvageable because it h as sustain ed a ver y low CBF (< 10
m L/100 g/m in ) for an excessive p eriod of t im e.

Prevent
Preve n t ion of se con d ar y isch e m ic st roke is an im p or t an t t ask,
an d on e t h at is n ow a qu alit y m et r ic for in p at ie n t s w it h st roke.
Pat ie n t s w h o h ave h ad a fir st -eve r st roke are at r isk for a su b -
se qu e n t st roke. Defin in g t h e st roke m e ch an ism is fu n d am e n -
t al t o gu id in g t h e t yp e of se con d ar y st roke p reve n t ion . For
exam p le, if a p at ie n t h as at r ial fib r illat ion cau sin g AIS, an d IV
r t -PA is give n w it h in 3 h ou rs, secon d ar y p reven t ion w it h asp i-
r in or in it iat ion of an t icoagu lat ion sh ou ld b e carefu lly con sid - Fig. 26.6 Mass effect and downward displacem ent of the brainstem (her-
e re d afte r t h e fir st 2 4 h ou r s. If t h e p at ie n t ’s st roke is relate d to niation) from convexit y m ass effect are shown for a subdural hem atom a,
sym p tom at ic carot id ar t e r y d isease, in it iat ion or m od ificat ion sim ilar to the compartm ental shifts following a m alignant m iddle cerebral
artery (MCA) infarct. Herniation not only displaces brain tissue but also
of an t ip lat elet t h e rapy sh ou ld b e con sid e re d , an d t h e b e n e -
causes vascular injury to brain tissue by compressing perforating arteries
fit s an d r isks of carot id revascu lar izat ion sh ou ld be w e igh e d . and arterioles. ACA, anterior cerebral artery; PCA, posterior cerebral artery.
For t h e lon ge r te r m , r isk-factor m od ificat ion su ch as op t i- (Courtesy of the Mayo Foundation for Medical Education and Research. All
m al b lood p ressu re m an age m e n t , in it iat ion or m od ificat ion of rights reserved.)

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 343

Pyknosis becom e severely hypoten sive are com m on ly obser ved to appear
w orse neurologically. Th erefore, w ith holding som e of th e patien t’s
Pykn osis refers to preven t ing secon dar y involut ion or apoptot ic
oral an t ihyper ten sive m edicat ion s is som et im es con sidered dur-
cell death of n euron s an d ast rocytes in in farcted t issue. Alth ough
ing th e acute (24 to 48 h ours) period after AIS. W h en t reat ing
the aforem entioned strategies are geared to m inim ize and restore
hyper ten sion is th ough t to be un avoidable, u sing sh or t-act ing
CBF to brain t issue as a p rim ar y st rategy, preven t ion of secon d-
an t ihyper ten sive agen ts is advised (Fig. 26.2).
ar y brain injur y is equally im portant. Peri-infarct depolarizations
are elect r ical d isch arges t h at occu r in p en u m bral brain t issu e.
Th ese d isch arges cau se an im balan ce in cellu lar “su p p ly-an d -
d em an d ” p hysiology in t h e con text of already low ered CBF, re- ■ Advanced Neuroimaging and
su lt ing in in creased cellu lar dem an d.16–20 A glutam ate cascade of
n eu rotoxicit y results, leading to su bsequen t cell death . Un for t u-
Interventional Management of Stroke
n ately, n o effect ive n eu roprotect ive st rategies are available an d Advan ced neuroim aging such as CT angiography and perfusion or
few n europrotect ive agen t s for st roke are un der developm en t .3 MRI diffusion-perfusion can be helpful, as long as they are rapidly
Th e on ly effect ive st rategy at presen t is to restore blood flow as available at th e ED or h ospital. Such advan ced n euro im aging can
qu ickly as possible. h elp iden t ify pat ien t s w ith poten t ially salvageable brain t issu e
Carefu l m edical in ter ven t ion s m ay offer in direct p rotect ive w h o w ou ld ben efit from revascu lar izat ion . MRI is often m ore
effect s. It is w ell kn ow n th at fever cau ses secon dar y brain inju r y u seful th an CT im aging for detect ing sm all-vessel disease-related
after st roke, an d elevated tem perat ure is deleterious to already in farct ion s, p art icu larly th ose located in th e brain stem an d pos-
inju red an d m et abolically fragile brain t issu e.21–26 Th erefore, it is terior fossa. The tim e of acquisition and processing for MRI exceed
im por t an t to detect , w ork u p, an d aggressively treat fever (i.e., th at for CT at m ost in st it u t ion s. For EDs an d h osp it als w ith ou t
tem p erat u re of 38.0°C or h igh er). Fever can be t reated w ith acet- access to advan ced im aging, a dedicated st roke team w ith expe-
am in op h en if t h e p at ien t can tolerate t h e d r ug from a h ep at ic rien ce in perform ing n eu rologic assessm en t s is advised. For th e
st an d p oin t (e.g., 650 m g to 1 g en terally or IV ever y 6 h ou rs, u n stable n eu rologic pat ien t , referral to a region al st roke or n eu -
m axim u m 4 g for m ost pat ien t s). For crit ically ill pat ien t s w h o rosurgical cen ter (“h igh er level”) is advised (Fig. 26.7).
are febrile, perform ing cult ures of appropriate cen t ral lin es an d Th e in ter ven t ion al m an agem en t of st roke su ch as m ech an ical
Foley u rin ar y cath eters an d t aking a ch est X-ray to iden t ify in fil- clot retrieval or other m eans of en dovascular reperfusion is a sub-
t rates sh ou ld be con sidered . ject of in ten se discourse and research. Im proved clin ical outcom es
Avoidan ce of sign ifican t hyp oten sion (MAP < 65 m m Hg) is h ave n ot been dem on st rated to date using th is t reat m en t st rat-
an ot h er p rotect ive st rategy in AIS p at ien t s.3 AIS p at ien t s w h o egy. How ever, several st udies h ave suggested h igh er rates of re-

Fig. 26.7 Overview of acute ischemic stroke (AIS) armam entarium of Som e interventional means of stroke therapy such m echanical clot retrieval
therapies approved by the Food and Drug Adm inistration (FDA). Intrave- devices (e.g., Merci Retrieval System , Concentric Medical, Mountain View,
nous (IV) recom binant tissue-t ype plasm inogen activator (rt-PA) is only ap- CA; Penum bra™ System , Penum bra, Inc., Alam eda, CA) and intracranial
proved by the FDA for use within 3 hours of the AIS, but the Am erican Heart stenting for stroke may have FDA approval under an investigational device
Association endorses its use for up to 4.5 hours based on results from the exemption (IDE), which is akin to hum anitarian or compassionate use. IA ,
European Cooperative Acute Stroke Study (ECASS) criteria–treated patients. intra-arterial; LMWH, low-m olecular-weight heparin; *under IDE.

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344 III Ischemic Stroke and Vascular Insufficiency

perfu sion after en dovascu lar t reat m en t com p ared w ith IV r t-PA cilit y for con siderat ion of in t ra-ar terial clot ret ract ion beyon d
alon e. Such im proved rates of reperfusion h ave driven , appropri- 3 h ours of sym ptom on set . Sh e did receive a n on con t rast h ead CT
ately, th e ongoing develop m en t of bet ter devices an d im proved an d a CT angiogram an d basic laboratories, w h ich foun d th at th e
system s for rapid adm in ist rat ion . com plete blood cou n t , platelets, an d seru m creat in in e w ere n or-
In th at con text , iden t ifying th e site of vascular occlu sion an d m al. Due to t ran sport delays, th e pat ien t arrived at our h ospital
determ in ing w h eth er or n ot a salvageable vascu lar pen u m bra at 6 h ours post–st roke on set , an d h er act ivated par t ial th rom bo-
exist s are crit ical, especially if th e p at ien t does n ot m eet criteria plast in t im e w as 41.9 secon ds (n orm al range is 22.7 to 36.1 sec-
for IV r t-PA. Tim e delays sh ould be m in im ized an d an alyzed for onds). Her noncontrast head CT scan (Fig. 26.8a) revealed a dense
con t in u ou s p ract ice im p rovem en t to expedit iou sly t reat st roke dist al righ t MCA-M1 sign .
pat ien ts. For exam ple, a secon dar y n u rse can be ver y h elpfu l to An im m ediate CT angiogram w ith perfusion w as perform ed
est ablish a periph eral IV or to draw n eeded laboratories. Rap id th at sh ow ed a m ism atch bet w een cerebral blood volu m e (CBV)
availabilit y of a respirator y th erapist or an elect rocardiogram and CBF com pared w ith the tim e-to-peak and tim e-to-drain m aps
(ECG) tech n ician can h elp expedite th e perform an ce of an cillar y (Fig. 26.8b).
test s. Th e CT sh ou ld be p erform ed w ith ou t delay, w ith in pu b - Th e m ism atch on p erfu sion im aging suggested a p oten t ially
lish ed t im e an d oth er Am erican Hear t Associat ion (AHA)-recom - salvageable vascu lar p en u m bra of abou t h alf of th e righ t MCA
m en ded m et rics for st roke cen ters.2 territor y. Th e en dovascular team review ed th e im aging in th e
angiogram suite an d proceeded to perform an im m ediate m e-
ch anical clot extraction by direct syringe “suction” technique. The
Example Case 1: Salvageable Penumbra pat ien t’s digit al su bt ract ion angiogram sh ow ed a righ t MCA-M1
A 66-year-old left-h an ded w om an w ith at rial fibrillat ion w h o dist al lu m in al filling d efect con sisten t w ith in t ralu m in al th rom -
w as on dabigat ran for st roke p reven t ion u n der w en t a cardiac ab - bu s (Fig. 26.8c) prior to clot ext ract ion .
lat ion p rocedu re. Her dabigat ran w as w ith h eld several days p rior After clot ext ract ion , t h ere w as robu st filling of t h e r igh t
to th e procedure. Sh e w as given 150 m g of dabigat ran orally after MCA-M1 an d it s bran ch es (Fig. 26.8d,e). Th e p at ien t h ad a dra-
th e p rocedu re to h elp re-an t icoagu late h er for secon dar y st roke m atic neurologic im provem ent after the procedure, w ith an NIHSS
preven tion . Thirt y m inutes after th e ablation , she developed acute score of 3 (2 for left-face an d 1 for left-arm drift). Th e follow ing
dysar th ria, left h em iparesis (face, arm , an d leg), sen sor y loss, an d day, h er NIHSS score h ad im proved to 2 (subject ive n um bn ess
at axia. Sh e h ad an NIHSS score of 14. Sh e w as seen by th e local an d su btle residual facial w eakn ess).
n eu rologist an d th e cardiologist w h o did n ot feel com for t able It is also im por t an t to recogn ize cases by advan ced n euroim -
adm in istering IV r t-PA due to th e lack of kn ow ledge abou t th e aging in w h ich th ere m ay n ot be a salvageable p en u m bra. Th ese
in terp lay of dabigat ran an d r t-PA. Th ey felt th at th e risk of in t ra- pat ien ts m ay m ore often h ave st at ic th an flu ct u at ing n eu rologic
cran ial bleed in g w as too h igh an d requ ested t ran sfer to ou r fa- deficit s, bu t th e clin ical p ict ure is n on specific.

Fig. 26.8a–e (a) Noncontrast computed tom ography (CT) im age showing dense
a right middle cerebral artery (MCA)-M1 sign (black arrow).

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 345

c d e

Fig. 26.8a–e (continued ) (b) CT perfusion study shows m ism atch be- (c) Digital subtraction angiogram (DSA) shows the right MCA-M1 distal lu-
t ween cerebral blood volum e (CBV, upper right im age), and cerebral blood minal filling defect consistent with intralum inal throm bus (arrow) prior to
flow (CBF, upper m iddle im age) compared with the tim e-to-peak (TTP) and clot extraction. (d) DSA after clot extraction, with robust right MCA filling
tim e-to-drain (TTD) m aps, which are the bot tom left and m iddle images, and m ore MCA branches seen diffusely. (e) The “red clot” fragm ents ex-
respectively. The m ism atch on perfusion im aging suggests a potentially tracted from the syringe that were ejected out of the syringe onto a sterile
salvageable vascular penum bra of about half of the right MCA territory. cloth.

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346 III Ischemic Stroke and Vascular Insufficiency

Fig. 26.9 Nonsalvageable tissue infarction with m atched cerebral blood flow (CBF), cerebral blood volum e (CBV), and tim e-to-peak (TTP) m aps.

Example Case 2: Nonsalvageable Infarct p aten t bilaterally. It is believed th e pat ien t h ad an em bolic left
MCA-M2 in farct . As on e can see from th e im aging, th e CT perfu-
A 63-year-old m an w ith a h istor y of st age IV lu ng can cer pre- sion CBF, CBV, an d t im e-to-p eak m ap s are all m atch ed. Th erefore,
sen ted to th e ED 4 h ou rs after last seen n orm al. Th e pat ien t’s th is w as an in farct w ith ou t a detect able pen u m bra w ith in th e
NIHSS score w as 21 for severe ap h asia, righ t h em ip legia, an d dist ribu t ion of th e left MCA-M2 bran ch . Th e risk of h em orrh age
sen sor y loss. Th e pat ien t’s CT p erfu sion st u dy is sh ow n in Fig. in pat ien t s t reated beyon d 3 h ours w ould be h igh er th an in pa-
26.9. He m et all th e criteria for t h e NINDS st u dy 6 except for th e t ien ts t reated w ith in 3 h ou rs. Th e NINDS t rial, h ow ever, did n ot
t im e cr iter ia bein g less th an 3 h ou rs from on set . Th e CT an gio - in clude advan ced n eu roim aging to determ in e viabilit y of brain
gram p ict u res are n ot sh ow n , bu t t h e MCA-M1 ar ter ies w ere t issu e by th e CT perfu sion m eth od—on ly th e n on con t rast h ead

Table 26.3 ABCs of Stroke Management and Complications w ith Levels of Evidence

Management Issue Management Plan or Potential Complication Level of Evidence

A: Airway/aspiration Cardiac monitor at least 24 hours in all patients, O2 for hypoxic patients, intubation/ I
mechanical ventilation for compromised airway
B: Blood pressure Control specific to stroke t ype II
Hypotension cause should be evaluated and treated I
C: Cerebral perfusion pressure Control intracranial pressure if elevated II
D: Deep venous thrombosis Prevention with compression devices or treatm ent until bleeding stops I
Consider subcutaneous unfractionated heparin or low-molecular-weight heparin II
E: Early mobilization Consider early m obilization with physical therapy; caution about fall risk I
F: Fever Aggressive treatm ent to reach norm othermia I
G: Glucose If greater than 140–185 mg/dL, use insulin as needed; hypoglycemia is harm ful and should I
be rapidly corrected
Sources: Modified from Freeman et al5 and Am erican Heart Association guidelines. 3

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 347
Fig . 26.10 Com plications after ischem ic stroke. DVT,
deep venous throm bosis; UTI, urinary tract infection.
(Modified from Langhorne P, Stot t DJ, Robert son L, et al.
Medical complications after stroke: a m ulticenter study.
Stroke 2000;31:1223–1229, with permission from Wolters
Kluwer Health.)

CT an d th e eligibilit y criteria listed w ere used (see th e “NINDS in tern al carot id arter y term in us occlusion (T-lesion ) or MCA
Th rom bolysis Eligibilit y” text box, earlier in th e ch apter). proxim al trunk occlusion. Such infarction and cerebral edem a can
cau se p rogressive m id lin e sh ift , h ern iat ion , an d death . To at ten u -
ate th is process, hyp erton ic salin e an d m an n itol are th e in it ial
first-lin e opt ion s. Man n itol m ay be given th rough a periph eral IV
■ Topographic Medical Management w ith a cr yst allin e filter, w h ereas hyper ton ic salin e above 3%con -
of Complications after Acute cen t rat ion m ust be given via a cen t ral ven ous lin e. Dosing can be
t it rated to clin ical effect or an u pp er seru m osm olalit y lim it of
Ischemic Stroke 320 m Osm , or a serum sodiu m of 155 m Eq per liter before h alt-
Med ical an d n eu rologic com plicat ion s occu r in acu te st roke p a- ing addit ion al d oses.
t ien t s, w h ich m ay requ ire ICU m an agem en t (Table 26.3). Th e If hyp erosm olar t h erapy fails, oth er opt ion s in clu d e d eep se-
t im e cou rse for th ese com p licat ion s varies from w ith in th e first dat ion follow in g in t u bat ion an d in d u ct ion of p aralysis. In t ra-
w eek to m on th s later (Fig. 26.10). St roke-related com plicat ion s ven ou s barbit urates reduce cerebral m et abolic con su m pt ion of
(Table 26.4) th at occur after AIS can be categorized as eith er in - oxygen an d brain m et abolism , effect ively p u t t in g t h e n or m al
t racran ial com p licat ion s related to th e st roke itself or secon dar y brain “asleep” to lessen edem a an d m ake room for th e edem a-
ext racran ial com p licat ion s su ch as asp irat ion pn eu m on ia (Fig. tou s, dam aged brain in t racran ially. Hyp oth erm ia is un der inves-
26.11). t igat ion , an d som e su ccess h as been rep or ted for hyp ot h er m ia
as a t reat m en t for cases of refractor y cerebral ed em a. Decom -
p ressive h em icran iectom y (DHC) h as been st udied in th e t rials
Intracranial Complications DECIMAL (DEcom p ressive Cran iectom y In MALign an t MCA In -
If at tem pts at revascularizat ion fail, progressive in farct ion en - farct ion ), DESTINY (DEcom p ressive Su rger y for t h e Treat m en t
su es. Th is can resu lt in severe cerebral edem a, especially w ith of m align an t INfarct ion of t h e m id d le cerebral ar terY), an d

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Table 26.4 Complications and Management

Intracranial Complication Management

Primary brain injury


• Initial stroke
• Neurologic motor, sensory Rehabilitation (physical therapy, occupational therapy)
• Functional deficits, dysphagia, cognitive Cognitive therapy, speech and swallow therapy
• Recurrent stroke Stroke prevention, rehabilitation
Secondary brain injury
• Ischemic stroke progression
• Penumbra (“borderline tissue”) progression to frank infarction Revascularization
• Hemorrhagic conversion of ischemic infarct (e.g., after Avoid extrem e hypertension, reperfusion injury
thrombolysis)
• Cerebral edema, m ass effect, herniation, raised ICP Mannitol 0.25–1 g/kg IV bolus, craniectomy for refractory cases
• Hydrocephalus (t ypically obstructive from herniation) Ventriculostomy
• Seizures Antiepileptic drugs
• Stroke-specific complications
• Neurologic breathing pat terns (e.g., Cheyne-Stokes sign, Support airway, supplemental O2 , intubate if needed
cluster, apneustic ataxic)
• Autonom ic dysfunction—acute hypertensive response Frequent BP monitoring
• Cushing’s reflex Treat ICP if elevated
• Depression/anxiet y Antidepressants
• Compressive mononeuropathies (“pressure palsies”) and critical Identify/remove compression, aggressive rehab
illness myoneuropathy if in the ICU
• Pain—imm obilit y, contractures, spasticit y, or central pain Mobilit y, physical therapy, gabapentin or tricyclic antidepressants for
syndrome central pain, antispasm odics for spasticit y
Extracranial Complication Management

Head and neck


• Tongue bite, with lingual edema, fall after stroke Monitor for airway comprom ise
• Angioedema with airway compromise after rt-PA or ACEI/ARB Stop ACEI/ARB, HOB evaluation, steroids, assess difficult airway for
possible intubation
• Craniofacial trauma, fall after stroke Review CT head for intracranial bleeding, skull fracture, consider cervical-
spine imaging
Pulmonary
• Atelectasis (relative hypoventilation from hemiparetic stroke Supplem ental O2 respiratory therapy
[upper motor neuron injury])
• Aspiration pneumonia, pneum onitis NPO, antibiotics, HOB elevation
• Acute lung injury, pulm onary edema, ARDS, pulmonary embolism O2 , possible intubation mechanical ventilation
Endocrine
• Sodium and water homeostasis disturbance (e.g., SIADH) Fluid management/fluid restrict, or 3% hypertonic saline, or conivaptan,
tolvaptan (ADH antagonists), or demeclocycline
Cardiac
• Stress-induced or prim ary MI O2 , pain/HR control, aspirin, BB, coronary intervention if severe
• Neurocardiogenic injury (e.g., Takotsubo cardiomyopathy, Supplem ental O2 , pain and heart rate control, beta- blockade
troponin “leak”)
• ECG changes: arrhythmias, ST and T wave changes on ECG, atrial Treatment of arrhythm ia, ectopy, MI workup with ECG and troponin
fibrillation
Gastrointestinal
• Cushing’s ulcer H2 blockers such as ranitidine or proton pump inhibitor
• Gastrointestinal immobilit y (ileus) Mobilization, stool softener, nasogastric suction if em esis and bowel
obstruction
Genitourinary
• Acute urinary retention Urinary catheter
• Chronic urinary (urge incontinence, or neurogenic or “overactive Bladder program, neurogenic bladder agents darifenacin, solifenacin,
bladder”) and trospium
• Urinary tract infection Antibiotics, rem ove Foley as soon as possible
Limb
• Lympho-venostasis (“lim b edema”) from im mobilit y Mobilize, fluid balance
• Deep vein thrombosis, IVCF Anticoagulation if no contraindications (recent intracranial bleeding or
large hem ispheric ischem ic stroke at risk for hemorrhagic conversion)
• Contractures and adhesive capsulitis Physical therapy, botulinum toxin if contractures severe
Skin
• Decubitus ulcers Turns every 2 hours, specialt y bed, wound care nurse, optim ize nutrition
Abbreviations: ACEI, angiotensin-converting enzyme inhibitor; ARB, angiotensin receptor-blocking agent; ARDS, acute respiratory distress syndrom e; BB, beta-blocker,
if no contraindications such as asthma; BP, blood pressure; CT, computed tomogram; ECG, electrocardiogram; HOB, head of bed—elevate to 30 to 45 degrees to minimize
aspiration; HR, hypersensitive response; ICP, intracranial pressure; ICU, intensive care unit; IV, intravenous; IVCF, inferior vena cava filter; MI, myocardial infarction; NPO,
nil per os (nothing by m outh); rt-PA, recom binant tissue-t ype plasminogen activator; SIADH, syndrome of inappropriate antidiuretic horm one secretion.

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26 Medical Managem ent and Throm bolytic Therapy for Acute Ischem ic Stroke 349

HeADDFIRST (Hem icran iectom y An d Du rotom y upon Deteriora-


t ion From In farct ion -Related Sw elling Trial).27–29 Meta-an aly-
ses 30,31 sh ow th at alth ough DHC im p roves th e ch an ce of sur vival
in m align an t MCA in farct ion , it does n ot ch ange th e un derlying
in it ial st roke deficit .

Extracranial Complications
Ext racran ial com p licat ion s are listed in Table 26.4, w h ich sh ow s
th ese com plicat ion s as w ell as possible m an agem en t st rategies.
Th ese com p licat ion s are d iscu ssed in d et ail in ot h er review
ar t icles.3–5

■ Conclusion
Acu te isch em ic st roke m an agem en t is p red icated on t im ely
evalu at ion for IV r t -PA t h rom bolysis, w h ich rem ain s t h e on ly
FDA-ap p roved m edical t h erapy for AIS at p resen t . Recen t ly,
dat a in ECASS III h as sh ow n t h at som e p at ien t s ben efit from IV
r t -PA u p to 4.5 h ou rs after st roke on set . Med ical m an agem en t
of blood p ressu re, p reven t in g an d aggressively t reat ing fever,
Fig . 26.11 Chest radiograph shows aspiration pneum onia in the right
lower lobe of a 77-year-old wom an with stroke. The patient later becam e an d p reven t ing d eep ven ou s t h rom bosis an d p n eu m on ia are
progressively hypoxic and was intubated. There are also findings of hyper- crit ical to opt im izin g p at ien t ou tcom es, w h ich h ave im p roved
vascularit y or pulm onary congestion. over t im e.

References
1. Tow figh i A, Saver JL. St roke declin es from four th leading cau se of death in 10. Hacke W, Don n an G, Fiesch i C, et al; ATLANTIS Trials Invest igators; ECASS
th e Un ited St ates. St roke 2011;42:2351–2355 Trials Invest igators; NINDS rt-PA St udy Group Invest igators. Associat ion
2. Rosam ond W, Flegal K, Furie K, et al; Am erican Hear t Associat ion St at is- of ou tcom e w ith early st roke t reat m en t: pooled an alysis of ATLANTIS,
t ics Com m it tee an d St roke St at ist ics Subcom m it tee. Heart disease an d ECASS, an d NINDS rt-PA st roke t rials. Lan cet 2004;363:768–774
st roke st at ist ics—2008 u pdate: a repor t from th e Am erican Hear t Associa- 11. Gom ez CR. Tim e is brain ! J St roke Cerebrovasc Dis 1993;3:1–2
t ion St at ist ics Com m it tee an d St roke St at ist ics Subcom m it tee. Circulat ion 12. Saver JL. Tim e is brain —quan t ified. St roke 2006;37:263–266
2008;117:e25–e146 13. Row ley HA. Th e four Ps of acute st roke im aging: paren chym a, pipes, per-
3. Adam s HP Jr, del Zoppo G, Alber t s MJ, et al; Am erican Hear t Associat ion; fusion , and pen um bra. AJNR Am J Neuroradiol 2001;22:599–601
Am erican St roke Associat ion St roke Coun cil; Clin ical Cardiology Cou ncil; 14. Felberg RA, Naidech AM. Th e 5 Ps of acute isch em ic st roke t reat m en t:
Card iovascu lar Radiology an d In ter ven t ion Cou n cil; Ath erosclerot ic Pe- paren chym a, pipes, perfusion , penu m bra, an d prevent ion of com plica-
r ip h eral Vascu lar Disease an d Qu alit y of Care Ou tcom es in Research In - t ion s. South Med J 2003;96:336–342
terdisciplin ar y Working Groups. Guidelin es for th e early m an agem en t of 15. Rose JC, Mayer SA. Opt im izing blood p ressu re in n eu rological em ergen -
adult s w ith isch em ic st roke: a guidelin e from th e Am erican Heart Asso- cies. Neu rocrit Care 2004;1:287–299
ciat ion /Am erican St roke Associat ion St roke Coun cil, Clin ical Cardiology 16. Sh in HK, Dun n AK, Jon es PB, Boas DA, Moskow it z MA, Ayat a C. Vasocon -
Cou n cil, Cardiovascu lar Radiology an d In ter ven t ion Cou n cil, an d th e Ath - st rict ive n eu rovascu lar cou p ling du ring focal isch em ic dep olarizat ion s.
erosclerot ic Periph eral Vascular Disease an d Qualit y of Care Outcom es in J Cereb Blood Flow Met ab 2006;26:1018–1030
Research In terd iscip lin ar y Working Grou p s: th e Am erican Acad em y of 17. Doh m en C, Sakow it z OW, Fabriciu s M, et al; Co- Op erat ive St u dy of Brain
Neu rology affirm s th e value of th is guidelin e as an educat ion al tool for Inju r y Dep olarisat ion s (COSBID). Sp reading d ep olar izat ion s occu r in
n eurologist s. St roke 2007;38:1655–1711 h um an isch em ic st roke w ith h igh inciden ce. An n Neurol 2008;63:720–
4. Langh orne P, Stot t DJ, Rober t son L, et al. Medical com plicat ion s after 728
st roke: a m ult icen ter st udy. St roke 2000;31:1223–1229 18. St rong AJ, An derson PJ, Wat t s HR, et al. Peri-in farct depolarizat ion s lead to
5. Freem an W D, Daw son SB, Flem m ing KD. Th e ABC’s of st roke com plica- loss of perfusion in isch aem ic gyren ceph alic cerebral cor tex. Brain 2007;
t ion s. Sem in Neurol 2010;30:501–510 130(Pt 4):995–1008
6. Th e Nat ion al In st it ute of Neurological Disorders an d St roke r t-PA St roke 19. Selm an W R, Lust W D, Pun dik S, Zh ou Y, Ratcheson RA. Com prom ised
St u dy Grou p . Tissu e p lasm in ogen act ivator for acu te isch em ic st roke. m et abolic recover y follow ing spon t an eous spreading depression in the
N Engl J Med 1995;333:1581–1587 pen um bra. Brain Res 2004;999:167–174
7. Fon arow GC, Sm ith EE, Saver JL, et al. Tim elin ess of t issue-t ype plasm in o- 20. Obren ovitch TP. Th e ischaem ic pen um bra: t w ent y years on . Cerebrovasc
gen act ivator th erapy in acu te isch em ic st roke: p at ien t ch aracterist ics, Brain Met ab Rev 1995;7:297–323
h ospit al factors, an d outcom es associated w ith door-to-n eedle t im es 21. Oliveira-Filh o J, Ezzed d in e MA, Segal AZ, et al. Fever in su barach n oid
w ith in 60 m in utes. Circulat ion 2011;123:750–758 h em orrh age: relat ion sh ip to vasosp asm an d ou tcom e. Neu rology 2001;
8. Quresh i AI. Acute hyper ten sive respon se in pat ient s w ith st roke: path o- 56:1299–1304
physiology an d m an agem en t . Circulat ion 2008;118:176–187 22. Carh uapom a JR, Gupt a K, Coplin W M, Muddassir SM, Meratee MM. Treat-
9. Hacke W, Kaste M, Bluh m ki E, et al; ECASS Invest igators. Th rom bolysis m en t of refractor y fever in th e n euroscien ces crit ical care un it using a
w it h altep lase 3 to 4.5 h ou rs after acu te isch em ic st roke. N Engl J Med n ovel, w ater-circulat ing cooling device. A single-cen ter pilot experien ce.
2008;359:1317–1329 J Neu rosurg An esth esiol 2003;15:313–318

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350 III Ischemic Stroke and Vascular Insufficiency

23. Diringer MN; Neu rocrit ical Care Fever Reduct ion Trial Group. Treat m en t 28. Jü t tler E, Schw ab S, Schm iedek P, et al; DESTINY St udy Group. Decom pres-
of fever in th e n eurologic in ten sive care un it w ith a cath eter-based h eat sive surger y for th e t reat m en t of m align an t infarct ion of th e m iddle cere-
exch ange system . Crit Care Med 2004;32:559–564 bral arter y (DESTINY): a ran dom ized, con t rolled t rial. St roke 2007;38:
24. Leira R, Dávalos A, Silva Y, et al; St roke Project , Cerebrovascular Diseases 2518–2525
Group of th e Span ish Neu rological Societ y. Early neu rologic deteriorat ion 29. Fran k JI. Hem icran iectom y an d du rotom y upon deteriorat ion from in farc-
in in t racerebral h em orrh age: predictors an d associated factors. Neurol- t ion -related sw elling t rial (HeADDFIRST): first public presen tat ion of th e
ogy 2004;63:461–467 prim ar y st udy fin dings. Neurology 2003;60(Suppl 1):A426
25. Marion DW. Con t rolled n orm oth erm ia in n eurologic in ten sive care. Crit 30. Vah edi K, Hofm eijer J, Juet tler E, et al; DECIMAL, DESTINY, an d HAMLET
Care Med 2004;32(2, Su pp l):S43–S45 invest igators. Early decom pressive su rger y in m align an t in farct ion of th e
26. Kilpat rick MM, Low r y DW, Firlik AD, Yonas H, Marion DW. Hyper th erm ia m iddle cerebral ar ter y: a pooled an alysis of th ree ran dom ised cont rolled
in th e n eurosurgical in ten sive care un it . Neurosurger y 2000;47:850–855, t rials. Lan cet Neurol 2007;6:215–222
discu ssion 855–856 31. Gupt a R, Con n olly ES, Mayer S, Elkind MS. Hem icran iectom y for m assive
27. Vah edi K, Vicaut E, Mateo J, et al; DECIMAL Invest igators. Sequen t ial-de- m iddle cerebral ar ter y territor y in farct ion : a system at ic review. St roke
sign , m ult icen ter, ran dom ized, con t rolled t rial of early decom pressive 2004;35:539–543
cran iectom y in m alignan t m iddle cerebral ar ter y infarct ion (DECIMAL
Trial). St roke 2007;38:2506–2517

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27 Current Endovascular Treatment
of Acute Ischemic Stroke
Philipp Taussk y, Rabih G. Taw k , David A. Miller, and Ricardo A. Hanel

St roke rem ain s on e of th e m ain pu blic h ealth issu es w orldw ide. outcom e.7–10 Segm en t al assessm en t of MCA territor y is m ade,
It is th e th ird leading cause of death in th e Un ited States, w ith an d 1 poin t is rem oved from th e in it ial score of 10 if th ere is evi-
m ore th an 200,000 people dying from st rokes each year.1 St roke den ce of in farct ion in th at region (Table 27.1).9 Alth ough th is
is also th e m ain cau se of seriou s, long-term disabilit y in North scoring h elp s in determ in ing th e progn osis, pat ien t select ion for
Am erica. Each year, 795,000 people suffer a stroke. About 600,000 acu te en dovascu lar in ter ven t ion s rem ain s ch allenging.
of th ese are first at t acks an d 185,000 are recurren t at tacks.2 Th e u se of CT p erfu sion p aram eters (m ean con t rast t ran sit
Approxim ately 80% of all acute isch em ic st rokes are due to t im e [MTT], cerebral blood volu m e [CBV], an d cerebral blood
in t racran ial ar ter y occlu sion , m ost com m on ly th rom boem bolic flow [CBF]) m ay h elp dist ingu ish bet w een an est ablish ed area of
clot occlu sion .3 Revascularizat ion of occluded territories is th e in farct (core) an d an area of oligem ic brain t issue (pen um bra),
corn erston e of acu te isch em ic st roke t reat m en t , as it ap pears to w h ich m ay be salvaged by t im ely revascularizat ion . Alth ough an
be th e m ost beneficial of all th erapeut ic st rategies.4 Begin n ing in area of low CBV usu ally defin es th e core of in farcted t issu e, w h ich
th e 1930s, in it ial effor t s cen tered on th e con cept of clot -bu st ing can n ot be salvaged, an area of low CBF an d h igh MTT defin es
drugs; h ow ever, in th e absen ce of com pu ted tom ograp hy (CT) poten t ially salvageable pen u m bra at risk of in farct ion . Alth ough
scan s, an d faced w ith in adequ ate diagn osis, th ese effort s often th is tech n iqu e h as n ot been validated in large ran dom ized con -
resu lted in adm in ist rat ion of fibrin olyt ic d rugs to pat ien t s w ith t rolled t rials, it h as sh ow n ben efit in select ing pat ien t s w ith a
acute h em orrh age.5 Th rom bolysis for isch em ic st roke h as been salvageable p en u m bra w h o m ay ben efit from rapid revascu lar-
system at ically st u died in large ran dom ized t rials on ly sin ce th e izat ion .11–13 On t h e ot h er h an d , m agn et ic reson an ce im agin g
1990s. To date, t h rom bolyt ic t h erapy for isch em ic st roke h as (MRI) offers som e dist in ct advan tages. For exam ple, diffusion -
been invest igated in 21 ran d om ized con t rolled clin ical t rials w eigh ted im aging h as been p roven to be both sen sit ive an d sp e-
en rolling m ore th an 7,000 pat ien ts.6 cific for t h e p resen ce of early cerebral isch em ia an d is su p erior
Th e adven t of m odern im aging an d en dovascu lar tools an d to n on con t rast CT in detect ing early m et abolic abn orm alit ies
tech n ology h as revolut ion ized t reat m en t of st roke. With th e in - du e to isch em ia. It is gen erally u n derstood th at diffu sion ch anges
t rod u ct ion of m od er n en d ovascu lar tools, m ost n ot ably sten t presen t th e core of in farcted t issu e, w h ereas p erfu sion -w eigh ted
ret rievers, th e field of en d ovascu lar st roke th erapy h as u n der- im aging delin eates th e pen um bra, an area of hypoperfu sion at
gone en orm ous ch anges in th e last few years, an d th is dom ain risk. Th e volu m e d ifferen ce bet w een th ese t w o is n oted as th e
h as rem ain ed un der in ten se clin ical an d research invest igat ion . perfu sion -diffu sion m ism atch . Th e absen ce of a m ism atch w ou ld
sp eak for an in farcted core w it h ou t p en u m bra an d w ou ld ex-
clu d e p at ien t s from revascu lar izat ion effor t s, w h ereas a large
m ism atch con firm s a p en u m bra of brain t issu e, w h ich m ay be
salvageable by revascularization. Additional MRI sequences, such
■ Neuroimaging as gradien t-recalled ech o (GRE), en able th e rapid detect ion of
Th e w ide availabilit y an d sim p licit y of obt ain ing a CT scan h as in t racran ial bleeding an d can dist ingu ish bet w een isch em ic an d
m ade th is tech n ology th e m ain diagn ost ic tool in all m ajor st roke h em orrh agic st roke. Th e fact th at MRI is m ore expen sive, is less
t rials. Non con t rasted im ages en able th e rapid an d sen sit ive dis- w idely available, an d requ ires a longer scan n ing t im e, h ow ever,
tinction bet w een ischem ic an d hem orrhagic strokes, w hich is the m akes w idesp read an d prom pt u sage m ore t rou blesom e in acu te
first step in th e t reat m en t algorith m of acute st roke. Alth ough st roke treat m ent. In addition, it is cont rain dicated in pat ients w ith
n on con t rasted CT im ages do n ot provide input w ith regard to pacem akers an d cert ain im p lan ts, an d screen ing can be t im e-
cerebral perfu sion , th ey h ave proven to provide en ough in form a- con su m ing an d occasion ally n ot feasible.
t ion to assess t issu e viabilit y. Th e Alber ta St roke Program Early Despite th e w ide adopt ion of eith er CT or MRI for select ing
CT Score (ASPECTS), a 10-poin t quan t it at ive topograph ic CT scan pat ien ts w h o m igh t ben efit from en dovascu lar t reat m en t, th e
score u sed in pat ien ts w ith m iddle cerebral ar ter y (MCA) st roke, select ion criteria rem ain con t roversial an d th e su bject of ongo-
h as been w idely adopted by n um erous t rials to predict st roke ing debate.

351

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352 III Ischemic Stroke and Vascular Insufficiency

Table 27.1 Alberta Stroke Program Early CT Score (ASPECTS) Score gen erat ion th rom bolyt ics such as prourokin ase, th is led to th e
evalu at ion of in t ra-ar terial th rom bolysis in large ran dom ized
Caudate
con t rolled t rials.14 A ph ase II t rial, th e Prolyse in Acu te Cerebral
Putamen
Internal capsule Th rom boem bolism (PROACT I), tested th e safet y an d th e recan a-
Insular cortex lizat ion rates after ad m in ist rat ion of in t ra-ar terial prou rokin ase
M1 Anterior MCA cortex, corresponding to frontal operculum in 40 pat ien ts w ith acu te isch em ic st roke (39 pat ien t s receiving
M2 MCA cortex lateral to insular ribbon corresponding to anterior p rou rokin ase an d 14 p at ien t s receiving p lacebo on ly) (Table
temporal lobe 27.2).15 Th e st u dy involved 37 cen ters, an d its resu lts w ere re-
M3 Posterior MCA cortex corresponding to posterior temporal por ted in 1998. A h igh recan alizat ion rate w as sign ifican tly as-
lobe sociated w ith th e adm in ist rat ion of recom bin an t prou rokin ase
M4 Anterior MCA territory imm ediately superior to M1 (r-proUK). Hem orrh agic t ran sform at ion causing n eu rologic de-
M5 Lateral MCA territory imm ediately superior to M2 ter iorat ion w it h in 24 h ou rs of t reat m en t occu r red in 15.4% of
M6 Posterior MCA territory immediately superior to M3 t h e r-p roUK–t reated p at ien ts an d 7.1% of th e p lacebo-t reated
Note: Segm ental assessm ent of the m iddle cerebral artery (MCA) territory is pat ien ts, a t ren d th at w as n ot st at ist ically sign ifican t . Th is led to
made, and 1 point is rem oved from the initial score of 10 if there is evidence of th e PROACT II (rep or ted in 1999), w h ich ran dom ized 180 su b -
infarction in that region. jects w ith in 6 h ours of MCA occlusion to receive 9 m g of in t ra-
ar terial p rou rokin ase an d h ep arin or in t raven ous h eparin on ly.16
Th e prim ar y ou tcom e, an alyzed by in ten t ion to t reat , w as based
on th e propor t ion of pat ien ts w ith sligh t or n o n eurologic dis-
■ Stroke Therapies: abilit y at 90 days as defin ed by a m odified Ran kin scale (m RS)
score of 2 or less. Secon dar y ou tcom es in clu ded MCA recan aliza-
Intra-Arterial Thrombolysis t ion , th e frequ en cy of in t racran ial h em orrh age w ith n eu rologic
Th e d evelop m en t of m icrocat h eters d esign ed to access t h e d is- d eter iorat ion , an d m or t alit y. For th e p r im ar y an alysis, 40% of
t al in t racran ial vasculat u re en abled th e deliver y of clot-bust ing r-proUK pat ien ts an d 25% of con t rol pat ien t s h ad an m RS score
drugs to th e target clot at h igh con cen t rat ion , m in im izing th e of 2 or less (p = 0.04). Mort alit y w as 25% for th e r-proUK grou p
system ic exp osu re to h igh dosage an d likely resu lt ing in im - an d 27% for th e con t rol group. Th e recan alizat ion rate w as 66%
proved recanalization rates. Along w ith the developm ent of second- for th e r-proUK grou p an d 18% for th e con t rol group (p < 0.001).

Table 27.2 The Results of the Prolyse in Acute Cerebral Thromboembolism (PROACT) Trials II and II

PROACT I PROACT II

Number of patients 40 180


CT scan exclusion ICH, mass effect with m idline shift, intracranial tumor Sam e as PROACT hypodensit y or effacement of sulci
early changes of ischemia included in more than ⅓ of the MCA territory
Median NIHSS score r-proUK = 17, placebo = 19 r-proUK = 17, placebo = 17

Heparin All patients received IV heparin All patients received 2000-U heparin dose by
First 16 patients received 100 U/kg bolus, bolus IV, then 500 U/h
then 100 U/h infusion during 4 hours; remaining infusion for 4 hours
patients received 4000 U bolus followed by a 500 U/h
infusion for 4 hours
Agent used 6 mg of r-proUK 9 mg over 2 hours 9 mg of r-proUK over 2 hours and heparin
Placebo group Saline at 30 mL/h over 2 hours IV heparin alone
Mechanical thrombolysis Not permit ted Not permit ted
r-pro UK Placebo r-pro UK Placebo
% recanalization 58 14 66 18
(TIMI score of 2 or 3)
% Symptomatic ICH 15 7 10 2
% Outcome:
mRS 0 and 1 31 21 – –
mRS 0 to 2 – – 40 25
% Mortalit y within 90 days 27 43 25 27
Abbreviations: CT, computed tom ography; ICH, intracranial hem orrhage; MCA; m iddle cerebral artery; r-proUK, recom binant prourokinase; NIHSS, National Institutes of
Health Stroke Scale; IV, intravenous; r-proUK, recom binant prourokinase; TIMI, Throm bolysis in Myocardial Infarction; mRS, m odified Rankin scale.

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27 Current Endovascular Treatm ent of Acute Ischem ic Stroke 353

In t racran ial h em orrh age w ith n eu rologic deteriorat ion w ith in


24 h ours occurred in 10% of r-proUK pat ien t s an d 2% of con t rol
pat ien ts (p = 0.06). Despite an in creased frequen cy of early sym p -
tom at ic in tracran ial h em orrh age, t reat m en t w ith in t ra-ar terial
r-p roUK w ith in 6 h ou rs of acu te isch em ic st roke on set cau sed
by MCA occlusion sign ifican tly im proved clin ical outcom e at 90
days.16 Despite th e posit ive results of PROACT I an d II, prouroki-
n ase h as n ot been approved by th e U.S. Food an d Drug Adm in is-
t rat ion (FDA).

Early Efforts at Mechanical Thrombectomy


Th e u se of in t ra-ar terial th rom bolysis n at u rally led to effor t s to
act ively ret r ieve t h e clot , rat h er t h an lyse it by u se of d r ugs. Fig. 27.1 The Penum bra suction device, showing its approach to separat-
Obviou s advan t ages of th is ap proach , com m on ly referred to as ing and suctioning the clot.
“en dovascular th rom bectom y,” in clu de deliver y of a direct t reat-
m en t of th e occluded vessel an d poten t ially rapid flow restora-
t ion , avoidan ce of side effects from th rom bolyt ic dr ugs, an d th e fu l recan alizat ion in 75 of 131 (57.3%) t reat able vessels an d in
th eoret ical advan t age of im proving th e ou tcom e w ith revascu - 91 of 131 (69.5%) vessels after adjun ct ive th erapy (in t ra-arterial
larizat ion . Early d evices develop ed for clot rem oval in clu de th e t-PA, m ech an ical). Overall, 36% h ad favorable clin ical ou tcom e
Merci ret riever (St r yker Neu rovascu lar, Frem on t , CA) an d Pen - (m RS score 0 to 2) an d m or talit y w as 34%; both outcom es w ere
u m bra su ct ion device (Pen u m bra, Alam eda, CA) (Figs. 27.1 an d sign ifican t ly related to vascu lar recan alizat ion . Sym ptom at ic
27.2), w h ich w ere m ost w idely used prior to th e adven t of sten t in t racerebral h em orrh age occurred in 16 pat ien ts (9.8%). Clin i-
ret rievers. cally sign ifican t procedural com plication s occurred in nine (5.5%)
Th e Merci ret riever system is a flexible n it in ol w ire w ith coil pat ien ts.17
loops essen tially in a corkscrew design th at is u sed in conju n c-
t ion w ith a m icrocath eter an d an 8 or 9 Fren ch (F) balloon -gu ided
cath eter. Th e device w as ap p roved by th e FDA in Augu st 2004 for
th e in d icat ion of in t racran ial clot ret rieval in pat ien t s w ith acu te
isch em ic st rokes an d th u s w as th e first en dovascular device ap -
proved for in t racran ial th rom bectom y.17,18 Th e resu lts of th is
system w ere ou tlin ed in th e Mech an ical Em bolu s Rem oval in Ce-
rebral Isch em ia (MERCI) an d Mu lt i-MERCI t rials.17,18 Th e p h ase I
m u lticen ter t rial en rolled 30 pat ien t s w ith Nat ion al In st it u tes of
Healt h St roke Scale (NIHSS) scores of ≥ 10 in t h e set t in g of an -
giograph ic occlu sion of a m ajor cerebral ar ter y.19 A tot al of 28
pat ien ts (m ean age 68 years; m edian baselin e NIHSS score 22
[range, 12–39]) w ere t reated. Th e occlu sion sites w ere th e in t ra-
cran ial in tern al carot id ar ter y (ICA) in five (18%), th e MCA in 18
(64%), both th e ICA an d MCA in th ree (11%), an d th e ver tebro-
basilar ar ter y in t w o (7%) pat ien t s. Th e m edian t im e from on set
of sym ptom s to com plet ion of t reat m en t w as 6 hours an d 15
m in utes. Successfu l recan alizat ion (Th rom bolysis in Myocardial
Infarction [TIMI] score 2–3) w ith th e retriever alone w as achieved
in 12 (43%) p at ien t s an d w ith addit ion al in t ra-arterial recom bi-
n an t t issue-t ype plasm in ogen act ivator (r t-PA) in 18 (64%) pa-
t ien ts. Th ere w as on e p rocedu re-related tech n ical com plicat ion ,
w ith n o clin ical con sequen ce. Th ere w ere 12 asym ptom at ic in -
t racran ial h em orrh ages (43%) an d n o in ciden ts of sym ptom at ic
in t racran ial h em orrh age. At 1 m on th , 9 of 18 revascularized pa-
tients and 0 of 10 non revascularized patients ach ieved sign ifican t
recover y (m RS score ≤ 3). Ten pat ien ts (36%) died during th e 30-
day follow -u p period. Non e of th e death s w ere related to th e
st u dy device.
Th e MERCI an d Mu lt i-MERCI t r ial w ere bot h p rosp ect ive
single-arm m u lt icen ter t rials d esign ed to test th e safet y an d ef-
ficacy of th e Merci device to restore th e paten cy of in t racran ial
ar ter ies 8 h ou rs after acu te st roke.17,18 Th e Mu lt i-MERCI t rial
in clu ded 164 pat ien t s w ith a m edian NIHSS score of 19 (range, Fig. 27.2 The Merci retriever device rem oving an occlusive clot by means
15–23). Treat m en t w ith th e MERCI ret riever resulted in success- of its corkscrew design.

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354 III Ischemic Stroke and Vascular Insufficiency

Th e Pen u m bra system h as a rep erfu sion cath eter th at asp i- described as u seful tools for acute in t racran ial vessel recan aliza-
rates th e clot an d a separator device th at fragm en ts it an d pre- t ion eith er as salvage for failed revascu larizat ion w ith oth er
ven t s obst r u ct ion of t h e cat h eter. Th e m u lt icen ter p ilot t r ial tools 24 or as prim ar y t reat m en t .25
in clu ded 23 su bject s at six in tern at ion al cen ters w ith 21 vessel Usin g t h e W in gsp an sten t (St r yker) in a p rosp ect ive, FDA-
occlusions (seven in tern al carot id arteries, five m iddle cerebral approved, single-arm t rial, Levy et al25 dem on st rated th at sten t
ar teries, an d n in e basilar ar teries) t reated in 20 pat ien ts (m ean dep loym en t ap pears to be a safe an d feasible first-lin e m eth od to
NIHSS score, 21 ± 8) u p to 8 h ou rs after sym ptom on set . Th ree ach ieve recan alizat ion w h en t reat ing acute isch em ic st roke re-
en rolled subjects w ere n ot t reated becau se of vessel tor t u osit y, su lt ing from acu te in t racran ial ar terial occlu sion . Th ese au th ors
resu lt ing in an access rate of 87% (20/23). Recan alizat ion before ach ieved a 100% recan alizat ion rate (60% TIMI score of 3, 40%
in t ra-ar terial lysis w as ach ieved in all t reated cases (48% TIMI TIMI score of 2).
score of 2; 52% TIMI score of 3). Six p at ien t s w ere refractor y to Major con cern s w ith acu te sten t u t ilizat ion in clu de th e n eed
in t raven ou s r t-PA th erapy, an d n in e received p ostdevice in t ra- for im m ediate du al an t iplatelet regim en, w h ich could lead to in -
ar terial rt-PA. Good ou tcom e at 30 days (m RS score ≤ 2 or NIHSS creased rates of in t racran ial h em orrh age.
4-p oin t im provem en t) w as dem on st rated in 45% of th e pat ien t s.
Th e m or talit y rate w as 45%w ith n o device-related death s. Th ere
w ere eight cases of in t racerebral h em orrh age, of w h ich t w o w ere The Advent of Stent Retrievers
sym ptom at ic. Th e u se of adju n ct ive in t ra-ar terial th rom bolyt ic Th e lim ited su ccess of th e Merci an d Pen u m bra asp irat ion sys-
th erapy w as associated w ith a h igh er in ciden ce of h em orrh age.20 tem s an d t h e relat ive ease of revascu lar izat ion u sing in t racra-
Th e resu lt s of a su bsequ en t p rosp ect ive single-arm m u lt icen ter n ial sten ts resulted in th e developm en t of a hybrid form of clot
t rial (Pen u m bra St roke Trial) sh ow ed sim ilar resu lt s, w ith 84% ret rievers called sten t ret rievers. Th e su ccessful use of th ese re-
revascularizat ion rate, an d con sequ en tly led to FDA approval in t rievable sten t devices feat u res th e dep loym en t of th e device
Jan u ar y 2008 of th e t h rom bu s-asp irat ion device for clot rem oval w ith in th e clot . Th is leads to en t rapm en t of th e clot w ith in th e
in acu te pat ien ts w ith st roke.21,22 lu m en of th e device, en abling its rem oval an d a su ccessfu l revas-
Alth ough th e Merci an d Pen um bra devices spearh eaded th e cularizat ion w h ile ret rieving th e device. Com pared w ith oth er
era of m ech an ical th rom bectom y, th e real-p ract ice u se of th ese devices, th ere is a h igh er su ccess in revascu larizat ion w ith u se of
devices resulted in successful revascularization in on ly t w o-thirds sten t ret rievers, w ith an addit ion al advan t age of restoring cere-
of cases. bral p erfusion after th eir d ep loym en t an d prior to ret rieving th e
clot . Cu rren t m odels in clu de th e Solit aire device (Covidien /eV3,
Map le Grove, MN) an d th e Trevo d evice (St r yker Neu rovascu lar)
(Figs. 27.3 an d 27.4).
■ Intracranial Stenting for Acute Th e Solit aire device h as been com m ercially available sin ce
2009. In March 2012, th e results of th e Solitaire With th e In ten -
Ischemic Stroke t ion For Th rom bectom y (SW IFT) t rial led to FDA app roval of th is
In it ial experien ce w ith angioplast y for m ech an ical breakdow n of device for th e t reat m en t of acu te isch em ic st roke.26,27 Th e SW IFT
a clot an d th e vast use of sten t ing as th e prim ar y tool for coro- t rial w as a ran dom ized, p arallel-grou p , n on in feriorit y t rial com -
n ar y an d periph eral vessel revascularizat ion led to in it ial effor ts paring th e Solitaire device an d th e Merci. Th e t rial involved 18
at sten t ing for acu te isch em ic st roke. Before th e adven t of m icro- sites (17 in th e Un ited States an d on e in Fran ce) w ith 58 p at ien t s
cath eter-delivered sten t s, t h e u se of coron ar y sten t s w as t ried in th e Solitaire arm an d 55 p at ien t s in th e Merci group. Pat ien t s
bu t lim ited by th e n avigabilit y of th ese devices.23 h ad acute isch em ic st roke w ith m oderate to severe n eurologic
Self-exp an dable sten t s d esign ed for an eu r ysm t reat m en t deficit s an d w ere t reated w ith in 8 h ou rs of st roke on set . Th e p ri-
(Neu rofor m , St r yker; En ter p r ise, Cod m an , Rayn h am , MA) or in - m ar y en d p oin t w as a TIMI score of 2 or 3 an d flow in all t reated
t racran ial ath erosclerot ic disease (Wingsp an , St r yker) h ave been vessels w ith ou t sym ptom at ic in t racran ial h em orrh age, after u p

Fig. 27.3 Illustration of the design of the Solitaire stroke retriever.

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27 Current Endovascular Treatm ent of Acute Ischem ic Stroke 355
Fig. 27.4 Photograph of the Trevo stroke retriever.

to th ree p asses of th e assign ed device. Th e p rim ar y efficacy ou t- The high revascularization rate of current stroke retrievers has
com e w as ach ieved m ore often in th e Solitaire group th an in th e resulted in a sh ift in th e focu s of en dovascu lar st roke t reat m en t .
Merci grou p (61% vs 24%; p < 0.0001 [n on in feriorit y], p = 0.0001 Alth ough earlier effor t s w ere con cen t rated on tech n ical issu es
[su p eriorit y]). More pat ien t s h ad good 3-m on th n eu rologic ou t- relat ing to u sing th e en dovascular tools available in th e m ost ef-
com es w ith th e Solit aire th an w ith th e Merci (58% vs 33%; p = ficien t an d successful m an n er at clot ret rieval, m ore em ph asis is
0.0001 [n on in feriorit y], p = 0.02 [su p eriorit y]), an d th e 90-day curren tly put on pat ien t select ion . With a 90% su ccess rate of re-
m ortalit y w as low er in th e Solitaire group th an in th e Merci vascularizat ion , th e correct select ion of pat ien t s h as becom e a
grou p (17% vs 38%; p = 0.0001 [n on in fer ior it y], p = 0.02 [su p e- p ivotal issue, essen t ially t reat ing th e p at ien t s w h o w ill ben efit
r iorit y]). Th ese resu lts firm ly establish ed th e Solit aire d evice as from a st roke inter vention w h ile at th e sam e t im e excluding those
on e of th e m ain devices in th e t reat m en t of acu te isch em ic w h o w ill m ost likely sh ow n o ben efit or m ay even be h arm ed by
st roke. In addit ion to it s ease of u se an d low com p licat ion rate, it an in ter ven t ion , esp ecially from in t racran ial h em orrh age.
h as proven in n um erous real-pract ice t rials to be safe an d effec-
t ive for clot ret rieval an d restorat ion of flow.28–31
Illustrative Case 1
Th e Trevo device, a sim ilar sten t ret riever, ach ieved FDA ap -
proval in Augu st 2012 based on th e resu lts of th e TREVO-2 t rial.32 A 76-year-old m an w as foun d lying ou tside h is w orkplace an d
Th is w as a ran dom ized con t rolled t rial at 26 sites in th e Un ited w as t ran sported to th e h ospit al. A physical exam in at ion revealed
St ates an d on e in Sp ain an d in clu d ed ad u lt s bet w een 18 an d aph asia an d severe righ t-sided w eakn ess. His NIHSS score w as
85 years old w ith angiograp h ically con firm ed large vessel occlu - 23, an d h e w as given in t raven ous t-PA. He failed to im prove, so
sion an d NIHSS scores of 8 to 29 w ith in 8 h ou rs of sym ptom en d ovascu lar in ter ven t ion w as in it iated 2 h ou rs after th e on set
on set . Pat ien ts w ere ran dom ly assign ed to th rom bectom y w ith of sym ptom s. An occlusion of an M2 bran ch w as recogn ized. A
th e Trevo or Merci devices. Ran dom izat ion w as st rat ified by age Solitaire 4 × 20 m m device w as used an d a clot w as retrieved w ith
(≤ 68 years vs 69–85 years) an d NIHSS scores (≤ 18 vs 19–29) com p lete revascu larizat ion . A post in ter ven t ion al MRI sh ow ed
w ith altern at ing blocks of variou s sizes. Th e prim ar y efficacy en d som e left tem poral diffusion restriction. The patient im proved sig-
p oin t , assessed by an u n m asked core laborator y, w as Th rom - nifican tly an d regained his speech an d his right m otor strength
bolysis in Cerebral In farct ion (TICI) scores of ≥ 2 reperfusion w ith w ith in 48 h ou rs. He w as disch arged on postoperat ive day 5 w ith
th e assign ed device alon e. Th e p rim ar y safet y en d poin t w as a som e residu al w ord-fin ding difficu lt ies, bu t flu en t sp eech . Th ree
com posite of procedure-related adverse even t s. An alyses w ere w eeks later, h e w as back at w ork (Fig. 27.5).
don e by in ten t ion to t reat . Eigh t y-eigh t pat ien ts w ere ran dom -
ized to th e Trevo arm an d 90 pat ien ts to th e Merci Ret riever arm .
Illustrative Case 2
Seven t y-six (86%) pat ien t s in th e Trevo grou p an d 54 (60%) in th e
Merci grou p m et th e p rim ar y en d poin t after th e assign ed device An 83-year-old m an w ith a h istor y of coron ar y ar ter y disease
w as u sed (p < 0.0001 [superiorit y]). Th e in ciden ce of th e prim ar y presen ted w ith sp eech difficu lt ies an d left-sided w eakn ess. His
safet y en d p oin t did n ot d iffer bet w een grou p s (15% pat ien ts in NIHSS w as 18. CT angiograp hy sh ow ed com p lete occlu sion of th e
th e Trevo grou p vs 23% in th e Merci group ; p = 0.1826). righ t ICA, an d CT perfu sion sh ow ed a m oderate-size core in farct
To su m m ar ize, both t h e Solit aire an d t h e Trevo d evices sh ow of the basal ganglia w ith a large right hem ispheric penum bra. The
a h igh rate of su ccessfu l clot ret rieval, resu lt ing in a h igh revas- pat ien t w as t aken to th e angiograp hy su ite 6 h ou rs after sym p -
cu larizat ion rate. In con t rast to earlier d evices, w ith th ese m od - tom on set . A righ t ICA occlusion w as n oted w ith ou t in t racran ial
er n sten t ret r ievers su ccessfu l revascu lar izat ion is ach ieved in flow. After t w o passes w ith th e Solitaire device, par t ial recan ali-
90% of all large vessel occlu sion s. Solit aire an d Trevo sh ow ver y zat ion of th e carot id term in us w as ach ieved. Th en th e Trevo de-
sim ilar su ccess an d safet y rates; as a resu lt , t h e ch oice of w h ich vice w as u sed to ach ieve com plete revascu larizat ion of th e proxi-
device to u se is m ostly th e p hysician’s p referen ce. In som e cases m al MCA w ith delayed distal filling an d som e sm all rem ain ing
w h ere revascu lar izat ion is d ifficu lt , bot h d evices m ay be u sed in th rom bi. Desp ite th e su ccessfu l revascu larizat ion of in t racran ial
an effor t to ret rieve an occlu sion w it h a p ar t icu larly h igh clot flow, th e pat ien t n ever sh ow ed any n eu rologic im provem en t an d
bu rd en . h ad to be t ran sferred to a n u rsing facilit y (Fig. 27.6).
(text cont inues on page 358)

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356 III Ischemic Stroke and Vascular Insufficiency

a b

c d

Fig . 27.5a– e Illustrative case 1. (a) Com puted tom ography angiogram
of the head at the tim e of adm ission showing occlusion of the left m iddle
cerebral artery (MCA) with distal reconstitution. (b) A cerebral angiogram
with injection into the left internal carotid artery showing an MCA trifurca-
tion with occlusion of one of the M2 branches. (c) Deploym ent of a Solitaire
4 × 20-m m device into the clot, showing expansion of the sent m arkers.
(d) After retrieving the Solitaire device, complete revascularization of the
MCA trifurcation is now apparent. (e) Post interventional diffusion-weighted
m agnetic resonance im aging shows som e hyperintensities in the left insula
e and left temporal lobe.

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27 Current Endovascular Treatm ent of Acute Ischem ic Stroke 357

a b

c d

Fig. 27.6a–e Illustrative case 2. (a) Cerebral blood volum e showing an


infarcted core of the right basal ganglia and anterior temporal lobe. (b) Ce-
rebral blood flow shows a large right hem ispheric penum bra. (c) Injection
into the right com m on carotid artery shows no filling of the right internal
carotid artery (ICA). (d) Injection into the right com m on ICA with a Solitaire
6 × 20-m m stent deployed prior to retrieval showing partial revasculariza-
tion of the carotid term inus and proxim al m iddle cerebral artery (MCA).
(e ) After a final pass with the Trevo device, revascularization of the right ICA
and MCA can be seen with som e residual clot at the MCA bifurcation but
e distal filling.

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358 III Ischemic Stroke and Vascular Insufficiency

vs. 19.1%) w ith out any sign ifican t differen ces in m or talit y or th e
■ Recent Trials of Endovascular
occurren ce of sym ptom at ic in t racerebral h em orrh age. Th is st u dy
Intervention for Stroke is on e of th e first to dem on st rate im p roved fun ct ion al ou tcom es
Alth ough th e literat ure cites m any series of successfu l applica- w it h t h e u se of en d ovascu lar revascu larizat ion in ad dit ion to
t ion s of en dovascu lar th erap ies for revascu larizat ion of large st an dard st roke th erapy.
vessel occlusion , th e resu lt s of such in ter ven t ion s in th e set t ing
of clin ical t rials h ave been m ixed. Tw o recen t t rials w arran t a
m en t ion .
Th e In ter ven t ion al Man agem en t of St roke (III) t r ial (IMS3)
■ Conclusion
t r ial 33 ran d om ized p at ien t s w it h m od erate to severe acu te isch - Alth ough en dovascular st roke th erapy con t in ues to evolve w ith
em ic st roke to en d ovascu lar t h erapy after ad m in ist rat ion of h igh rates of revascu larizat ion , several ch allenges st ill n eed to
int raven ous t issue plasm in ogen act ivator (t-PA) or to adm in istra- be resolved . Th ere are st ill n o st an dard s of care, an d th e sp eed
tion of in travenous t-PA w ithin 3 h ours after onset of sym ptom s. of t ran sfer of pat ien ts to h igh ly specialized st roke cen ters is st ill
Th e p rim ar y ou tcom e m easu re u sed in th is t rial w as th e m odi- less th an opt im al. It is est im ated th at on ly 1 to 7% of st roke vic-
fied Ran kin scale score (a score of 2 or less, in dicat ing fun ct ion al t im s ar r ive at a h osp it al in t im e for st roke revascu lar izat ion
in depen den ce, at 90 days w as deem ed a favorable ou tcom e). t h erapies. Even in com m u n it ies w ith h igh ly organ ized an d act ive
Th is st u dy w as h alted p rem at u rely du e to a lack of differen ce in st roke program s, on ly 10% of st roke vict im s receive im m ediate
outcom es bet w een groups after 656 pat ien ts un der w en t ran - t reat m en t .35 Pat ien t select ion con t in u es to evolve, an d ou r cu r-
dom izat ion (434 pat ien ts to en dovascu lar th erapy an d 222 to ren t u n d erstan ding of st roke path ophysiology as seen by CT per-
in t raven ous t-PA alon e). Notably th e m odified Ran kin score of fu sion an d MRI at t im es st ill sh ow s lim ited cor relat ion w it h
2 or less at 90 days did n ot differ sign ifican tly bet w een th e t w o clin ical resu lt s an d fu n ct ion al ou tcom es. Th e tech n ical su ccess
grou ps (40.8% w ith en dovascu lar th erapy an d 38.7% w ith in t ra- in ach ieving revascularizat ion is curren tly in th e 90% range, but
ven ous t-PA; 95% con fiden ce in ter val [CI], –6.1 to 9.1) Th e rates fu r th er w ork is n eeded to ach ieve a bet ter iden t ificat ion of p a-
of m ortalit y bet w een th e en dovascular th erapy an d in t raven ous tients w h o w ill benefit from an inter vention and avoid revascular-
t-PA grou p s w ere n ot sign ifican t ly differen t at 90 days (19.1%an d ization of patien ts at high risk of post-reperfusion hem orrhage.
21.6%, respect ively; p = 0.52) n or w ere th e propor t ion s of pa- Alth ough CT perfusion is w idely available an d can be obtain ed
t ien ts w ith sym ptom at ic in t racerebral h em orrh age w ith in 30 rapidly, several au th orit ies believe th at an MRI series t ailored to
h ou rs after receiving t-PA (6.2% an d 5.9%, resp ect ively; p = 0.83). an alyzing diffu sion an d perfusion profiles w ill play a sign ifican t
A m u lt icen ter ran d om ized con t rolled t r ial of in t raar ter ial role in th e fut ure. Fur t h er develop m en t w ill be ach ieved in ob -
t reat m en t for acu te isch em ic st roke dem on st rated im p roved ef- taining physiological im aging in the angiography suite before and
ficacy of in t raar terial in ter ven t ion .34 In th is t rial, p at ien ts w ith even du ring th e st roke in ter ven t ion . Fin ally, en dovascular th er-
proxim al ar terial occlu sion s in th e an terior cerebral circu lat ion apy, w ith it s h igh revascu larizat ion rate, h as st ill n ot been proven
w ere ran dom ly assign ed to en dovascular in t raarterial t reat m en t in a ran dom ized con t rolled t rial to be su perior to in t raven ous
plu s in t raven ou s clot bu st ing m edicat ion s or clot bu st ing m edi- t-PA. Alt h ough m any p ract it ion ers believe th ere is n o equ ip oise
cat ion s alon e w ith in 6 h ou rs of sym ptom on set . In tot al 500 p a- w ith respect to th is quest ion because clin ical experien ce clearly
tients (m ean age 65 years) w ere enrolled. Th e m ajorit y of patien ts favors en dovascular tech n iqu es, several st udies are curren tly in -
(89.0%) w ere t reated w ith in t raven ous alteplase before ran dom - vest igat ing th is quest ion to an sw er it scien t ifically. As our en do-
izat ion . Th ere w as an absolute differen ce of 13.5% (95% CI, 5.9 to vascu lar techn iques evolve, th ere is a n eed for fut ure st udies to
21.2) in th e rate of fun ct ion al in depen den ce (as assessed by th e bet ter un derst an d th e path ophysiology of th e isch em ic territor y
m od ified Ran kin score, 0 to 2) in favor of th e in ter ven t ion (32.6% an d validate st roke t reat m en t paradigm s.

References
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urokin ase by using ASPECTS. St roke 2003;34:1925–1931 2014;9:658–668
15. del Zoppo GJ, Higash ida RT, Furlan AJ, Pessin MS, Row ley HA, Gent M. PRO- 27. Saver JL, Jah an R, Levy EI, et al; SW IFT Trialist s. Solit aire flow restorat ion
ACT: a ph ase II ran dom ized t rial of recom bin an t pro-urokin ase by direct device versu s th e Merci Ret riever in pat ien t s w ith acu te isch aem ic st roke
ar terial deliver y in acu te m iddle cerebral ar ter y st roke. PROACT Invest iga- (SW IFT): a ran dom ised, parallel-group, n on -in feriorit y t rial. Lancet 2012;
tors. Prolyse in Acu te Cerebral Th rom boem bolism . St roke 1998;29:4–11 380:1241–1249
16. Furlan A, Higash ida R, Wech sler L, et al. In t ra-ar terial prourokin ase for 28. Dávalos A, Pereira VM, Ch apot R, Bon afé A, Andersson T, Gralla J; Solit aire
acu te isch em ic st roke. Th e PROACT II st u dy: a ran d om ized con t rolled trial. Group. Retrospective m ulticenter st udy of Solitaire FR for revascularization
Prolyse in Acute Cerebral Throm boem bolism . JAMA 1999;282:2003–2011 in th e treatm ent of acute ischem ic stroke. St roke 2012;43:2699–2705
17. Sm ith WS, Su ng G, Saver J, et al; Mult i MERCI Invest igators. Mech an ical 29. Koh JS, Lee SJ, Ryu CW, Kim HS. Safet y an d efficacy of m ech an ical th rom -
th rom bectom y for acu te isch em ic st roke: fin al resu lt s of th e Mu lt i MERCI bectom y w ith solit aire sten t ret rieval for acute ischem ic st roke: a system -
t rial. St roke 2008;39:1205–1212 at ic review. Neurointer ven t ion 2012;7:1–9
18. Sm ith WS, Sung G, St arkm an S, et al; MERCI Trial Invest igators. Safet y and 30. Mach i P, Cost alat V, Lobotesis K, et al. Solit aire FR t h rom bectom y sys-
efficacy of m ech anical em bolectom y in acute isch em ic st roke: result s of tem : im m ediate resu lt s in 56 con secu t ive acu te isch em ic st roke p at ien t s.
th e MERCI t rial. St roke 2005;36:1432–1438 J Neu roin ter v Su rg 2012;4:62–66
19. Gobin YP, St arkm an S, Duckw iler GR, et al. MERCI 1: a ph ase 1 st udy of 31. St am pfl S, Har t m an n M, Ringleb PA, Haeh n el S, Ben dszu s M, Roh de S.
Mech an ical Em bolu s Rem oval in Cerebral Isch em ia. St roke 2004;35: Sten t p lacem en t for flow restorat ion in acu te isch em ic st roke: a single-
2848–2854 center experien ce w ith th e Solit aire sten t system . AJNR Am J Neuroradiol
20. Bose A, Henkes H, Alfke K, et al; Pen um bra Ph ase 1 St roke Trial Invest iga- 2011;32:1245–1248
tors. Th e Pen u m bra System : a m ech an ical d evice for t h e t reat m en t of 32. Nogueira RG, Lut sep HL, Gupt a R, et al; TREVO 2 Trialist s. Trevo versus
acu te st roke due to th rom boem bolism . AJNR Am J Neuroradiol 2008;29: Merci ret rievers for th rom bectom y revascu larisat ion of large vessel occlu -
1409–1413 sion s in acu te isch aem ic st roke (TREVO 2): a ran d om ised t r ial. Lan cet
21. Pen um bra Pivot al St roke Trial Invest igators. Th e Penu m bra Pivot al St roke 2012;380):1231–1240
Trial: safet y an d effect iven ess of a n ew gen erat ion of m ech anical devices 33. Broderick JP, Palesch YY, Dem ch uk AM, et al; In ter vent ion al Man agem en t
for clot rem oval in in t racran ial large vessel occlu sive disease. St roke 2009; of St roke (IMS) III Invest igators. En dovascular th erapy after in t raven ou s
40:2761–2768 t -PA versu s t -PA alon e for st roke. N Engl J Med 2013;368:893–903 (Er-
22. Tarr R, Hsu D, Kulcsar Z, et al. Th e POST t rial: in it ial post-m arket experi- rat um in N Engl J Med. 2013 Mar 28;368(13):1265)
en ce of th e Pen u m bra system : revascu larizat ion of large vessel occlusion 34. Berkh em er OA, Fran sen PS, Beum er D, et al; MR CLEAN Invest igators.
in acute isch em ic st roke in th e United St ates an d Europe. J Neuroin ter v A ran dom ized t rial of in t raar terial t reat m en t for acu te isch em ic st roke.
Surg 2010;2:341–344 N Engl J Med 2015;372:11–20
23. Levy EI, Ecker RD, Horow it z MB, et al. Sten t-assisted in t racran ial recan ali- 35. Morgen stern LB, St aub L, Ch an W, et al. Im proving deliver y of acute st roke
zat ion for acu te st roke: early resu lt s. Neurosu rger y 2006;58:458–463, th erapy: Th e TLL Tem p le Fou n dat ion St roke Project . St roke 2002;33:
discu ssion 458–463 160–166

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28 Pathophysiology and Surgical
Management of Intracerebral Hematomas
A. David Mendelow

Sp on t an eou s, in t racerebral h em orrh age (ICH) (Fig. 28.1) is on e like th e in tern al cap sule, th en t h e pat ien t in evit ably w ill becom e
of t h e m ost d evast at in g for m s of st roke. Th e m orbid it y an d perm an en tly h em ip legic. Disru pted w h ite m at ter t racts w ill
m or t alit y from ICH is h igh , p ar t icu larly if t h ere is associated n ever realign ; n eu rosurgeon s recogn ize th is as a basic prin ciple.
in t raven t ricular h em orrh age (IVH) an d hydroceph alus.1 Th ese By con t rast , w h en a w h ite m at ter t ract is d isplaced rath er th an
pat ien ts h ave a m orbidit y an d m or t alit y th at app roach es 90%. By t ran sected, th en rem oval of th e m ass effect m ay allow it to re-
con t rast , p at ien t s w ith n o IVH or hydroceph alu s h ave a m orbid - cover. Th is is w hy m any pat ien t s w ith d eep -seated basal ganglia
it y an d m ort alit y of on ly 70%. Th e ou tcom e from spon tan eous h em atom as presen t w ith a h em iplegia, an d th ey do n ot recover
su p raten torial ICH is ver y differen t from th e ou tcom e from sp on - from th is deficit u n less t h e in ter n al cap su le is sp ared, as for ex-
t an eou s cerebellar ICH. Also, an ICH d u e to an eu r ysm or ar te- am p le, w it h a sm all, d eep -seated h em atom a. Th e p recise site of
r ioven ou s m alform at ion (AVM) develop s at a differen t bleeding t h e d eep - seated ICH in relat ion to th e in ter n al cap su le is t h ere-
pressu re from a spon t an eou s hyp er ten sive ICH. Th e age of th e fore of great p rogn ost ic sign ifican ce.
pat ien t an d associated sen escen t at rop hy also affect th e con se-
qu en ce of th e h em orrh age. Th ese con dit ion s are often lum p ed
togeth er, but an un derstan ding of th eir path ophysiology sh ould Elevated Intracranial Pressure and Reduced
m ake it clear t h at t h ey are ver y d ifferen t d iseases. Mu ch also Cerebral Perfusion Pressure
d epen ds on th e cau se of th e ICH.
Th e secon d m ech an ism of brain dam age w ith ICH is elevat ion of
Cau ses of in t racerebral h em orrh age in clude th e follow ing:
in t racran ial pressure (ICP) an d th e frequen t associat ion w ith re-
• Hyper ten sion du ced cerebral perfu sion p ressu re (CPP). Th is is on e of th e m ech -
• An eu r ysm s an ism s again st w h ich n eu rosurgeon s can direct t reat m en t eith er
• AVMs an d ar terioven ou s (AV) fist ulas by m edical or su rgical m ean s. A full un derstan ding of th e path o-
• Clot t ing disorders physiology of au toregu lat ion is n eeded by th e crit ical care team
• Am yloid angiop athy to avoid un n ecessar y blood pressu re reduct ion w h en th e CPP
• Recreat ion al drugs (crack/cocain e) m ay already be low becau se of elevated ICP. Clin ical t rials are
• Tu m ors curren tly un der w ay to evaluate th e acute t reat m en t of hyper-
• Trau m a ten sion in pat ien ts w ith ICH (see below ). Th ere is also th e danger
• Cavern ou s angiom as th at persisten tly h igh blood pressu re m ay cau se fu rt h er h em or-
• Hem orrh agic conversion of isch em ic st roke rh age exp an sion .
• Ven ou s th rom bosis

With som e of th ese causes, th ere is a risk of h em orrh age ex- The Perihematoma Penumbra
pan sion or rebleeding. Th ere are th erefore t w o issu es to con sider
in th e m an agem en t of pat ien ts w ith ICH: first , th e t reat m en t of The m ost interesting controversy in patients w ith ICH is the ques-
th e ICH it self, an d secon d, th e t reat m en t of th e u n derlying cau se. t ion abou t w h eth er or n ot a pen u m bra of fu n ct ion ally im p aired
Many t im es th ese t w o ap p roach es h ave to occu r sim u ltan eously. bu t p oten t ially viable t issu e su rrou n d s t h e clot it self. Th ere is
So, for exam p le, a p at ien t w ith an u n derlying AVM or an eu r ysm exten sive experim en t al eviden ce th at con firm s th e presen ce of
m ay n eed t h e lesion t reated im m ed iately or at th e t im e of evacu - an isch em ic pen um bra aroun d an ICH (Fig. 28.2).2,3 Th ere is also
at ion of th e ICH. Th ese sp ecific sit u at ion s are discu ssed later in exp erim en t al eviden ce th at rem oval of a m ass lesion im proves
th e ch apter; th e t reat m en t of an eu r ysm s an d ar terioven ous m al- cerebral blood flow (CBF) com pared w ith con t rols.4 Clin ical CBF
form ation s is con sidered in detail in Section s V and VI of this book. m easurem en t w ith single ph oton em ission com pu ted tom ogra-
phy (SPECT) scan n ing h as also iden t ified th e p en um bra in p a-
t ien ts w ith sp on tan eou s su praten torial ICH (Fig. 28.3).5 Like-
w ise, Zazulia et al6 iden t ified a p en u m bra w ith redu ced CBF 21
h ours after an ICH u sing a posit ron em ission tom ography (PET)
■ Mechanisms of Brain Damage w ith scan (Fig. 28.4). Fu rth er eviden ce of th ere being a p en u m bra h as
Intracerebral Hemorrhage been obt ain ed from specim en s of brain at th e edge of th e h em a-
tom a th at w ere n ecessarily rem oved to gain access via a cran iot-
White Matter Tract Disruption om y. Alth ough th ere is isch em ic n eu ron al dam age im m ediately
A pat ien t w ith ICH can suffer brain dam age th rough a variet y of adjacen t to th e h em atom a, th ere is eviden ce of apoptosis sligh tly
m ech an ism s. If th e ICH dest roys im port an t w h ite m at ter t ract s m ore rem otely from th e h em atom a. Th is p rogram m ed cell d eath

360

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28 Pathophysiology and Surgical Management of Intracerebral Hematomas 361

Fig. 28.1 Magnetic resonance im aging (MRI) showing a left superficial


intracerebral hem orrhage (ICH) (black area at right) with a penum bra of
functionally impaired but potentially viable tissue around it (white area).

b
in dicates th at cells th at w ere on ce living u n der w en t apoptosis
Fig. 28.2a,b (a) Sections of a rat brain showing a contained intracerebral
(Fig. 28.5). Th is fu r th er eviden ce favors th e existen ce of a p en - hematoma on the left. (b) A C14 auto radiograph of an im mediately adja-
u m bra in som e pat ien ts w ith ICH. cent section from the sam e rat showing a reduction in blood flow that
In addit ion to th e m ass effect , blood itself an d its con ten ts are occupies a m uch larger area than the hem atom a itself.3
toxic to t h e brain . Th e con cept of a ch em ical p en u m bra, t h ere-
fore, also exist s. Hem oglobin an d it s breakd ow n p rod u ct s an d
iron are d irect ly toxic, an d t h e p er ih em atom a ed em a seen in th ere w ere n o pen u m bra, su ch t reat m en t w ou ld be fu t ile. It m ay
t h e m ajorit y of p at ien t s m ay be du e to blood–brain barrier (BBB) w ell be t h at th e p en u m bra exist s in som e p at ien t s bu t n ot in
breakdow n . Th ere h ave been over 150 experim en tal ICH st udies ot h ers, an d m edical an d surgical th erapies sh ould be targeted at
sin ce 2008, m any of w h ich are su m m arized by Zh ang an d Colo- th ese p at ien t s. Th e experim en t al w ork, th erefore, is h igh ly rele-
h an 7 in th e proceedings of th e Th ird In tern at ion al Con feren ce on van t , because it t ran slates in to clin ical t rials th at seek to m it igate
In t racerebral Hem orrh age. A fur th er update w as provided at th e th e ch em ical p rocesses w ith in th e p erih em atom a edem a an d to
fourth such conference (http://w w w.m edim ond.com /proceedings/ rep erfu se th e pen um bra.
m oreinfo/20110502.htm ). Throm bin is im m ediately form ed w hen
blood is released in to th e brain , eith er directly or becau se of BBB
breakdow n.8 In addition, inflam m atory changes are produced w ith Obstruction of Cerebrospinal Fluid Circulation
elevat ion of t u m or n ecrosis factor-α (TNF-α ) an d in terleu kin -1 and Absorption Leading to Hydrocephalus
(IL-1).9 Th ese p rocesses st im u late t h e release of in tercellu lar
ad h esion m olecules (ICAM-1 an d E-select in ),10 w h ich facilit ate Obst r u ct ive hyd rocep h alu s m ay resu lt from t h e m ass of blood
th e m igrat ion of n eu t roph ils in to brain p aren chym a, th u s aggra- in th e th ird or four th ven t ricle or com pression of eith er of th ese
vat ing th e in flam m ator y effect s fur th er. Th rom bin also directly by adjacen t h em atom a. Som e pat ien ts deteriorate h ours or even
act ivates protease-act ivated receptors (PARs), w hich in duce act i- days after th e origin al ict us pu rely as a result obst ru ct ive hydro-
vat ion of sign aling m olecules th at lead to apoptosis, ast rocyte ceph alus. W h en th e h em atom a is in th e posterior fossa, extern al
proliferation, and nerve grow th factor production.11 Th ese patho- ven t ricular drain age (EVD) m ay im prove th e level of con scious-
physiological p rocesses m ay be m odifiable, th u s op en ing th e n ess, bu t if t h ere is brain stem com p ression , t h en t reat m en t of
w ay for n ovel th erapeu t ic m ed ical st rategies. t h e hyd rocep h alu s sh ou ld occu r sim u lt an eou sly w it h clot evac-
Many of th e m edical an d su rgical t reat m en t s for ICH dep en d u at ion . By con t rast , th e pat ien t w ith su praten torial ven t ricu lar
on th e existen ce of a pen um bra to preser ve brain fun ct ion ; if h em or rh age an d associated t h ird an d t h en fou r t h ven t r icu lar

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362 III Ischemic Stroke and Vascular Insufficiency

Fig. 28.3a,b Computed tomography (CT) and m atching single photon


em ission computed tom ography (SPECT) scans soon (a) and delayed (b)
after intracerebral hem orrhage (ICH) absorption showing a penum bra
with a flow increase of bet ween 15 and 40% of baseline (arrow), using
difference-based region growing (DBRG) m ethod.5

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28 Pathophysiology and Surgical Management of Intracerebral Hematomas 363
Fig . 28.4 Com puted tom ography (CT) and positron
em ission tom ography (PET) scans of a patient with an
intracerebral hem orrhage (ICH) dem onstrating a reduc-
tion in cerebral blood flow (CBF) despite preserved oxy-
gen extraction. 6

blood m ay resp on d to u n ilateral or bilateral EVD, alt h ough t h e Further Bleeding


cath eter frequ en tly becom es obst r u cted w ith clot ted blood. Tw o
clin ical t rials (Clot Lysis: Evalu at ing Accelerated Resolu t ion of In - In younger pat ien ts, 10 to 18%h ave an un derlying st ru ct ural vas-
traven tricular Hem orrhage [CLEAR IVH] and CLEAR III) are under- cular lesion .12 In older pat ien ts w ith larger ICHs, 30 to 40% of
w ay to evalu ate th e role of t ran scath eter fibrin olysis to p reven t h em atom as w ill en large over th e first 24 to 48 h ours.13 Th ese
su ch blockage (see below ). Th e m ain ten an ce of CPP m ay be t w o differen t t ypes of secon dar y ICH are both im p or tan t . An eu -
ach ieved by preven t ing excessive low ering of th e m ean ar terial r ysm s, AVMs, an d AV fist ulas m ay require t reat m en t in th eir ow n
blood pressure; clin ical t rials (An t ihyper ten sive Treat m en t of righ t at differen t t im es. In gen eral, an eu r ysm s are best dealt w ith
Acute Cerebral Hem orrh age II [ATACH II] an d In ter ven t ion s to acu tely at t h e t im e of evacu at ion of an ICH.14 AVMs are m ost
Redu ce Acu te Care Tran sfers II [INTERACT II]) are in p rogress to easily accessed su rgically w ith in 12 w eeks of th e ict u s becau se
address th is issu e. th ereafter th e h em atom a absorbs, m aking su rgical access m ore

Fig. 28.5 The site of apoptosis from specimens taken


during craniotomy for evacuation of intracerebral hem or-
rhage (ICH). The stains used to dem onstrate apoptosis
were Fractin and Ku-80 antibody stains. (M.S. Siddique,
personal com m unication.)

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364 III Ischemic Stroke and Vascular Insufficiency

difficu lt th an in th e early stages. Th e t im ing of t reat m en t of AV vest igat ion in t h ose p at ien t s w it h su d d en on set of h eadach e or
fist ulas depen ds on w h eth er or n ot th ere is cerebral ven ous re- raised ICP. For t u n ately, an ICH is easily recogn ized on bot h CT
flu x (CVR). The Borden,15 Cognard 16 an d Djin djian 17 classification s an d MRI in th e acute ph ase. As t im e goes by, th e radiological fea-
all at t ribu te h igh er risk of h em orrh age to th ose cases w ith evi- t u res of ICH ch ange, both on CT an d MRI (Table 28.1). On CT
den ce of CVR. Th e en largem en t of lobar h em atom as follow ing scan s, th e h igh den sit y of blood seen in it ially m ay fad e th rough a
hyper ten sion or cerebral am yloid angiopathy m ay be aggravated ph ase of isoden sit y to low den sit y. Th is can m ake dist inguish ing
by severe persisten t hyper ten sion . Th is is w hy th e advocates of a subacute ICH from oth er m ass lesion s difficult (Fig. 28.6). Many
low ering blood p ressu re are so en th u siast ic abou t th e possibilit y n eu rosurgical cen ters perform CT angiography (CTA) or MR angi-
th at m ed ical th erapy m ay lim it th e expan sion of th e ICH. Th e ography (MRA) at th e t im e of th e first scan to exclude un derlying
cou n terargu m en t abou t low ering CPP w as discu ssed in th e p re- vascu lar lesion s such as an eur ysm s (Fig. 28.6d) or ar terioven ous
viou s su bsect ion ; th e t w o t rials referred to sh ould resolve th e m alform at ion s.
issu e on e w ay or an oth er in du e cou rse. Fu rth er bleeding, an d
th erefore expan sion w ith secon dar y brain dam age, m ay also be
p reven ted by rapidly reversing clot t ing disorders, or even w ith
th e use of th e n ew th erapeut ic procoagulan t st rategies. For ex- ■ Surgical Management of
am ple, recom bin an t factor VIIa sh ow ed p rom ise in an early t rial. Intracerebral Hemorrhage
But th e recen t Factor Seven for Acu te Hem orrh agic St roke Trial
(FAST) failed to d em on st rate efficacy.18 Oth er n ew p rocoagu lan t Th ere are th ree object ives in th e su rgical t reat m en t of ICH. Th e
st rategies are being develop ed. first is to preven t fur th er bleeding eith er from th e w alls of th e
ICH or from a st ru ct ural vascular lesion such as an an eur ysm or
AVM. All th ese object ives can be ach ieved by cran iotom y, but
cran iotom y m igh t cause h arm w ith deep h em atom as, because of
■ Clinical Presentation th e n eed to t raverse n orm al brain t issu e. Th e in tern at ion al Su r-
Pat ien t s w it h ICH m ay p resen t w it h h eadach e, d ist u rbed con - gical Trial in In t racerebral Hem orrh age (STICH) 19 suggested th at
sciou sn ess, a st roke-like syn d rom e, or com a of su d d en on set . su p erficial h em atom as th at w ere t reated w ith open cran iotom y
Th ese sym ptom s m ay be th e m an ifestat ion s of elevated ICP. Pre- h ad a bet ter ou tcom e t h an d eep h em atom as. How ever, as t h is
sen tat ion as a st roke is com m on , th e diagn osis often being m ade w as n ot t h e p r im ar y ou tcom e m easu re, m ore t rials h ave been
on com puted tom ography (CT) or m agn et ic reson an ce im aging u n dertaken . STICH II is close to com plet ion ,20 w ith 572 pat ien ts
(MRI) scan n ing. Som et im es focal sign s m ay be presen t w ith ou t ran dom ized. Th e resu lt s sh ould be available at th e en d of 2013,
feat ures of raised ICP, an d epilepsy is th e presen t ing feat ure in w h en 600 pat ien ts sh ould h ave com pleted th eir 6-m on th follow -
20% of all pat ien ts w ith ICH. In th ose pat ien t s w h o presen t w ith u ps. In STICH II, superficial h em atom as are ran dom ized to early
a sm all h em atom a an d progressive en largem en t , th e clin ical pic- su rger y or in it ial con ser vat ive t reat m en t; p at ien ts w ith deep -
t u re m ay be dom in ated by in creasing ICP w ith deteriorat ion in seated h em atom as or IVHs are exclu d ed . Pat ien ts w ith an eu r ys-
con sciou sn ess or by an app aren t st roke exten sion . It is w ell rec- m al ICH h ave been sh ow n to fare bet ter w ith cran iotom y, an d all
ogn ized th at an ICH is difficult to dist inguish from an isch em ic su ch p at ien ts h ave been exclu ded from th e su bsequ en t t rials of
st roke on clin ical grou n ds alon e. In th e case of cerebellar h em or- surger y for ICH.14
rh age, th e presen tat ion m ay be w ith focal cerebellar sign s an d Th e secon d object ive is to rem ove th e m ass effect of th e ICH to
delayed deteriorat ion in con sciou sn ess du e to elevated ICP from restore fu n ct ion of any p en um bra th at m igh t exist . Th ere is n o
obst ruct ive hydroceph alus. In som e cases, th e cerebellar presen - doubt th at su rger y in any form h as th e p oten t ial to ach ieve th is
tation is relatively silent, and the prim ar y presentation is w ith de- object ive. For su p er ficial h em atom as, cran iotom y is t h e ideal
teriorating consciousness due to the obstructive hydrocephalus. ap proach to restore th e pen u m bra. For deep -seated h em atom as,
In all th ese sit uat ion s CT or MRI is th e m ain stay of diagn osis. m in im al in ter ven t ion tech n iqu es are less likely to h ar m t h e
overlying cortex an d m ore likely to safely ach ieve th e secon d ob -
jective of su rger y. To th is en d, th e Min im ally Invasive Surger y
Imaging plus t-PA for In t racerebral Hem orrh age Evacu at ion (MISTIE II)
For p at ien t s w h o presen t w ith a st roke syn drom e, MRI is often t rial21 rep orted th at clot w as successfu lly rem oved in 93 pat ien t s.
t h e p r im ar y invest igat ion , w h ereas CT is often t h e p r im ar y in - Th e outcom e of MISTIE III is aw aited. An in d ep en den t pat ien t

Table 28.1 MRI and CT Scan Features of Intracerebral Hemorrhage at Different Times After the Initial Ictus

MRI Appearance of Clot


CT Appearance
Time from Ictus Clinical Description T1 T2 State of Hemoglobin of Clot

Immediate Immediate Isointense Bright Intracellular oxyhemoglobin Bright


6 hours Acute Isointense Dark Intracellular deoxyhemoglobin Bright
6–48 hours Early subacute Bright Dark Extracellular deoxyhemoglobin Bright
2 weeks Late subacute Bright Bright Extracellular methemoglobin Isointense
More than 3 weeks Chronic Dark Dark Hem osiderin Dark
Abbreviations: MRI, m agnetic resonance im aging; CT, computed tom ography.

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28 Pathophysiology and Surgical Management of Intracerebral Hematomas 365

a b

c d

Fig. 28.6a–d Computed tom ography (CT) and m agnetic resonance im - on MRI. (c) Im aging finding of chronic blood on CT. (d) CT angiogram dem -
aging (MRI) scans of different intracerebral hem orrhages (ICHs). (a) Im ag- onstrates a ruptured aneurysm of the middle cerebral artery.
ing finding of acute blood on CT. (b) Im aging finding of late subacute blood

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366 III Ischemic Stroke and Vascular Insufficiency

dat a (IPD) m et a-an alysis of eigh t previou s t rials of su rger y for Craniotomy
ICH (2,186 pat ien t s) in dicated th at early surger y (w ith in 8 h ours)
St an dard cran iotom y en ables evacu at ion of th e h em atom a an d
is likely to h ave th e greatest ben efit , part icu larly w h en th e h e-
h em ostasis un der visual con t rol. Cran iotom y ach ieves both th e
m atom a volum e w as 20 to 50 m L, th e Glasgow Com a Scale score
first an d secon d object ives referred to above. Alth ough it is n ot
w as bet w een 9 an d 12, an d pat ien ts w ere aged bet w een 50 an d
essential, the operating m icroscope and im age guidance facilitate
69 years.22 A sum m ar y of th e t im ing com pon en t of th e IPD m eta-
the perform ance of a m ore accurate and effective craniotom y. The
an alysis is sh ow n in Fig. 28.7. Overall m et a-an alysis of t h e 14
u se of m odern n on st ick bipolar forceps (Kir w an Aura, Kir w an
prosp ect ive ran dom ized con t rolled t rials of su rger y for ICH th at
Su rgical Produ ct s, Marsh field, MA; Codm an Iso- Cool t ip s, Med-
h ave been p u blish ed u p to 2010 is su m m ar ized in Fig. 28.8. It
lin e, Mu n d elein , IL), en su re m ore effect ive bip olar coagu lat ion
does app ear from th ese t rials, w h ich h ave t aken p lace over h alf a
w ith out ch arring an d st icking to coagulated t issues. In t raopera-
cen t u r y, that surger y redu ces th e m orbidit y an d m or talit y in
t ive im aging w ith MRI, CT, or th ree-dim en sion al u lt rasou n d can
these patients. The fin dings from these m eta-analyses w ill have to
also be used to con firm total rem oval of th e clot . Rebleeding can
be con firm ed or refuted in th e ongoing surgical t rials (STICH II
also be m in im ized w ith th e use of h em ostat ic m aterials such as
an d MISTIE III).
Su rgicel, Fibrillar, Gellat icel, or FloSeal (Ba xter, Deerfield, IL). On
Th e th ird object ive is to t reat hyd roceph alu s eith er du e to IVH
occasion , an un expected vascular m alform at ion , an eur ysm , or
or secon dar y to in fraten torial (cerebellar) h em orrh age. With cer-
t u m or m ay be en cou n tered at th e t im e of su rger y. Th e advan tage
ebellar h em orrh age th e hydroceph alu s m ay m an ifest itself 8 to
of cran iotom y is th at it en ables t h ese lesion s to be d iagn osed
12 h ours after th e on set of th e ict u s. Careful n eurologic m on itor-
and treated expeditiously. The disadvantage of craniotom y is that
ing is essent ial to differen t iate th e in it ial effects of th e cerebellar
deep -seated lesions require access through undam aged brain. Such
dam age from th e raised ICP cau sed by hydrocep h alu s becau se
deep -seated lesion s m ay be bet ter t reated u sing m in im ally inva-
th is is easily t reat able w ith EVD. By con t rast , p u re IVH produ ces
sive tech n iques su ch as stereot act ic aspirat ion or en doscopy.
a m ore acute an d rapid on set of hydroceph alus. In cases of pure
IVH, external ven t ricular drain s ten d to block as th e blood clot s
w ith in th em . For this reason, the CLEAR III trial23 aim s to random -
Minimally Invasive Techniques
ize 500 patien ts to EVD w ith an d w ithout tissue-t ype plasm in o-
gen activator (t-PA). Alm ost h alf of th ese pat ien ts h ave n ow been Stereotact ic or free-h an d aspirat ion can be u sed for any h em a-
ran dom ized. tom a but is ideal for deep -seated lesion s. Th e difficult y w ith as-

Fig. 28.7 Independent patient data (IPD) m eta-analysis from eight trials showing that early intervention (within 8 hours of ictus) improves the outcome
from surgical evacuation. evacuation. (Reprint with perm ission from ref. 22.)

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28 Pathophysiology and Surgical Management of Intracerebral Hematomas 367

Fig. 28.8 Meta-analysis showing death and disabilit y of the 14 trials of surgical treatm ent for intracerebral hem orrhage (ICH) that had been published
up to 2010.

pirat ion is th at th e evacu at ion is often in com p lete. It is for th is Brainstem Hemorrhage
reason th at t-PA–assisted drain age h as been recom m en ded.40 A
Pr im ar y h em or rh age in to t h e brain stem cau ses d evast at in g
form al prospect ive ran dom ized con t rolled t rial (MISTIE III) is
n eu rologic im pairm en t , depen ding on th e precise site of th e
plan n ed follow ing th e su ccessfu l resu lts of MISTIE II.21 En dos-
h em orrh age. Th ese lesion s are often associated w ith cavern ous
copy w as first recom m en ded by Au er et al31 in 1989 an d is cur-
angiom as, w h ich can be excised at th e t im e of clot evacuat ion ,
ren t ly being evalu ated in th e MISTIE–CT- Gu id ed En d oscop ic
provided th at su rgical access does n ot create m ore dam age th an
Su rger y (MISTIE-ICES) t rial.41 En doscop ic su rgical rem oval m ay
th e bleed it self. Th is is par t icu larly th e case w h en th e h em atom a
prove to be th e m ost effect ive form of clot evacu at ion , bu t fu r-
an d caver n ou s angiom as reach a su rgically accessible su r face
th er clin ical t rials are n eed ed.
of t h e brain stem . Su ch su rger y som et im es p rod u ces grat ifying
resu lt s.44
Decompressive Craniectomy
Decom pressive cran iectom y is occasion ally u sed after rem oval of
ICH because of a ver y t igh t brain th at m akes dural closure diffi-
cult . How ever, few n eurosurgeon s pract ice decom pressive cran i-
■ Conclusion
ectom y for ICH, and a review has indicated that it is seldom used.42 Alth ough th ere is clear eviden ce of th e efficacy of surger y from
m et a-an alysis of previous ran dom ized con t rolled t rials, n o in di-
vidual t rial h as been large en ough to bring about ch anges in
Cerebellar Hemorrhage
clin ical p ract ice. It is for th is reason th at t h e eviden ce from ongo-
Th e ou tcom e from cerebellar h em orrh age can be su rprisingly ing clin ical t rials (STICH II, MISTIE III, an d CLEAR III) is aw aited.
su ccessfu l. For th is reason su rger y is m ore frequ en tly recom - Firm con clu sion s about m an agem en t of p at ien ts w ith ICH m ust
m en ded for cerebellar h em orrh age th an w ith su praten torial ICH. aw ait th ese results. Th e except ion s in clude th e t reat m en t of pa-
No p rosp ect ive ran d om ized con t rolled t rials h ave been u n der- t ien ts w ith ICH du e to an u n derlying st ru ct u ral vascu lar lesion ,
taken . A useful algorith m for th e t reat m en t of cerebellar h em or- and patients w ith cerebellar hem orrhage w here the m anagem ent
rh age w as suggested by Math ew et al.43 of hydrocep h alus is of overriding im por tan ce.

References
1. Bh at t ath iri PS, Gregson B, Prasad KS, Men delow AD; STICH Invest igators. term ch anges in local cerebral blood flow m easured by autoradiography.
In t raven t ricular h em orrh age an d hydroceph alus after spon t an eous int ra- Neurol Res 1984;6:189–193
cerebral h em orrh age: result s from th e STICH t rial. Act a Neuroch ir Suppl 4. Kingm an TA, Men delow AD, Grah am DI, Teasdale GM. Experim ent al in -
(Wien ) 2006;96:65–68 t racerebral m ass: descript ion of m odel, in t racran ial pressure ch anges an d
2. Men d elow AD. Mech an ism s of isch em ic brain dam age w it h in t racere- neu ropath ology. J Neuropath ol Exp Neurol 1988;47:128–137
bral h em or rh age. St roke 1993;24(12, Su p p l):I115–I117, d iscu ssion I118– 5. Sid diqu e MS, Fern an d es HM, Wooldr idge TD, Fenw ick JD, Slom ka P,
I119 Men delow AD. Reversible isch em ia aroun d int racerebral h em orrh age: a
3. Mendelow AD, Bullock R, Teasdale GM, Graham DI, McCu lloch J. In t ra- single- ph oton em ission com pu terized tom ography st udy. J Neurosurg
cran ial haem orrh age in duced at arterial pressure in th e rat . Par t 2: Sh or t 2002;96:736–741

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6. Zazulia AR, Diringer MN, Videen TO, et al. Hyp operfu sion w ith ou t isch - 26. Ch en X, Yang H, Ch eng Z. The com parat ive st udy of th e tot al m edical and
em ia surroun ding acute in t racerebral h em orrh age. J Cereb Blood Flow surgical t reat m en t of hyperten sive in t racerebral h aem orrh age. Act a Acad
Met ab 2001;21:804–810 Med Sh angh ai 1992;19:234–240
7. Zh ang JH, Coloh an A. In t racerebral Haem orrh age Research : From Ben ch to 27. Teernst ra OP, Evers SM, Lodder J, Leffers P, Fran ke CL, Blaauw G. Stereot ac-
Bedside. Lom a Lin da, CA: Springer; 2010 t ic t reat m en t of in t racerebral h em atom a by m ean s of a plasm in ogen act i-
8. Xi G, Reiser G, Keep RF. Th e role of th rom bin an d throm bin receptors in vator: a m u lt icen ter ran dom ized con t rolled t rial (SICHPA). St roke 2003;
isch em ic, h em orrh agic an d t raum at ic brain injur y: deleterious or protec- 34(4):968–974
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9. Hua Y, Keep RF, Hoff JT, Xi G. Brain inju r y after in t racerebral h em orrh age: BA. Outcom e assign m ent in th e In ternat ion al Surgical Trial of In t racere-
th e role of th rom bin an d iron . St roke 2007;38(2, Su pp l):759–762 bral Haem orrh age. Act a Neu roch ir (Wien ) 2003;145(8):679–681
10. Th orp KM, Sou th ern C, Bird IN, Mat th ew s N. Tu m our n ecrosis factor in - 29. Wang W Z, Jiang B, Liu HM, et al. Min im ally invasive cran iop u n ct u re
d u ct ion of ELAM-1 an d ICAM-1 on h u m an u m bilical vein en d ot h elial t h erapy vs. con ser vat ive t reat m en t for spon t an eous in t racerebral h em or-
cells—an alysis of t u m our n ecrosis factor-receptor in teract ion s. Cytokin e rhage: result s from a ran dom ized clinical t rial in Ch in a. Int J St roke 2009;
1992;4:313–319 4(1):11–16
11. Xi G, Keep RF, Hoff JT. Th rom bin an d secon dar y brain dam age follow ing 30. McKissock W, Rich ardson A, Taylor J. Prim ar y in t racerebral h aem orrh age:
in t racerebral h aem orrh age. In : Carh uapom a JR, Mayer SA, Han ley DF, eds. a con t rolled t rial of su rgical an d con ser vat ive t reat m en t in 180 u n selected
In t racerebral Haem or rh age. Cam bridge, Englan d : Cam bridge Un iversit y cases. Lan cet 1961;278:221–226
Press; 2010:206–216 31. Auer LM, Dein sberger W, Niederkorn K, et al. En doscopic su rger y versus
12. Zh u XL, Ch an MS, Poon WS. Spon t an eou s in t racran ial h em orrh age: w h ich m edical t reat m en t for spon t aneou s int racerebral h em atom a: a ran dom -
pat ien t s n eed diagn ost ic cerebral angiography? A p rosp ect ive st u dy of ized st udy. J Neurosurg 1989;70:530–535
206 cases and review of the literat ure. Stroke 1997;28:1406–1409 32. Juvela S, Heisken en O, Poran en A, et al. Th e t reat m en t of spon t an eous in -
13. Broderick JP, Brot t TG, Duldn er JE, Tom sick T, Leach A. In it ial an d recurren t t racerebral h em orrh age. A prospect ive ran dom ized t rial of surgical an d
bleeding are th e m ajor causes of death follow ing subarach n oid h em or- conser vat ive t reat m en t . J Neurosu rg 1989;70(5):755–758
rhage. St roke 1994;25:1342–1347 33. Batjer HH, Reisch JS, Allen BC, Plaizier LJ, Su CJ. Failure of surger y to im -
14. Heiskan en O, Poran en A, Kuu rn e T, Valton en S, Kaste M. Acute surger y for prove ou tcom e in hyp er ten sive pu t am in al h em orrh age. A p rosp ect ive
int racerebral h aem atom as cau sed by rupt ure of an in t racran ial arterial ran dom ized t rial. Arch Neu rol 1990;47(10):1103–1106
an eur ysm . A prospect ive ran dom ized st udy. Act a Neuroch ir (Wien ) 1988; 34. Morgen stern LB, Fran kow ski RF, Sh edden P, Pasteur W, Grot t a C. Surgical
90:81–83 treat m en t for in tracerebral hem orrhage (STICH): a single-cen ter, ran dom -
15. Borden JA, Wu JK, Sh ucart WA. A proposed classificat ion for spin al an d ized clin ical t rial. Neu rology 1998;51(5):1359–1363
cranial dural arterioven ous fist ulous m alform at ions an d im plicat ions for 35. Ch eng X- C, Wu J-S, Zh ou X-P. Th e ran dom ized m ult icen t ric prospect ive
t reat m en t . J Neu rosu rg 1995;82:166–179 cont rolled t rial in th e st andardized t reat m en t of hypertensive in t racere-
16. Cogn ard C, Gobin YP, Pierot L, et al. Cerebral dural arterioven ous fist u las: bral h em atom as: th e com parison of surgical th erapeut ic outcom es w ith
clin ical an d angiograph ic correlat ion w ith a revised classificat ion of ve- conser vat ive th erapy. Ch in J Clin Neurosci 2001;9(4):365–368.
n ous drain age. Radiology 1995;194:671–680 36. Hossein i H, Leguerin el C, Hariz M, et al. Stereot act ic aspirat ion of deep
17. Djin djian R, Coph ign on J, Rey Th éron J, Merlan d JJ, Houdart R. Superselec- in t racerebral hem atom as un der com puted tom ograph ic con t rol: a m ult i-
t ive ar teriograph ic em bolizat ion by th e fem oral route in n euroradiology. cen t ric prospect ive ran dom ised t rial. 12th European St roke Con feren ce
St udy of 50 cases. 3. Em bolizat ion in cran iocerebral path ology. Neu ro- 2003, Valen cia, Spain:57.
radiology 1973;6:143–152 37. Hat tor i N, Kat ayam a Y, Maya Y, Gat h erer A. Im p act of stereot act ic h em a-
18. Stein er T, Vin cent C, Morris S, Davis S, Vallejo-Torres L, Ch risten sen MC. tom a evacu at ion on act ivit ies of daily living du r ing t h ech ron ic p er iod
Neurosurgical outcom es after in t racerebral h em orrh age: result s of th e follow ing sp on t an eou s p u t am in al h em or rh age: a ran d om ized st u dy. J
Factor Seven for Acu te Hem orrh agic St roke Trial (FAST). J St roke Cerebro- Neu rosu rg 2004;101(3):417–420
vasc Dis 2011;20:287–294 38. Mendelow Ad, Gregson BA, Fernandes HM. Early surger y versus initial con-
19. Men delow AD, Gregson BA, Fern an des HM, et al; STICH invest igators. ser vat ive t reat m en t in pat ien t s w ith sp on t an eou s su p raten torial in t race-
Early su rger y versu s in it ial con ser vat ive t reat m en t in p at ien t s w ith spon - rebral haem atom as in th e In tern at ion al Surgical Trial in In t racerebral
t an eou s su p raten tor ial in t racerebral h aem atom as in t h e In ter n at ion al Haem orrhage (STICH): a random ised trial. Lancet 2005;365(9457):387–397
Surgical Trial in In t racerebral Haem orrh age (STICH): a ran dom ised t rial. 39. Pan t azis G, Tsit sopoulos P, Mih as C, Kat siva Vst avrian os V, Zym aris S. Early
Lan cet 2005;365:387–397 surgical t reat m en t vs con ser vat ive m an agem ent for spon t an eous supra-
20. Men delow AD. STICH II Trial. h t t p://research n cl ac uk/st ich . 2012. Ac- ten torial in t racerebral h em atom as: a prospect ive ran dom ized st udy. Surg
cessed May 13, 2012 Neurol 2006;66(5):492–501.
21. Mould WA, Carh uapom a JR, Musch elli J, et al; MISTIE Invest igators. Mini- 40. Naff NJ, Han ley DF, Keyl PM, et al. In t raven t ricu lar th rom bolysis sp eeds
m ally invasive surger y plus recom binan t t issue-t ype plasm in ogen act iva- blood clot resolut ion : resu lt s of a pilot , prospect ive, ran dom ized, double-
tor for in t racerebral h em orrh age evacuat ion decreases perih em atom al blin d, con t rolled t rial. Neurosurger y 2004;54(3):577–583
edem a. St roke 2013;44:627–634 41. Vespa P, Mar t in NA, Han ley DF. MISTIE-ICES t rial. h t t p://brain injur yout-
22. Gregson BA, Broderick JP, Au er LM, et al. In dividual pat ien t dat a su bgroup com es com /st udies/m ist ie. 2012. Accessed May 14, 2012
m et a-an alysis of surger y for spon t an eous supraten torial in t racerebral 42. Mitch ell P, Gregson BA, Vin dlach eruvu RR, Men delow AD. Surgical op -
hem orrh age. St roke 2012;43:1496–1504 t ion s in ICH in cluding decom pressive cran iectom y. J Neurol Sci 2007;261:
23. Han ley DF. CLEAR-III in t raven t ricular th rom bolysis clin ical t rial. h t t p:// 89–98
braininjur youtcom es com /bios/clear-about. 2012. Accessed May 14, 2012 43. Math ew P, Teasdale G, Ban n an A, Oluoch - Olunya D. Neurosurgical m an -
24. Morgan stern LB, Dem ch u k AM, Kim DH, Fran kow ski RF, Grot t a JC. Re- agem en t of cerebellar haem atom a an d in farct . J Neu rol Neu rosu rg Psy-
bleeding lead s to poor ou tcom e in u lt ra-early cran iotom y for in t racere- ch iat r y 1995;59:287–292
bral h em orrh age. Neu rology 2001;56(10):1294–1299 44. Sam ii M, Egh bal R, Car valh o GA, Mat th ies C. Surgical m an agem en t of
25. Zuccarello M, Brot t T, Derex L, et al. Early surgical t reat m en t for supraten - brainstem cavern om as. J Neu rosu rg 2001;95:825–832
torial in t racerebral h em orrh age: a ran dom ized feasibilit y st udy. St roke
1999;30(9):1833–1839

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29 Medical and Endovascular Treatment of
Cerebral Sinus and Venous Thrombosis
Nohra Chalouhi, Stavropoula I. Tjoum akaris, L. Fernando Gonzalez,
Aaron S. Dum ont, Robert Rosenw asser, and Pascal M. Jabbour

Cerebral sin u s an d ven ou s th rom bosis (CSVT) is a rare bu t p oten - Th e t ran sverse sin u s begin s at t h e torcu lar h erop h ili an d
t ially fat al con d it ion w ith an in ciden ce of th ree cases p er m illion cou rses laterally bet w een t h e at t ach m en t s of t h e ten tor iu m
per year, an d it accou n ts for less th an 1% of all st rokes.1 In th e along a sm all groove in th e occipital bon e. At th e jun ct ion w ith
pediat ric p op u lat ion , th e in cid en ce is th ough t to be h igh er, w ith th e su p erior p et rosal sin u s, th e t ran sverse sin u s leaves it s ten to-
6.7 cases per m illion per year.2 CSVT is m ore com m on ly seen in rial at t ach m en t s to becom e th e sigm oid sin u s. Th e righ t t ran s-
you ng p at ien t s (average age 39 years) w ith a 3:1 fem ale to m ale verse sin u s is u sually dom in an t , receiving m ost of th e drain age
predom in an ce.3 Given th e diversit y of clin ical an d radiological from th e su perior sagit t al sin u s (i.e., th e su p erficial p ar t s of th e
fin dings in CSVT, th e diagn osis is u su ally delayed for alm ost a brain ), w h ereas th e sm aller left t ran sverse sin us receives pri-
w eek after th e on set of sym ptom s.3 An t icoagulat ion is th e m ain - m arily th e drain age of th e st raigh t sin us (i.e., th e deep parts of
st ay of t reat m en t for CSVT. In severe an d refractor y cases, en do- th e brain ). Th is pat tern of drain age accou n t s for th e differen ce in
vascu lar ch em ical an d m ech an ical th rom bolysis can be un der- presen tat ion of a left an d a righ t t ran sverse sin u s th rom bosis. Up
taken to recan alize th e affected sin uses. to 45% of pat ien t s w ith CSVT h ave th rom bosis of th e t ran sverse
sin u s.3 Th e sigm oid sin us drain s from th e t ran sverse sin us an d
receives th e in ferior p et rosal sin u s ju st after crossing th e occipi-
tom astoid sut ure to form th e in tern al jugu lar vein . Th e in tern al
■ Relevant Anatomy jugular vein is involved in alm ost 12% of all cases of CSVT.3
Th e cavern ou s sin u s is a m ajor m u lt icom part m en t al ven ou s
Kn ow ledge of th e cerebral ven ou s system is of u t m ost im por-
sin u s located bilaterally on th e greater w ing of th e sp h en oid. It
tan ce for th e en dovascular an d n eurovascular surgeon . Th e cere-
con n ect s t h e in t racran ial w ith th e ext racran ial circu lat ion via
bral ven ous system displays a rath er con stan t an atom ic pat tern
th e in ferior an d su p erior op h th alm ic vein s. Th e cavern ou s sin u s
albeit w ith som e variat ion s in size, locat ion , an d con n ect ion s of
com m u n icates also w ith th e basilar sin us, th e in ferior an d su pe-
sm all vein s. Th e p aten cy of cerebral vein s an d sin u ses is essen t ial
rior pet rosal sin u s, th e sp h en op ariet al sin u s, th e pter ygoid ve-
for the adequ ate outflow of th e cerebral circulation . Despite som e
n ous plexus of th e pter ygopalat in e fossa, an d th e con t ralateral
an astom ot ic n et w orks, occlusion of m ajor cerebral vein s can lead
cavernous sin us via intercavernous sinuses. Each cavernous sinus
to disast rou s con sequen ces w ith congest ion , h em orrh age, u n cal
con t ain s th e in tern al carot id ar ter y an d cran ial n er ves (CNs) III,
h ern iat ion , an d possibly death .
IV, V1, V2, an d VI. Th rom bosis of th e cavern ous sin us is seen in
Th e dural sin uses are endothelial-lin ed ven ous chann els foun d
on ly 1.3% of all cases of CSVT.3
bet ween the layers of the dura m ater and form the term inal part of
Apar t from sm all vein s drain ing th e fron t al, parietal, tem po-
th e cerebral ven ou s system , u lt im ately drain ing in to th e in tern al
ral, an d occipit al lobes, th e cor t ical ven ou s system also in clu des
jugular vein . Th e m ajor ven ous sin uses are th e superior sagit t al,
th e an astom ot ic vein of Trolard th at cou rses from th e fron t al an d
in fer ior sagit t al, st raigh t , t ran sverse, su p er ior p et rosal, sigm oid,
parietal cor tex in to th e su perior sagit tal sin u s, as w ell as th e vein
in fer ior pet rosal, caver n ou s, ten tor ial, occip it al, sp h en op ariet al,
of Labbé from th e tem poral lobe to th e sigm oid sin us. Th rom bo-
an d sph en obasal sin uses.4
sis of th e vein of Labbé can lead to aph asia an d h em ip aresis, as
Th e su p erior sagit t al sin u s cou rses from above th e foram en
t h is vein is th e m ajor ou t flow of t h e tem p oral lobe. Ap p roxi-
cecu m an teriorly to th e torcu lar h erop h ili p osteriorly, receiving
m ately 17% of p at ien t s w it h CSVT h ave th rom bosis of cor t ical
m ajor ou tflow from th e supraten torial cortex (fron t al, parietal,
vein s.3
and occipital lobes) via cortical bridging veins. It is the m ost com -
m on ly involved sin u s in CSVT (62% of cases).3
Th e st raigh t sin u s origin ates beh in d th e corpu s callosu m , at
t h e u n ion of t h e vein of Galen an d t h e in fer ior sagit t al sin u s,
an d cou rses posteriorly in th e ju n ct ion of th e falx an d ten torium ,
■ Pathophysiology and Risk Factors
drain ing in to th e t ran sverse sin u s. Th e vein of Galen itself origi- Virch ow ’s t r iad of hyp ercoagu labilit y, st asis, an d en d ot h elial
n ates from t h e in ter n al cerebral vein s an d t h e basal vein of inju r y u n d erlies CSVT. In a hyp ercoagu lable st ate, en d ot h elial
Rosen th al. Most of th e blood in th e deep cerebral vein s collect s injur y resu lt s in act ivat ion of th e coagulat ion cascade w ith resul-
in to th e vein of Galen . Th ese vein s drain th e lateral an d th ird tan t th rom bus form at ion . Occlu sion of cerebral vein s in creases
vent ricles, th e basal ganglia, th e in tern al capsule, th e th alam us, th e ven ou s p ressu re an d leads to pooling of blood in th e ven ou s
t h e hyp ot h alam u s, t h e m id brain , an d th e p in eal region . Th e com partm ent w ith disruption of the blood–brain barrier and sub-
st raigh t sin u s an d t h e deep ven ou s system are involved in 18% sequ en t vasogen ic ed em a.5 Th e drop in region al blood flow also
an d 10.9% of all cases of CSVT, resp ect ively.3 results in alteration of Na +/K+–adenosine triphosphatase (ATPase)

369

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370 III Ischemic Stroke and Vascular Insufficiency

pu m p fu n ct ion an d cytotoxic edem a.6 Th ese factors along w ith n eu rologic deficits, an d pose a sign ifican t diagn ost ic ch allenge.
the im pairm ent of cerebrospinal fluid absorption in to the ven ous You ng age an d th e presen ce of p redisp osing factors (oral con t ra-
system th rough p acch ion ian gran u lat ion s cu lm in ate in in t racra- cept ives use am ong oth ers) are im por t an t clues to th e diagn osis
n ial hyper ten sion . in such cases. Focal n eu rologic deficit s from ven ous in farct ion or
Com m on predisposing factors in clu de in h erited an d acquired h em orrh age are also com m on an d occur in m ore th an 70%of pa-
t h rom bop h ilia, p regn an cy an d p u er p er iu m , in fect ion s, d r ugs, t ien ts.3 Motor deficit s (h em iparesis, m on oparesis, an d parapare-
su rger y, an d t rau m a.7 Resu lt s from th e In ter n at ion al St u dy on sis) are m ost com m on ly seen , w ith aph asia an d sen sor y d eficit s
Cerebral Vein an d Du ral Sin u s Th rom bosis (ISCVT), a large pro- occu rring less frequ en tly. Aph asia occu rs in 19%of pat ien t s, t ypi-
spect ive m ulticen ter series of 624 pat ien ts w ith CSVT, sh ow ed cally w ith left transverse sinus th rom bosis. Bicortical injur y from
th at u p to 44% of pat ien t s h ave m ore th an on e predisposing fac- su p erior sagit tal sin u s th rom bosis resu lt ing in bilateral deficits
tor.3 It is th erefore im p or t an t to search for risk factors, th rom - (paraparesis) is a rare bu t ch aracterist ic feat u re of CSVT.
bophilia in par t icu lar, even w h en an apparen t cause is presen t . Seizures occu r in u p to 40% of CSVT pat ien t s, w h ich h elps to
Heller et al8 st ressed th e m ult ifactorial n at ure of th e disease in dist inguish CSVT from ar terial st rokes w h ere th e in ciden ce of
th e pediat ric p op u lat ion sh ow ing th at , in th e m ajorit y of cases, seizu res is as low as 5%.20 Seizures are t ypically focal an d lim ited,
CSVT resu lt s from th e com bin at ion of proth rom bot ic risk factors bu t gen eralizat ion an d stat u s epilept icus are relat ively com m on .
an d an u n derlying clin ical con dit ion . In cavern ou s sin us th rom bosis, orbit al congest ive sym ptom s,
Th e p revalen ce of p roth rom bot ic con dit ion s in p at ien t s w ith n am ely proptosis, ch em osis, diplopia, an d orbital pain , are at th e
CSVT ranges from 21 to 34%.3,9 Th rom boph ilic factors th at w ere forefron t of th e clin ical pict u re. In superior sagit tal sin us th rom -
sh ow n to be associated w it h CSVT in clu d e deficien cies in p ro- bosis, seizures an d bilateral deficits are t ypically seen . In t ran s-
tein C, protein S, an d an t ith rom bin III,10 as w ell as factor V Leiden verse sin us th rom bosis, sign s of ear or m astoid in fect ion can be
gen e m utat ion ,11 an t ip h osp h olip id an d an t icard iolip in an t ibod- presen t alongside in t racran ial hyper ten sion an d aph asia (for left
ies,10 an d proth rom bin G20210A m ut at ion .12 St u dies h ave also t ran sverse sin u s t h rom bosis). W h en t h e d eep ven ou s system
dem on st rated a st rong associat ion of CSVT w ith hyperh om ocys- (st raigh t sin us an d its bran ch es) is occluded, bilateral th alam ic
tein em ia.13,14 In a large case-con t rol st u dy, h igh plasm a levels of an d basal ganglia injur y can en su e, causing bilateral m otor defi-
h om ocystein e w ere foun d in 27%(33/121) of pat ien t s w ith CSVT cits, beh avioral sym ptom s, m en tal stat u s ch ange, an d com a. Cor-
versus 8%(20/242) of control subjects, w ith an odds ratio of 4.2.14 t ical vein occlu sion frequ en t ly lead s to seizu res an d m otor or
Pregn an t w om en h ave a h igh er risk of develop ing ven ou s sen sor y deficits.
th rom bosis in clu ding CSVT.15 Th e risk is h igh est in th e th ird t ri-
m ester an d th e puerperium .16 Oral con t racept ive use is a st rong
risk factor for CSVT w ith a relat ive risk as h igh as 15.9 according
to a m eta-an alysis of 16 st udies.17 In fact , n early all fem ale pa- ■ Perioperative Evaluation
t ien ts w ith CSVT (u p to 96%) are oral con t racept ive u sers.
Cerebral sin u s an d ven ou s th rom bosis sh ou ld be con sidered in
Abou t 12% of all cases of CSVT are at t r ibu t able to in fect ion s
you ng p at ien t s w ith ou t cardiovascu lar risk factors w h o p resen t
of th e cen t ral n er vou s system or th e ear, sin u s, m ou th , face, an d
w ith n ew -on set h eadach es or st roke-like sym ptom s. Predispos-
n eck.3 Head an d n eck in fect ion s are par t icularly com m on in th e
ing factors su ch as pregn an cy, puerperiu m , oral con t racept ives,
pediatric pop u lat ion an d accou n t for alm ost 40% of all cases.18
an d fam ily h istor y of th rom boph ilia am ong oth ers sh ou ld raise
Less com m on factors associated w ith CSVT in clude can cer, h e-
th e su sp icion for CSVT. Given th e lack of specificit y of clin ical
m atologic d isord ers an d iron d eficien cy an em ia, vascu lit is an d
sign s an d sym ptom s, im aging st u d ies are alw ays n ecessar y to
ot h er in flam m ator y system ic d isord ers, h ead t rau m a, lu m bar
est ablish th e diagn osis. A com p u ted tom ograp hy (CT) scan of th e
p u n ct u re, brain t u m ors, ar ter ioven ou s m alfor m at ion s, t hyroid
h ead is usually th e in it ial im aging test in th e evaluat ion of pa-
disease, su rger y, an d dehydrat ion .19 In a su bstan t ial n u m ber of
t ien ts p resen t ing w ith n ew n eu rologic sym ptom s (Fig. 29.1). CT
p at ien t s, n o u n d erlying con d it ion can be id en t ified (12.5% of
w ith out con t rast is rarely h elpful, w ith n orm al results in 70% of
p at ien t s en rolled in th e ISCVT st u dy).3
pat ien ts.21 A hyperden sit y filling th e affected sin us or vein is th e
classic CT fin d ing in CSVT. CT can also sh ow th e “den se t riangle”
sign (a hyp erd en sit y in t h e p oster ior p or t ion of t h e su p er ior
sagit t al sin us) or th e cord sign (hyperden se th rom bosed cort ical
■ Clinical Presentation vein s). After con t rast inject ion , CT dem on st rates a filling defect
Th e diagn osis of CSVT is h in dered by th e h igh variabilit y an d lack w ith in th e vein or th e sin u s; th e lack of filling of th e torcular is
of specificit y of th e clin ical presen tat ion . Com m on sign s an d kn ow n as th e “em pt y delta” sign . Fin ally, CT m ay sh ow th e pres-
sym ptom s in clu de h eadach es, focal n eu rologic deficit s, seizu res, en ce of cerebral edem a, ven ou s in farct s, or h em orrh age. High ly
papilledem a, an d altered consciousness. Headache, the m ost com - suggest ive of CSVT are in farcts th at are m u lt ip le, h em orrh agic,
m on sym ptom , is presen t in n early 90% of pat ien ts an d reflects n ot con fin ed to ar terial vascular territories, or in close proxim it y
m ain ly th e in crease in in t racran ial p ressu re. Headach e is u su ally to a ven ous sin u s.
diffu se an d in creases gradu ally over several days, bu t th u n der- Magn et ic reson an ce im aging (MRI) cou pled w ith m agn et ic
clap an d m igrain e-like h eadach e h ave also been described. Pap - reson an ce ven ography (MRV) is par t icu larly sen sit ive in detect-
illedem a is com m on in slow ly developing CSVT but can be absent ing CSVT an d is con sidered th e p referred im aging m odalit y in
in acu te cases. In pat ien t s w ith h eadach e an d p apilledem a or th is set t ing. Th e m ost t yp ical fin ding on MRI is th e visu alizat ion
diplop ia (CN VI p alsy), CSVT sh ou ld alw ays be con sidered . Som e of hyp er in ten se vein s or sin u ses. In it ially, t h rom bosed sin u ses
pat ien ts, esp ecially th ose w ith t ran sverse sin u s th rom bosis, can appear isoin ten se on T1-w eigh ted im ages an d hypoin ten se on
presen t w ith isolated h eadach e in th e absen ce of papilledem a or T2-w eigh ted im ages.22 After 5 days, T1- an d T2-w eigh ted im ages

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29 Medical and Endovascular Treatm ent of Cerebral Sinus and Venous Throm bosis 371

Fig. 29.2 An anteroposterior venous-phase angiogram with superselec-


tive injection showing clots in the superior sagit tal, transverse, and sigm oid
sinuses prethrom bolysis.

Fig. 29.1 A head computed tomography (CT) scan showing the hyper- u n dertaken in all pat ien t s w ith con firm ed CSVT.19 Measu rem en t
dense clot in the superior sagit tal and transverse sinuses (arrows). of D-dim er levels can h elp rule out CVST albeit w ith cer tain lim -
it s. Th e test h as a sen sit ivit y of 97.1%, a specificit y of 91.2%, a
n egat ive p red ict ive valu e as h igh as 99.6%, an d a p osit ive p red ic-
sh ow a hyp erin ten se sign al in th e affected sin u s. An abn orm al
t ive valu e of 55.7%.24 It sh ou ld be kept in m in d, h ow ever, th at
sign al in a sin u s on MRI in com bin at ion w ith th e absen ce of flow
th e rate of false n egat ives is h igh er in pat ien t s w ith ch ron ic
on MRV pract ically con firm s th e diagn osis of CSVT. MRV alon e,
sym ptom s an d th ose w ith isolated h eadach es or lim ited sin u s
h ow ever, can n ot reliably differen t iate bet w een sin us th rom bosis
th rom bosis, w h ich lim it s th e reliabilit y of th e test in su ch cases.
an d sin us hypoplasia (left t ran sverse sin u s), an d correlat ion w ith
Addit ion ally, in pat ien t s w ith a h igh clin ical su spicion of CSVT,
MRI is th erefore alw ays n ecessar y. Gradien t ech o T2-w eigh ted
a n egat ive test sh ou ld n ot p reclu d e im aging evalu at ion . Cere-
im ages com bin ed w it h MRI can h ave an ad d it ion al d iagn ost ic
brospin al flu id (CSF) exam in at ion is w arran ted on ly w h en CSVT
valu e esp ecially in th e acu te st age of t h rom bosis or in isolated
is susp ected to be caused by an in fect ion . Th ere m ay be a h igh
cor t ical ven ou s in farct s.19 Th rom bosed sin u ses u su ally ap p ear
open ing pressure w ith elevated protein s an d cell coun t but CSF
hypoin ten se on gradien t-ech o T2-w eigh ted MRI. CT ven ography
fin dings gen erally lack sp ecificit y.
(CTV) h as sim ilar sen sit ivit y an d specificit y com pared w ith MRV
in d etect ing CSVT.23 Iodin e con t rast allergy an d toxicit y, radia-
t ion exp osu re, an d bon e ar t ifacts in terfering w ith th e visu aliza-
t ion of en h an ced sin u ses are p oten t ial d raw backs of th e tech -
n ique. As a gen eral r ule, MRV or CTV sh ould alw ays be perform ed
■ Discussion of Various
to con firm th e diagnosis an d determ in e th e exten t of CSVT, an d Treatment Modalities
sh ou ld be repeated in pat ien ts w ith persisten t or evolving sym p - In 2011, the Am erican Heart Associat ion and the Am erican Stroke
tom s suggest ive of th rom bu s p ropagat ion . Associat ion p u blish ed evid en ce-based gu idelin es for th e m an -
Given t h e h igh sen sit ivit y an d specificit y of n on invasive im - agem en t of CSVT.19 Several em in en t organ izat ion s in clu ding th e
aging m odalit ies, n am ely MRV an d CTV, cerebral angiography is Am erican Associat ion of Neu rological Su rgeon s an d th e Congress
rarely requ ired to est ablish th e diagn osis (Fig. 29.2). It is per- of Neurological Surgeon s h ave en dorsed th eir recom m en dat ion s.
for m ed w h en MRV an d CTV are in con clu sive or u n available, or
in th e set t ing of an en dovascular procedure. Typical fin dings in -
clu de a filling defect in th e th rom bosed sin u s or vein , ven ou s Medical Treatment
congest ion , reversal of ven ou s flow, an d d elay in visualizat ion of
Anticoagulant Therapy
th e ven ous circulat ion .
Aside from rou t in e blood st u dies, a th orough screen ing for System ic an t icoagu lat ion w it h h ep arin is t h e m ain st ay of t reat -
t h rom bop h ilia (p rotein C, p rotein S, an t it h rom bin d eficien cy, m en t for CSVT. An t icoagu lat ion t h erapy aim s to ach ieve recan -
an t iph osph olipid syn drom e, proth rom bin G20210A m ut at ion , alizat ion of t h e occlu d ed sin u s, avoid t h rom bu s exten sion , an d
an d factor V Leiden) an d proth rom bot ic con dit ion s sh ou ld be p reven t p u lm on ar y em bolism . Regard less of t h e p resen ce of

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372 III Ischemic Stroke and Vascular Insufficiency

in t racran ial h em or rh age (ICH), p at ien t s w ith CSVT sh ou ld be risk of occu rren ce of seizu res is ver y low an d prophylact ic t h er-
an t icoagu lated w it h body w eigh t–adju sted su bcu t an eou s low - apy is th erefore n ot w arran ted.19
m olecular-w eigh t h eparin (LMW H) or w ith dose-adjusted u n -
fract ion ated h ep arin (UH) w ith a t arget act ivated p ar t ial th rom -
Antibiotics, Aspirin, and Steroids
boplast in t im e of t w o to th ree t im es th e baselin e.19 Th e safet y
an d efficacy of an t icoagu lan t th erapy h ave been rep or ted in W hen a bacterial infect ion is suspected as the cause of CSVT, anti-
t w o sm all t rials an d several obser vat ion al st udies.25,26 A m eta- biotics should be adm inistered and purulent collections drained
an alysis of th e t w o t rials (involving 79 pat ien t s) th at com pared as appropriate. Th ere is n o role for aspirin th erapy in th e m an -
an t icoagulan t th erapy w ith placebo sh ow ed th at an t icoagulat ion agem en t of CSVT. Th e u se of steroids in th e acu te ph ase of CSVT
led to a 13%absolu te risk redu ct ion in death or dep en den cy w ith is n ot h elpfu l an d could even be det rim en t al. Th e ISCVT invest i-
a relat ive risk reduct ion of 54%(but fell sh or t of stat ist ical sign ifi- gators com pared clin ical ou tcom es in pat ien t s w ith CSVT based
can ce).25 In addit ion , n o n ew sym ptom at ic ICHs w ere n oted de- on w h eth er th ey w ere t reated w ith steroids or n ot , an d foun d n o
spite an t icoagulat ion , w h ich suggests th at an t icoagulan t th erapy ben efit w ith th e u se of steroids. Moreover, pat ien t s w ith out pa-
does n ot in crease th e risk of ICH. Th e rate of ICH after in it iat ion ren chym al lesion s t reated w ith steroids h ad a w orse progn osis
of h ep arin in CSVT ranges from 0 to 5.4%.19 th an th ose t reated w ith ou t steroids (OR, 4.2; p = 0.008).32
It appears th at LMW H h as a bet ter safet y-efficacy profile
com pared w ith UH. Th e ISCVT invest igators h ave recen tly com -
Treatment of Intracranial Hypertension
pared clin ical ou tcom es in 119 pat ien ts t reated w ith LMW H an d
302 pat ien ts t reated w ith UH.27 Th e odds of being fu n ct ion ally In t racran ial hyper ten sion is com m on in pat ien t s w ith CSVT an d
in depen den t after 6 m on th s w ere m ore th an t w ice as h igh w ith cau ses h eadach es, p ap illedem a, an d CN III an d VI palsies. Pa-
LMW H as com pared w ith UH (odds rat io [OR], 2.4; 95% con fi- t ien ts w ith in t racran ial hyp er ten sion sh ou ld be star ted on acet-
den ce in ter val [CI], 1.0–5.7). Th ese fin dings are in lin e w ith th e azolam ide an d closely m on itored for progressive visu al loss. In
resu lt s of th e m et a-an alysis by van Dongen et al28 th at in cluded pat ien ts w ith th reaten ed vision , a lu m bar p u n ct u re w ith su ffi-
22 st udies an d 8,867 pat ien t s w ith ven ous th rom boem bolism cien t fluid rem oval to ach ieve a n orm al closing pressure sh ou ld
an d sh ow ed bet ter efficacy of LMW H com pared w ith UH w ith a be perform ed. This requires, how ever, tem porar y cessation of an-
sign ifican t redu ct ion in m ajor h em orrh age an d overall m or talit y ticoagu lat ion w ith th e associated risk of th rom bu s p rop agat ion .
rates. Opt ic n er ve d ecom p ression s an d sh u n t s sh ou ld be con sid ered
Th ere is a lack of con t rolled dat a p er t ain ing to th e opt im al if vision con t in ues to deteriorate despite acetazolam ide an d re-
du rat ion of oral an t icoagu lat ion follow ing CSVT. Th e goal of oral peated lu m bar pun ct ures.
an t icoagulan t th erapy is to preven t th e recurren ce of CSVT as
w ell as ot h er ext racerebral ven ou s t h rom bosis even t s. In t h e
Endovascular Treatment
ISCVT, t h e rate of recu r ren ce of CSVT w as 2.2% (14 of 624 p a-
t ien ts) an d th e rate of oth er th rom bot ic even t s (lim b or p elvic Th e several lim it at ion s of system ic an t icoagu lat ion in CSVT h ave
ven ou s th rom bosis, pulm on ar y em bolism , st roke, tran sien t isch - sparked in creased in terest in in ter ven t ion al t reat m en t . Abou t
em ic at t ack, acu te lim b isch em ia) w as 3% (19 of 624 pat ien t s).3 15%of patients w ith CSVT have poor outcom es despite anticoagu -
Abou t 40% of th ese p at ien t s w ere on an t icoagu lan t s at th e t im e lat ion an d opt im al m edical th erapy.3 System ic an t icoagulat ion
of th e th rom bot ic even t . Th e overall recurren ce rate for th rom - alon e can rarely dissolve exten sive or propagat ing th rom bi, an d
bot ic even ts w as 4.1 per 100 person -years. In an oth er large st udy m any pat ien ts m ay h ave in t ract able in t racran ial hyperten sion
th at involved 145 p at ien t s w ith CSVT, th e rate of recu rren ce of an d con t in u e to deteriorate du ring h eparin th erapy. Recan aliza-
cerebral an d ext racerebral ven ous th rom bosis after discon t in ua- t ion rates w ith an t icoagu lan t th erapy alon e m ay n ot be opt im al,
t ion of an t icoagulan ts w ere 3% an d 7%, respect ively, for a recur- w ith u p to 30%of pat ien ts sh ow ing n o recan alizat ion on im aging
ren ce rate of 2.03 p er 100 person -years for all ven ou s th rom bot ic follow -up.33 Ch em ical th rom bolysis an d m ech an ical th rom bec-
even ts.29 Male sex an d severe th rom boph ilia w ere iden t ified as tom y h ave show n ver y prom ising results an d h ave been in creas-
risk factors for recu rren t ven ou s th rom bosis. In an alogy to pa- ingly u sed in th e m an agem en t of CSVT. Th ese procedures en able
t ien ts w ith ext racerebral ven ou s th rom bosis, con t in u ing vit am in faster an d bet ter recan alizat ion of occluded sin uses w ith som e-
K an tagon ists is recom m en ded for 3 to 6 m on th s in pat ien ts w ith t im es dram at ic clin ical im p rovem en t of in t racran ial hyp er ten -
a t ran sien t risk factor, for 6 to 12 m on th s in pat ien ts w ith idio- sion an d n eurologic deficits an d can be lifesaving in crit ically ill
path ic CSVT, an d in defin itely in th ose w ith severe th rom bop h ilia pat ien ts.34 How ever, dat a from ran dom ized con t rolled t rials are
or recu rren t ven ous th rom bosis (target in tern at ion al n orm alized lacking, an d exp erien ce h as been largely lim ited to cases rep or ts
rat io [INR] of 2 to 3).19 an d sm all case series.35–37 En dovascu lar t reat m en t , th erefore, is
reser ved for cr it ically ill pat ien t s w h o con t in u e to d eter iorate
d espite adequate an t icoagulat ion .19
Treatment of Seizures
Ch em ical th rom bolysis can be perform ed w ith local inject ion
Seizu res are ver y com m on in p at ien t s w ith CSVT, occu rring in of u rokin ase or t issu e-t yp e p lasm in ogen act ivator (t -PA) (Fig.
40% of cases. Focal m otor/sen sor y deficits, cort ical vein th rom - 29.3). t-PA is preferred because of its clot specificit y an d its ca-
bosis, ICH, in farcts, an d focal edem a h ave been cited as possible pacit y to restore flow m ore qu ickly th an u rokin ase, w h ich is n o
predictors of early seizu re.30,31 In it iat ing early an t iepilept ic drugs longer com m ercially available. Regardless of th e agen t , ch em ical
is recom m en ded in pat ien ts w ith CSVT an d a single seizu re to th rom bolysis h as sh ow n good resu lt s in th e t reat m en t of CSVT.
preven t seizu re recu rren ce, regardless of th e p resen ce of p aren - Frey et al36 p erform ed ch em ical t h rom bolysis in com bin at ion
chym al lesion s.19 In pat ien t s w ith ou t seizu res on adm ission , th e w ith in t raven ou s h eparin in 12 pat ien t s w ith CSVT an d clin ically

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29 Medical and Endovascular Treatm ent of Cerebral Sinus and Venous Throm bosis 373

Based on th eir exp erien ce, th e auth ors recom m en ded system ic
an t icoagulat ion th erapy alon e or in conju n ct ion w ith m ech an i-
cal th rom bectom y for t reat ing pat ien t s w ith CSVT. A variet y of
devices h ave been u t ilized in CSVT in clu ding coron ar y angio-
plast y balloon s, th e AngioJet device (Medrad In c., Warren dale,
PA), th e Merci device (Con cen t ric Medical, Moun tain View, CA),
and recently the Penum bra System (Penum bra Inc., Alam eda, CA).
Regardless of th e t yp e of th e device, m ech an ical th rom bectom y
can be com plicated by ven ou s perforat ion w ith subsequen t su b -
dural hem atom a, pulm onar y em bolism , and theoretically arterial
isch em ic st rokes in th e p resen ce of a p aten t foram en ovale.
Coron ar y angiop last y balloon s or com plian t balloon s (Hyper-
For m , Hyp erGlid e, ev3 En d ovascu lar, Plym ou t h , MN) can be
used to perform partial th rom bectom y before th rom bolysis, th us
m in im izing th e dose of lyt ics an d th e occu rren ce of h em orrh agic
com p licat ion s.42 Th e d ifficu lt y in n avigat in g coron ar y an gio -
p last y balloon s in t h e cerebral ven ou s system an d t h e r isk of
sin u s ru pt u re or dissect ion w ith balloon angiop last y are p oten -
t ial draw backs of th e tech n iqu e.
Several case series h ave been rep or ted on th e safet y an d effi-
cacy of t h e AngioJet rh eolyt ic device, a periph eral vascu lar an d
coron ar y th rom bectom y device, in CSVT.40,43 AngioJet u ses h igh -
speed backw ard salin e jets to create a n egat ive pressure zon e,
Fig. 29.3 A lateral venous-phase angiogram with superselective injection cau sing a p ow erfu l vacu u m effect th at draw s th e th rom bu s in to
through the m icrocatheter in the superior sagit tal sinus post–tissue-t ype t h e cat h eter w h ere it is fragm en ted an d rem oved from t h e
plasm inogen activator (t-PA) injection over 24 hours.
body. In a recen t review of all cases of CSVT t reated w ith rh eo-
lyt ic th rom bolysis (32 pat ien t s overall), u p to 82% of p at ien t s
w ere fou n d to h ave a good ou tcom e an d on ly 12% exp er ien ced
disabling, n on resolving, or w orsen ing sym ptom s. Th ey ach ieved p roced u re-related com p licat ion s, n am ely fem oral ar ter y p seu -
com plete recanalization in six patients and partial recanalization doan eur ysm , posterior fossa h em atom a, an d an em ia.40 Recen tly,
in th ree p at ien t s, w ith a m ean t-PA dose of 46 m g at a m ean t im e Dashti et al43 reported on a series of 13 pat ients w ith CSVT under-
of 29 h ours. Clin ical im provem en t w as n oted in all n in e pat ien ts. going th rom bectom y w ith AngioJet as a first-lin e t reat m en t in
Tw o ot h er p at ien t s exp er ien ced h em orrh agic w orsen ing t h at com bin at ion w ith system ic an t icoagu lat ion . All occlu ded sin u ses
requ ired h em atom a evacuat ion in on e case. In an oth er st u dy on w ere su ccessfu lly recan alized an d rem ain ed so on follow -u p
ch em ical th rom bolysis in CSVT, Kim an d Su h 38 t reated n in e pa- im aging. Th e on ly p rocedu ral com p licat ion obser ved w as th e
t ien ts w ith direct t-PA inject ion , ach ieving su ccessfu l recan aliza- asym ptom at ic perforat ion of a cerebellar vein . Of n in e p at ien t s
t ion (at a m ean t im e of 20 h ou rs) an d im p rovem en t of sym ptom s w ith available follow -up, seven h ad excellen t clin ical outcom e
in all pat ien t s. No w orsen ing or n ew ICH w as noted in th eir se- an d t w o died. Th e au th ors con cluded th at m ech an ical th rom bec-
ries. A system at ic review th at in clu ded 169 pat ien t s t reated w ith tom y is feasible as a first-lin e t reat m en t for CSVT an d leads to
local th rom bolysis suggested a possible ben efit for th rom bolysis rap id sym ptom at ic an d n eu rologic rest it u t ion . How ever, h igh -
in severe cases of CSVT su ch as th ose w h o presen t in a com atose qu alit y eviden ce from ran dom ized con t rolled t rials is clearly
st ate or w ith th rom bosis of th e deep ven ou s system .39 Th e au - n eeded to suppor t th e rout in e use of th is tech n ique as a first-lin e
th ors also fou n d th at in t racran ial h em orrh ages occu rred in 17% t reat m en t for all p at ien ts w ith CSVT. Th e size an d rigidit y of th e
of cases causing clin ical deteriorat ion in 5%, w h ereas ext racra- AngioJet catheter, w h ich m akes it difficult to n avigate th rough
n ial h em orrh ages w ere seen in 21% of cases an d required blood th e in t racran ial circu lat ion , along w ith th e poten t ial for flu id
t ran sfu sion in 2%. Overall, despite th e risk of h em orrh agic com - overload are lim itat ion s of th e tech n ique.
plicat ion s, ch em ical th rom bolysis seem s to be effect ive an d rela- Th e Merci d evice h as been su ccessfu lly u sed in a case of
t ively safe in CSVT an d represen ts a viable opt ion in critically ill CSVT.44 W h en d ep loyed , t h is d evice ret u r n s to it s p refor m ed
or d eteriorat ing pat ien ts. coiled sh ap e to en sn are t h e t h rom bu s. It is t yp ically u sed to
Mech anical throm bectom y, w ith or w ithout concurrent chem - m ech an ically disru pt th e clot an d ach ieve p ar t ial recan alizat ion
ical t h rom bolysis, h as been recen t ly u t ilized in t h e t reat m en t of th e sin us, w h ich reduces th e dose of lyt ics delivered in to th e
of CSVT.37,40 Mech an ical th rom bectom y offers th e possibilit y of sin u s. Th e device h as su perior n avigabilit y com pared w ith th e
qu ickly recan alizing th e th rom bosed sin u s w ith ou t th e n ecessit y AngioJet bu t carries th e risk of dam age to th e en doth eliu m an d
for t-PA inject ion , w h ich is par t icularly problem at ic in pat ien ts t rabeculae of th e du ral sin us.
w ith preexist ing ICH. In fact , th e rate of h em orrh agic com plica- Th e Pen u m bra System is a n ew em bolectom y device specifi-
t ion s seem s to be low er w ith m ech an ical devices com pared w ith cally design ed to rem ove large th rom boem boli, w h ich m akes it
lyt ics. Soleau et al41 repor ted th eir experien ce in 31 pat ien ts par t icu larly su it able for CSVT. Th e device u ses a com bin at ion of
t reated for CSVT w ith differen t m odalit ies an d fou n d th at h em - clot separat ion (t h rough a sep arator) an d aspirat ion (t h rough an
orrh agic com plicat ions occurred in 37.5%of th e ch em ical th rom - aspirat ion source) to rem ove th e th rom bus. Th e Pen um bra Sys-
bolysis group versus 25%of the m echanical throm bectom y group. tem looks prom ising for th e t reat m en t of CSVT but experien ce

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374 III Ischemic Stroke and Vascular Insufficiency

h as been lim ited to case repor ts an d on e sm all case series.37,45 in gton , IN) is in t rod u ced in to t h e cerebral ven ou s system an d
Ch ou lakian an d Alexan der 37 su ccessfu lly t reated fou r p at ien t s placed as d ist ally as possible in th e affected sin u s. A 4F or 5F
w ith CSVT using the Penum bra System w ithout concurrent chem - AngioJet cath eter is th en in t roduced over a m icroguidew ire an d
ical th rom bolysis. Th ey ach ieved recan alizat ion an d n eu rologic delivered in to th e occlu ded sin u s w ith th e su pp or t of th e KSAW
im p rovem en t in all fou r p at ien t s an d rep or ted n o p roced u ral sheath. Th e AngioJet device is act ivated to init iate rheolyt ic throm -
com plicat ion s or n ew /w orsen ing ICH. bectom y and slow ly w ithdraw n through the throm bosed sinus.
Ran dom ized con t rolled t rials are n eeded to bet ter defin e th e Th e Pen u m bra an d Merci d evices are design ed specifically for
role of ch em ical an d m ech anical t h rom bolysis in CSVT. Mean - th e cerebral vascu lat u re an d can be easily n avigated th rough th e
w h ile t h ese tech n iqu es sh ou ld be u sed cau t iou sly in a select cerebral ven ous sin uses. Th rom bectom y w ith th ese devices is
n um ber of cases. follow ed, if n ecessar y, by balloon angioplast y.

Surgical Treatment
Surgical treatm ent has a lim ited role in th e m an agem ent of CSVT. ■ Patient Outcomes
Decom pressive cran iectom y m ay be con sidered in pat ien t s w ith
ICH an d im pen ding un cal h ern iat ion or th ose w ith large ven ou s In con t rast to ar terial st roke, CSVT carries a favorable ou tcom e in
in farcts causing refractor y in t racran ial hyp erten sion .19 gen eral, w ith up to 80% of pat ien t s experien cing a com plete re-
cover y at follow -u p.3 In a system at ic review, th e rates of d eath
an d depen den cy w ere foun d to be as low as 9.4% an d 9.7%, re-
sp ect ively.3 According to th e ISCVT, th e predictors of poor long-
■ Endovascular Technique term outcom e are age > 37 years, m ale sex, com a, m en t al st at us
d isord er, ICH on ad m ission CT scan , t h rom bosis of t h e deep
En dovascu lar p roced u res are p erform ed u n d er gen eral an esth e- ven ou s system , cen t ral n er vou s system in fect ion , an d can cer.3
sia an d con t in u ou s in t raven ou s h ep arin in fu sion to m ain tain an Conversely, a Glasgow Com a Scale score ≥ 14–15 an d an isolated
act ivated clot t ing t im e of 200 to 300 secon ds, w ith con t in uous in t racran ial hyperten sion syn d rom e are predictors of favorable
n eu rophysiological m on itoring in cluding som atosen sor y evoked outcom e.46 Th e m ost com m on cau se of early death (w ith in 30
poten t ials, brain stem au ditor y evoked resp on ses, an d elect ro- days) in p at ien t s w ith CSVT is t ran sten torial h ern iat ion du e to
en cep h alography. A 5-Fren ch (F) sh eath is placed in it ially in th e ICH, d iffu se ed em a, or m u lt ip le p aren chym al lesion s.47 Ot h er
fem oral ar ter y. A 5F gu iding cath eter is in t roduced an d posi- possible cau ses of death in clu de stat u s epilept icu s, pu lm on ar y
t ion ed in th e com m on carot id ar ter y. Bilateral carot id inject ion s em bolism , an d m ed ical con dit ion s. Risk factors for 30-day m or-
are perform ed to con firm th e presen ce of th e th rom bus an d de- t alit y are com a, d eep ven ou s t h rom bosis, ICH, an d p osterior
lin eate its locat ion an d exten t on th e ven ou s p h ase. A 6F gu iding fossa lesion s.47 Min or n europ sych iat ric sym ptom s (depression ,
cath eter is th en select ively in t rodu ced in to th e in tern al jugu lar an xiet y) an d m ild cogn it ive deficit s can be seen in up to 50% of
vein th rough th e fem oral vein . A m icrocath eter is in t roduced over pat ien ts after CSVT.
a m icroguidew ire an d advan ced in to th e occluded sin us. Th e Th e rate of recan alizat ion of occlu ded sin u ses/vein s is 85%
th rom bu s can be m ech an ically m an ip u lated an d disru pted w ith an d occurs m ostly in th e first 3 m on th s after th e th rom bot ic
th e gu idew ire an d th e cath eter to in crease exposu re of th e clot even t .7 Recan alizat ion is rare beyon d th is p oin t . Alth ough recan -
to th e th rom bolyt ic agen t w h ile also redu cing th e tot al dose of alizat ion is n ot related to outcom e, perform ing a follow -up CTV
th rom bolyt ics delivered. A loading dose of t-PA is in it ially ad- or MRV is gen erally recom m en ded in all pat ien ts after 3 to 6
m in istered th rough th e length of th e th rom bus. Th is is follow ed m on th s to assess for recan alizat ion of th e occluded sin us/vein .19
by con t in uous in fusion of t-PA at 1 to 2 m g/h w ith th e m icrocath - Recu rren ce of CSVT is u n com m on , occu rring in on ly 2.2% of p a-
eter posit ion ed at th e rost ral segm en t of th e th rom bus. During t ien ts.3 Late com p licat ion s in clu de h eadach es (in 50% of cases),
the infusion therapy, sinus venography is perform ed and repeated rem ote seizu res (11%), visual loss (2%) due to pap illedem a an d
as n ecessar y to m on itor th e effect of t reat m en t . Th e pat ien t’s opt ic atrop hy, an d dural or pial ar terioven ou s fist u la (1%).
n eu rologic st at us an d vital sign s sh ould be frequen tly assessed,
as t reat m en t t im e m ay be prolonged (24 h ou rs or m ore).
Mech an ical th rom bolysis m ay allow faster an d m ore efficien t
sin u s recan alizat ion com p ared w ith th rom bolyt ics. Mech an ical
th rom bolysis is u su ally com bin ed w ith ch em ical th rom bolysis.
■ Conclusion
As discu ssed above, th e arm am en t ariu m in clu des coron ar y or Overall, CSVT is a rare con dit ion th at h as a favorable long-term
com p lian t balloon s, th e AngioJet device, th e Merci device, an d clin ical outcom e an d it s recu rren ce is rare. Th e presen tat ion can
th e Pen u m bra System . Neu rosu rgeon s can u se a com bin at ion of be ver y subtle, an d a h igh in d ex of suspicion is required to m ake
th ese d evices to ach ieve opt im al recan alizat ion of th e th rom - th e diagn osis. Th e diagn osis sh ou ld alw ays be con firm ed w ith
bosed sin us. A balloon can be advan ced in to th e occluded sin us, MRI an d MRV (or CTV). System ic an t icoagu lat ion is th e m ain st ay
exp an ded, an d th en ret racted . Mu lt ip le passes m ay be n ecessar y of th erapy. En d ovascular th erapy w ith m ech an ical th rom bec-
u n t il p ar t ial recan alizat ion is ach ieved . Th e AngioJet device h as tom y or chem ical throm bolysis is reserved for critically ill patients
been th e m ost com m on ly used device in m ech an ical th rom bec- an d th ose w h o deteriorate or fail to im prove despite m a xim al
tom y for CSVT. A 6F KSAW sh ut tle sh eath (Cook Medical, Bloom - m edical th erapy.

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29 Medical and Endovascular Treatm ent of Cerebral Sinus and Venous Throm bosis 375

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p relim in ar y resu lt s using th e AngioJet device. J Neuroin ter v Surg 2013;5: 46. Ferro JM, Lop es MG, Rosas MJ, Ferro MA, Fon tes J; Cerebral Ven ou s
49–53 Th rom bosis Por t ugese Collaborat ive St u dy Grou p . Long-term p rogn osis of
44. New m an CB, Pakbaz RS, Nguyen AD, Kerber CW. En dovascular t reat m en t cerebral vein an d dural sin us th rom bosis. resu lt s of th e VENOPORT st udy.
of exten sive cerebral sin us th rom bosis. J Neurosurg 2009;110:442–445 Cerebrovasc Dis 2002;13:272–278
45. Ku lcsár Z, Marosfoi M, Beren tei Z, Szikora I. Con t in u ou s th rom bolysis an d 47. Can h ão P, Fer ro JM, Lin dgren AG, Bou sser MG, St am J, Bar in agar rem en t -
repeated th rom bectom y w ith th e Pen um bra System in a ch ild w ith h em - er ia F; ISCVT Invest igators. Cau ses an d p red ictors of d eat h in cerebral
orrh agic sin u s th rom bosis: tech n ical n ote. Act a Neuroch ir (Wien ) 2010; ven ous throm bosis. St roke 2005;36:1720–1725
152:911–916

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30 Spinal Cord Infarction
Michael J. W ang, W illiam P. Cheshire, and Jam es F. How ard, Jr.

Acu te sp in al cord isch em ia is often a p oten t ially d evast at in g creased ar terial supply to th e th oracic spin al cord occurs in par-
con dit ion associated w ith sign ifican t m orbidit y an d m or t alit y. allel to its m et abolic dem an d.6 Th e m ajor th oracic radicu lar ar-
For t u n ately, spin al cord in farct ion occu rs far less com m on ly th an ter y, th e ar teria radicularis m agn a an terior of Adam kiew icz (also
cerebral in farct ion . Alth ough th e in ciden ce of spin al cord isch - kn ow n as th e ar ter y of Adam kiew icz), provides th e m ajor blood
em ia is u n kn ow n , th e gen eral con sen su s in th e m edical com m u - su p p ly to t h e low er t h oracic an d lu m bar sp in al cord an d t h e
n it y is th at it is con sidered to be relat ively in frequen t , accoun t ing con u s m edu llaris (Fig. 30.2). This ar ter y usu ally arises from th e
for 1.2% of adm ission s for vascular n eurology path ologies at on e left in tercost als, var iably from T9 to T12 in 75% of in d ivid u als,
m ed ical cen ter in t h e 1980s.1 Ext rap olat in g from est im ates of T5 to T8 in 15%, an d L1 to L2 in 10%.7 An oth er radicu lar ar ter y
total st roke in ciden ce in th e United St ates, w h ich m ay be as h igh com m on ly occu rs n ear T7.
as 800,000 an n u ally, it is exp ected th at 9,600 cases of spin al cord Th e p osterior sp in al ar teries origin ate from th e ver tebral or
in farct ion occu r each year.2 Th is con dit ion t yp ically affect s adult posterior in ferior cerebellar ar teries an d descen d th e sp in al cord
pat ien ts, alth ough ch ildren can develop sp in al cord in farct ion in th rough t h e posterior lateral su lci (Fig. 30.3). Like th e an terior
cer t ain circu m st an ces.3 sp in al ar ter y, th e posterior sp in al arteries are sup plied by radic-
Sp iller first described a case of an terior ar ter y syn drom e in u lar arteries, com m on ly bet w een 10 an d 20.8 Th ey frequen tly
1909 in a p at ien t w h o h ad su ffered an an terior sp in al ar ter y an astom ose w ith each oth er an d are h eavily con n ected to th e
th rom bosis an d w as su bsequ en t ly fou n d to h ave an in farct in th e periph eral an d posterolateral p lexu ses. Th e dorsal colu m n s an d
an terior aspect of th e spin al cord u pon au topsy.4 Th e t ypical pre- th e p osterior h orn s are areas of th e sp in al cord th at th e posterior
sen tat ion of spin al cord in farct ion involves acu te p arap aresis or sp in al ar teries sup ply.
qu adrip aresis, dep en ding on th e affected level of th e spin al cord. Th e an terior an d posterior spin al ar teries form a spin al ar te-
Diagn osis is u sually m ade clin ically based on h istor y an d clin ical rial p lexu s th at is rich ly in ter w oven arou n d th e su rface of th e
sign s an d sym ptom s, alth ough n eu roim aging can be u sed to h elp spin al cord. Th ese an astom oses give rise to circum feren t ial ar-
con firm th e diagn osis an d exclu de oth er con dit ion s. teries th at provide vascular supply to th e periph er y of th e cord.
Th e p en et rat ing exten sion s of th e an terior spin al ar ter y are t h e
left an d righ t su lcocom m issu ral ar teries, w h ich su p ply th e deep
st r u ct u res of th e sp in al cord.6
It sh ou ld be n oted t h at an area of relat ive hyp ovascu lar it y
■ Anatomy exist s in th e m idth oracic region at ap p roxim ately T4 to T8 th at
Th ree m ajor blood vessels arising from th e ver tebral ar teries in lies bet w een th e lu m bar an d vertebral ar terial su pplies. Th is re-
th e n eck ser ve as th e prim ar y vascu lar su p p ly to th e sp in al cord: gion con tain s few er an astom oses an d h as relat ively decreased
on e an terior spin al ar ter y an d a pair of posterior spin al ar teries. perfu sion com p ared w ith th e rest of th e spin al cord.9,10 Th u s, th is
The anterior spinal arter y, w hich supplies the anterior t w o-thirds vu ln erable zon e is t h e m ost su scept ible to in farct ion d u r in g
of th e spin al cord, origin ates in its m ost rost ral por t ion from th e t h oracic su rger y or ot h er con d it ion s cau sin g d ecreased aor t ic
ver tebral ar ter ies at th e level of t h e m ed u lla oblon gat a. It d e- pressure an d com prom ise of direct in flow to segm en t al ar teries.
scen ds along th e cen ter of th e an terior aspect of th e sp in al cord Un der th ese circu m st an ces, m ain tain ing adequate spinal perfu-
in th e an terior m edian su lcu s from th e foram en m agn um to th e sion pressure is vital to protect ing th is region from ischem ic dam -
con u s m edu llaris (Fig. 30.1). Alth ough th e blood flow th rough age.11 Ven ou s d rain age of t h e sp in al cord occu rs via t w o m ajor
th e an terior sp in al ar ter y is t ypically con t in u ou s th rough ou t it s sp in al vein s, t h e m ed ian p oster ior an d an terior sp in al vein s,
cou rse,4 th e diam eter of th e an terior spin al ar ter y varies con sid- w h ich are associated w ith an exten sive ven ou s n et w ork en cir-
erably th rough ou t it s length , w ith th e sm allest diam eter occu r- clin g t h e sp in al cord . Th ese t w o vein s d rain in to a ser ies of ra-
ring in th e th oracic segm en t of th e spin al cord an d th e largest dicu lar vein s. An terior an d p osterior radicu lar vein s drain in to
diam eter occu rring in th e lu m bosacral region of th e cord.5 th e epidural ven ou s plexus (also kn ow n as Bat son’s plexus). Th e
Along its cou rse, th e an terior spin al ar ter y receives input from ven ou s p lexu s d rain s in to t h e t h oracic, abd om in al, an d in ter-
six to n in e rad icu lar ar ter ies in var iable locat ion s. Th ese sm all costal vein s, an d th en fin ally in to th e azygous an d pelvic ven ou s
ar ter ies en ter t h e sp in al can al t h rough t h e in ter ver tebral fora- system s.12 Of n ote, th e ven ou s drain age of th e spin al cord does
m en an d supply blood to th e em erging n er ve roots. In part icular, n ot con tain valves, so in creased in t ra-abdom in al pressure can
th e th oracic sp in al cord is d ep en den t on vascu lar con t ribu t ion s cau se reflu x of blood carr ying m et ast at ic cells or in fect iou s or-
from th e radicu lar ar teries an d con sequ en tly m ay be m ore vu l- gan ism s in to th e epidu ral space, p erm it t ing pelvic or abdom in al
n erable to isch em ic inju r y, alt h ough t h e con cept of a t h oracic n eoplast ic or in fect ious processes to spread h em atogen ously to
w atersh ed zon e h as been qu est ion ed becau se th e relat ively de- th e spin al cord .

377

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378 III Ischemic Stroke and Vascular Insufficiency

Fig. 30.1 Extrinsic arterial supply to the spinal cord. Radicular arteries at arteries and caudally from the great radicular artery of Adamkiewicz. (Re-
various levels join to form the discontinuous anterior spinal artery, which printed from Cheshire WP, Santos CC, Massey EW, Howard JF Jr. Spinal cord
connects via the spinal arterial plexus to the pair of posterior spinal arteries. infarction: etiology and outcom e. Neurology 1996;47:321–330, with per-
The anterior spinal artery arises rostrally from branches of the vertebral m ission from Lippincot t Williams & Wilkins.)

Th rom boem bolic disease is an oth er vascu lar cau se of sp in al


■ Pathophysiology cord in farct ion . Cardiogen ic em bolism from at rial m yxom as, ar-
A w ide variet y of disease processes can con t ribute to spin al cord t ificial h ear t valves, valvu lar vegetat ion s, or invasive procedu res
in farct ion . Am ong th e m ost com m on cau ses of spin al cord in - su ch as coron ar y angiograp hy are kn ow n cau ses of spin al cord
farct ion are diseases an d procedu res involving th e aor t a. In par- in farct s.18 Fibrocar t ilagin ou s em bolism is a rare cau se of spin al
t icu lar, p rocedu res involving th e descen ding th oracic aor ta an d cord in farct ion . Fibrocart ilagin ou s em boli are gen erated from
th oracoabdom in al aor t a carr y a sign ifican t risk of isch em ia to h ern iated in ter ver tebral disks, but th e m ech an ism by w h ich disk
th e sp in al cord, as th e in ciden ce of spin al isch em ia in an op en fragm en t s en ter th e vessels is u n clear. Often th ere is a tem p oral
rep air of th e aor t ic an eu r ysm s m ay be as h igh as 32%.13 Th e risk relat ion ship w ith m in or h ead or n eck t raum a prior to th e on set
of spin al cord in farct ion appears to be low er w ith th oracic en do- of sym ptom s. It is hypoth esized th at h igh axial loading cau ses
vascu lar aor t ic repair, bu t both open surger y an d en dovascular in creased pressu re w ith in a h ern iated disk, w h ich th en inject s
repair are n on eth eless associated w ith sp in al cord isch em ia.14 sem iflu id n u cleu s p u lp osu s m ater ial in to t h e sp in al ver tebral
Th e su rgical risk of sp in al cord isch em ia is greater w h en com pli- p lexu s an d ar ter ial ch an n els, lead ing to cord in farct ion . Most
cated by in t raop erat ive hypoten sion or p rolonged clam p ing of cases involve em bolism in th e cer vical cord, som et im es exten d-
th e aor t a proxim al to th e ren al ar teries. Op erat ive ligat ion of th e ing in to th e low er m edu lla oblongat a or th e upper th oracic spi-
low er t h oracic or lu m bar segm en t al vessels fu r t h er in creases n al cord.19
t h is r isk.15 In frequ en t ly, an acu te d issect ion of t h e d escen d ing In ad d it ion to vascu lar et iologies for sp in al cord in farct ion ,
aor ta disten ding from th e aor t ic valve to th e aor t ic bifurcat ion occlu sion of spin al ar teries due to m ech an ical st ress associated
can lead to occlu sion of th e spin al arteries, cau sing sp in al cord w ith sp in al disease (e.g., lum bar spon dylosis, sp in e com p ression
in farct ion .16 fract u res, spon dylolist h esis, an d cer vical disk p rot ru sion ) an d
System ic hyp oten sion (e.g., secon dar y to card iop u lm on ar y forcefu l m ovem en t s t h at m ay t r igger ar ter ial d issect ion (e.g.,
ar rest , h em or rh age, etc.) is a m ajor con t r ibu tor to sp in al cord exten sion of t h e back, m ovem en t of t h e ar m , Valsalva m an eu -
ischem ia. On e autopsy series of pat ien t s w ith kn ow n cerebral ver, an d in it iat ion of gait ) also h ave rarely p recip it ated acu te
hypoxic-isch em ic dam age due to cardiac arrest or paroxysm al sp in al cord in farct ion .20 Th is lin k is esp ecially st rong in th e con -
system ic hypoten sion fou n d th at 45% of cases also h ad sp in al text of m ech an ical spin al disease at th e sam e level, as th is m ay
cord dam age, m ost prevalen t in t h e lu m bosacral levels of th e in crease th e risk for occlusion or t raum at ic inju r y of th e local
cord .17 It h as been hypoth esized th at h igh m etabolic dem an ds radicular ar ter y. Sp in al disk prolapse or h ern iat ion can lead to
an d a large n um ber of n eu ron s in th e lum bosacral cord m ay ex- acute vascular com pression , usually involving th e radicu lar ar-
plain w hy th e low er levels of th e cord seem m ost p ron e to th e ter y, th ough th e an terior sp in al ar ter y or lu m bar ar ter y can also
effects of hyp oten sion after global isch em ia.17 be com prom ised.

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30 Spinal Cord Infarction 379
Fig. 30.2 Segm ental arterial supply to the spinal cord. The
anterior radicular artery issues from the posterior ram us of
a lum bar intercostal artery. L., left; R., right. (Reprinted from
Cheshire WP, Santos CC, Massey EW, Howard JF Jr. Spinal cord
infarction: etiology and outcom e. Neurology 1996;47:321–
330, with perm ission from Lippincot t William s & Wilkins.)

Fig. 30.3 Intrinsic arterial supply shown in an oblique


cross section of the spinal cord. The anterior spinal artery
arises from the anterior radicular artery and com m uni-
cates with the posterior spinal arteries via the spinal ar-
terial plexus. Sulcocom m issural arteries arise from the
anterior spinal artery and supply the anterior t wo-thirds
of the spinal cord. Circum ferential arteries perforate and
supply the cord surface. The posterior spinal arteries sup-
ply the dorsal columns. (Reprinted from Cheshire WP,
Santos CC, Massey EW, Howard JF Jr. Spinal cord infarc-
tion: etiology and outcome. Neurology 1996;47:321–330,
with perm ission from Lippincot t William s & Wilkins.)

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380 III Ischemic Stroke and Vascular Insufficiency

Sp in al t ran sien t isch em ic at t acks (TIAs) are d escr ibed an d sexu al dysfu n ct ion , an d hypoten sion th at m ay be or th ostat ic or
t ypically m an ifest as p ain less p arap aresis or qu adriparesis th at su stain ed. Im p aired th erm oregu lat ion m ay occu r as a resu lt of
m ay be tem porar y, last ing a few m in u tes to several h ours, an d im pairm en t of in terru pt ion of vasom otor an d su dom otor in n er-
w ith out loss of con sciousn ess or cran ial localizing feat ures. Local vat ion below th e level of th e lesion . Urin ar y reten t ion is t ypical
ath erosclerot ic disease m ay resu lt in in term it ten t clau d icat ion of in th e acu te ph ase, an d involun t ar y voiding or defecat ion m ay
th e spin al cord m an ifested by act ivit y-in du ced t ran sien t sym p - occur n ear th e on set of isch em ia. Overact ive bladder sym ptom s
tom s of m yelopathy.20,21 Th is in term it ten t sp in al clau d icat ion are t ypical of th e ch ron ic ph ase. Pat ien ts w ith spin al cord lesion s
syn drom e is m ost likely to occu r in pat ien ts w ith foram in al ste- above th e level of T5 m ay presen t w ith auton om ic dysreflexia, in
n osis during cer vical or lum bar exten sion , w h ich com prom ises w h ich disin hibited sym path et ic neurons of the interm ediolateral
th e in t raver tebral foram in a th rough w h ich th e sp in al radicu lar cell colum n cause an exaggerated hypersym path et ic resp on se to
ar teries p ass. m ildly n oxious st im uli such as a disten ded bladder.26 In addit ion ,
Many pat ien t s w ith spin al cord in farct ion do n ot h ave a clearly if th e lesion is in th e rost ral spin al cord at th e level of C3 th rough
iden t ified et iology. Often th ese p at ien ts h ave ath erosclerot ic risk C5, in terr u pt ing in n er vat ion to th e ph ren ic n er ve, resp irat ion
factors, an d ath eroth rom bot ic disease is presum ed to be a con - m ay be com p rom ised.
t ribu t ing cau se of sp in al cord in farct ion . Oth er p rim ar y th rom - Posterior sp in al ar ter y in farct ion is qu ite rare. Th is can resu lt
bot ic an d vascular even ts can cause spin al cord isch em ia as w ell.6 from in terr u pt ion of th e posterior sp in al ar teries or from defi-
Vascu lit is result ing from system ic in flam m ator y con dit ion s such cien t collateral perfusion in th e set t ing of diffuse arteriosclero-
as Croh n’s disease, polyar terit is n odosa, an d gian t cell ar terit is sis. Becau se of th e involvem en t of th e dorsal colu m n s from th is
also m ay lead to isch em ic m yelopathy. Hypercoagulabilit y an d injur y, p osterior spin al ar ter y in farct ion t ypically produ ces a loss
sickle cell disease h ave been im plicated in som e cases of sp in al of p ropriocept ion an d vibrator y sen se below th e level of injur y,
cord in farct ion . Vasosp ast ic agen t s su ch as cocain e or in t rat h ecal suspen ded global an esth esia at th e level of th e injur y, an d are-
ch em ical irrit an t s u sed in ep idu ral inject ion s can also p red is- flexia due to posterior h orn involvem en t.8 Motor w eakn ess can
pose to th rom bosis an d spin al cord in farct ion . Syp h ilit ic ar terit is be associated w ith posterior spin al ar ter y in farct ion , but t ypi-
w as on ce a com m on cau se of an terior sp in al ar ter y isch em ia, an d cally is m ilder in degree an d often t ran sien t .
bacterial in fect ion s st ill occasion ally cause paraplegia of vascular A t h orough n eu rologic exam in at ion of p at ien t s p resen t in g
origin . Spin al ven ous in farct ion is rare an d can be h em orrh agic w ith suspected spin al cord isch em ia is ver y im por tan t because
or isch em ic in n at u re. Decom pression sickn ess m yelopathy in clin ical p resen t at ion s are n ot alw ays as clear as on e fin d s in text-
scu ba d ivers resu lts from n it rogen bu bbles lodging in th e spin al book descript ion s, an d in som e cases early fin dings can be quite
vein s, w h ich m ay be associated w ith region s of focal h em orrh age su btle. Th e m ost com m on exam fin ding (especially in an terior
w ith in th e sp in al cord.22,23 spin al arter y in farct ion ) is flaccid w eakn ess in both low er ex-
trem ities and dim inished or absent m uscle stretch reflexes below
th e level of th e lesion . A clin ical presen t at ion w ith p reser ved
m otor st rength an d reflexes is m ore suggest ive of p osterior sp i-
n al ar ter y territor y isch em ia. Loss of spin oth alam ic percept ion
■ Clinical Presentation to pain an d tem perat ure is often seen on sen sor y exam in at ion ,
Th e cou rse of sp in al cord isch em ia can be variable in term s of an d propriocept ion loss m ay accom pany th ese sym ptom s acutely.
t im ing an d severit y of sym ptom s. Im pairm en ts from spin al cord Isolated propriocept ive loss is rarely n oted. Acute bladder dis-
infarction m ay range from m inor weakness to paraplegia or quad- ten t ion due to an aton ic u rin ar y bladder is t ypical, but m ay n ot
rip legia. In m ost cases, sen sor y sym ptom s occu r first , follow ed be n ot iced by th e pat ien t due to sen sor y loss. Rect al ton e is usu-
by m otor w eakn ess. Th e t im e from on set of sym ptom s to evolu- ally dim in ish ed in th e acute set t ing of a spin al cord in farct .15
t ion of w eakn ess m ay var y from several m in u tes u p to 24 h ou rs.24
In m any cases, acu te back p ain at th e level of th e lesion h as been
n oted to be a com m on sym ptom at on set th at disappears after
oth er n eu rologic deficits h ave developed.
Most spin al cord in farct ion s occu r in th e low er th oracic an d
■ Diagnostic Testing
lum bar spinal levels of the spinal cord. The m ost com m on presen- Alth ough th e diagn osis of spin al cord in farct ion is m ade clin i-
tation for spinal cord infarction is anterior spinal arter y syndrom e, cally, th e presen t ing sign s of a spin al cord in farct ion m ay be vari-
in w hich infarction occurs over the anterior t wo-thirds of the spi- able an d n on specific in th e in it ial ph ase. Th ere are several oth er
nal cord . A pat ien t w ith an an terior spin al ar ter y in farct t ypically poten t ial cau ses of abr u pt-on set m yelop athy th at m u st be con -
presen ts w ith abru pt on set of w eakn ess an d loss of sp in oth a- sidered in th e differen t ial diagn oses. A com p ressive m yelop athy
lam ic p ain an d tem perat u re sen se below th e level of th e lesion . du e to a h em atom a, abscess, or n eop lasm in th e epid u ral or su b -
Other com m on sym ptom s include burning, aching, cram ping, and du ral sp ace is th e m ost im p or tan t categor y of diagn osis to ex-
t in glin g in t h e low er t r u n k an d low er ext rem it ies. Vibrator y clude, as these cases are surgical em ergencies that require urgent
sen se an d p ropriocept ion are relat ively sp ared in th is syn drom e. in ter ven t ion w ith su rgical decom pression or em ergen t radiat ion
Flaccid p arap legia an d areflexia m ay be seen in th e acu te st ages th erapy. At yp ical p resen tat ion s of t ran sverse m yelit is an d acute
of spin al cord in farct ion , but th ese sym ptom s progress over th e polyn eu rop athy (e.g., Gu illain -Barré syn drom e) are oth er con di-
cou rse of several w eeks to sp ast icit y an d hyperreflexia.25 t ion s th at m ay be con fu sed w ith sp in al cord in farct ion . Given th e
It should be noted th at sign ificant autonom ic dysfunction m ay w ide range of differen t ial diagn oses th at m ay also cause an acute
be presen t w ith acu te spin al ar ter y in farct ion . Th ese auton om ic m yelopathy-t ype of presentation , other diagnost ic st udies sh ould
deficit s in clu d e bow el or blad d er dysfu n ct ion , p aralyt ic ileu s, be perform ed as p ar t of th e w orku p.

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30 Spinal Cord Infarction 381

Magn et ic reson an ce im aging (MRI) sh ou ld be p erform ed u r- A lum bar pun ct ure sh ould also be perform ed if an in fect ious
gen tly in m ost cases, prim arily to exclu de th e altern at ive diagn o- or in flam m ator y cause of m yelopathy is suspected. Spin al cord
sis of com pressive m yelopathy. MRI can also provide confirm ator y in farct ion m ay cau se elevated p rotein in th e cerebrospin al fluid
eviden ce of spin al cord in farct ion as w ell as in form at ion regard- (CSF), bu t d oes n ot u su ally resu lt in a p leocytosis. Test in g CSF
ing th e u n derlying et iology. MRI ch anges w ith hyperin ten sit ies for im m un oglobu lin G levels an d oligoclon al ban ds m ay be h elp -
on T2-w eigh ted im ages h ave been repor ted in m ore th an 90% of fu l in dist ingu ish ing dem yelin at ing disease from vascu lar cau ses
spinal cord in farct ion cases, alth ough th ese ch anges are n ot al- of acute m yelopathy.
w ays specific to et iology.27 It rem ain s ch allenging to dist inguish
sp in al cord in farct ion from ot h er cau ses of acu te n on com p res-
sive m yelop at h ies based on MRI alon e. Moreover, on e of t h e
m ajor lim itat ion s of cu rrent MRI tech n iques is th e lim ited sen si-
t ivit y of a stan dard MRI, esp ecially in th e first few h ou rs follow -
■ Treatment
ing on set of sym ptom s.28 Diffusion -w eigh ted im aging h as been To date, th ere are n o establish ed th erapeut ic regim en s for spin al
est ablish ed as th e m ost sen sit ive m odalit y for diagn osing acu te cord in farct ion . In th e p ast , oth er th erap eu t ic ap proach es to t reat
cerebral isch em ia an d h as th e poten t ial to becom e an im por tan t spin al cord in farct ion in th e acute set t ing h ave been invest igated,
tech n ique in th e evaluat ion of spin al cord isch em ia.29 How ever, part icu larly in th e set t ing of th oracic an d th oracoabdom in al aor-
th e effect iven ess of th is m odalit y in obtain ing ad equ ate im aging t ic an eu r ysm repair. Th ese in ter ven t ion s in clu ded dist al aor t ic
is lim ited by var iou s tech n ical asp ect s, su ch as m ot ion ar t ifact perfusion, deliberate hypotherm ia, reim plan tation of in tercostal
an d su scept ibilit y ar t ifact . More recen t ly, m agn et ic reson an ce ar teries, an d ph arm acological approach es to protect th e spin al
lin e-scan diffusion im aging (a variat ion of diffu sion -w eigh ted cord from isch em ia.37 Alth ough th ese tech n iques h ave decreased
im aging th at is relat ively in sen sit ive to m agn et ic suscept ibilit y th e in ciden ce of spin al cord in farct ion in th e p eriop erat ive an d
effects and m otion artifact) seem s to hold som e prom ise for being p ostop erat ive set t ing, t h e r isk of sp in al cord isch em ia rem ain s
a m ore reliable m eth od of diagn osing spin al cord in farct ion in sign ifican t .38
th e acu te set t ing.30,31 In pat ien ts w h o h ave experien ced spin al cord isch em ia fol-
Com pu ted tom ograp hy (CT) w ith m yelography w as th e pre- low ing aort ic su rger y or t h oracic en dovascu lar aort ic repair, a
ferred m eth od of im aging in evaluat ing cases of suspected spin al specific protocol involving a com bin at ion of blood pressure aug-
cord in farct ion p rior to th e adven t of MRI. CT con t in u es to be th e m en t at ion w ith vasopressors an d reduct ion of spin al cord can al
im aging tech n iqu e of ch oice in evaluat ion of t raum a, accurately p ressu re w it h lu m bar d rain s m ay be effect ive in lim it ing t h e
depict ing bony abn orm alit ies an d h em orrh age in th e sp in al col- exten t of n eu rologic d eficit s.13 Preop erat ively, p at ien t s d eem ed
u m n , as w ell as su sp ected d isk h er n iat ion .32 How ever, MRI is to be at h igh risk for spin al cord isch em ia (e.g., previous abdom i-
t h e preferred im aging m odalit y w h en spin al cord in farct ion is n al aor t ic an eu r ysm repair, previous aor t ic dissect ion , exten sive
su sp ected , as MRI exceed s t h e sen sit ivit y of CT in detect ing p a- sten t coverage of th e aor t a or of th e posterior in tercost al ar teries
ren chym al lesion s of th e brain an d spin al cord. W h en it is n ot at T6–L2, or bilateral in ter n al iliac ar ter y occlu sion s) u n d ergo
p ossible to p er for m an MRI on a p at ien t d u e to a con t rain d ica- in t raoperat ive n eu rop hysiological m on itoring. Su ch m on itoring
t ion su ch as a card iac p acem aker, a CT m yelograp hy m ay be a (e.g., elect roen ceph alogram an d som atosen sor y or m otor evoked
reason able im aging altern at ive. Myelography is usually n orm al poten t ials) can iden t ify eviden ce of isch em ic inju r y to th e brain
in sp in al cord in farct ion . How ever, a filling defect seen at t h e or spin al cord during th e procedure, en abling acute in ter ven -
level of t h e lesion m ay suggest sp in al cord en largem en t d u e to t ion s to reverse or lim it th e exten t of n eu rologic inju r y.39 In addi-
in t ram edu llar y sw elling of th e spin al cord.33 t ion , a lu m bar d rain is often p laced in th ese h igh -risk pat ien ts,
Sp in al angiography is an ot h er im aging m odalit y th at can be an d in t raoperat ive in t racerebral pressure is m ain tain ed at 8 to
u sefu l in t h e evalu at ion of sp in al cord vascu lar d isord ers. Th e 12 m m Hg w it h in ter m it ten t CSF drain age.40 If t h e p at ien t h as
m ost com m on clin ical in d icat ion for sp in al an giograp hy is su s- a n orm al p ostoperat ive n eu rologic exam , spinal drain age is con -
p icion of a spin al vascu lar abn orm alit y, su ch as ar terioven ou s t in u ed for 12 h ou rs, an d th en th e lu m bar drain is cap p ed . Th e
m alform at ion .34 Spin al angiography can also be u sed to iden t ify lu m bar drain is su bsequ en tly rem oved if th ere are n o sign s or
occlusion s or sten osis of th e involved vessels, alth ough on e case sym ptom s of spin al cord isch em ia in th e n ext 24 h ou rs.
series suggests th at th e sen sit ivit y of th is im aging m odalit y for Serial n eu rologic assessm en t in th e p ostoperat ive set t ing is a
iden t ifying any vascu lar abn orm alit y is 55%.24 Historically, th ere n ecessar y com pon en t in th e early detect ion of sym ptom s sug-
h ave been som e con cern s over th e safet y of spin al angiography; gest ive of sp in al cord isch em ia. If t h e p at ien t d oes exp er ien ce
h ow ever, m ore recen t literat ure suggests th at spin al angiography low er ext rem it y w eakn ess in t raop erat ively or p ostop erat ively,
car r ies a ver y low r isk of n eu rologic an d system ic com p lica- th e m ean ar terial p ressu re is in creased in in crem en t s of 10 m m
t ion s.35 Th e u t ilit y of m agn et ic reson an ce angiograp hy an d CT Hg ever y 5 m in u tes w ith volu m e an d vasop ressor agen ts u n t il
angiograp hy is less w ell est ablish ed. sym ptom s resolve, bleeding com plicat ion s occu r, or th e m ean
In rare cases in w h ich t raum a h as been associated w ith spin al ar terial pressu re is judged to be u n acceptably h igh . Often th ese
cord in farct ion , it is ap propriate to obt ain spin e radiograp h s to vasop ressor d osages far exceed t yp ical d osages u sed to t reat
exclu de any p ossible fract u re as a con fou n ding factor for sp in al hypoten sion . If a lum bar drain is already in place, it sh ould be
pain or con t ribu t ing factor for sp in al cord inju r y. How ever, on e open ed an d set to drain at 8 to 12 m m Hg; if th ere is n o lum bar
lim ited case series of eigh t pat ien ts w ith a diagn osis of t rau m at ic drain in place, aggressive blood pressure augm entat ion is the first-
in farct ion of th e sp in al cord foun d n o bon e abn orm alit ies on th e lin e th erapy. A lu m bar drain sh ou ld be placed if th ere is n o re-
plain film s. In addit ion , CT m yelography w as p erform ed in seven spon se to blood pressure augm en tat ion w ith in 10 to 20 m in utes.
of th ese p at ien t s an d fou n d to be n orm al in all of th em .36 Vasopressors are slow ly w ean ed over th e n ext 24 to 48 h ours,

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382 III Ischemic Stroke and Vascular Insufficiency

w ith close serial m on itoring of n eurologic fun ct ion . After vaso- m en t s S4 an d S5. ASIA grade B in dicates th at sen sor y, but n ot
pressor su p por t h as been w ean ed, th e lu m bar d rain sh ou ld be m otor, fun ct ion is preser ved below th e n eurologic level an d in -
cap ped an d th en rem oved after 24 h ou rs if th e n eu rologic exam clu des th e sacral segm en t s S4 an d S5, an d n o m otor fu n ct ion is
rem ain s st able.13 It sh ou ld be n oted t h at t h is p rotocol h as n ot preser ved m ore th an th ree levels below th e m otor level on eith er
been evalu ated in any con t rolled st u dy, an d t h e u se of t h is p ro - side of th e body. ASIA grade C an d D spin al injuries both h ave
tocol in spin al cord in farct ion due to oth er cau ses h as n ot been preser ved m otor fu n ct ion below th e n eu rologic level of injur y,
st u d ied. w ith th e key differen ce being th at m ore th an h alf of sign ifican t
Th rom bolyt ic th erapy for sp in al cord isch em ia rem ain s inves- m uscle fun ct ion s below th e n eurologic level are un able to dis-
t igat ion al at th is t im e an d h as n ot been system ically st u died. play fu ll range of m ot ion again st gravit y in ASIA grade C, w h ereas
Th ere h ave been isolated case rep or t s of in t raven ou s th rom boly- fu ll range of m ot ion again st gravit y is d em on st rated in ASIA
sis being u sed for p at ien t s presen t ing w ith sign s an d sym ptom s grade D.45
of spin al cord in farct ion w ith in 3 h ours of sym ptom on set .41 Fu r- Severit y of im p airm en t (esp ecially w ith grade A or B on th e
th er st u dies are n ecessar y to w eigh th e p oten t ial ben efit s of ASIA im pairm en t scale) on th e in it ial n eu rologic exam seem s to
using in traven ou s th rom bolyt ic agen t s in sp in al cord isch em ia be th e best predictor of poor clin ical ou tcom e. Th e likelih ood of
again st th e p oten t ial risks of h em orrh age. In p ar t icu lar, on e sig- clin ical im provem en t in creases w h en th e in it ial deficit s are less
n ifican t barrier to th rom bolyt ic t reat m en t w ith in th e th erapeu- severe. It h as been suggested th at som e degree of preser vat ion of
tic treatm ent w in dow is the need to exclude aortic dissection and spinal cord fun ct ion s below th e n eurologic level is essen t ial for
vascu lar m alform at ion s, w h ich are con t rain dicat ion s to th rom - th e recover y process. In a st u dy from Bern , Sw it zerlan d, n early
bolyt ic agen ts. on e-th ird of pat ien ts w ith m ore severe im pairm en t (ASIA grade
Any determ in ed un derlying et iology for spin al cord in farct ion A or B) on in it ial exam in at ion requ ired a w h eelch air long-term ,
(e.g., system ic vasculitis, aortic dissection , cardiogenic em bolism ) w hereas m ore th an 90% of pat ien t s w h ose acute deficits w ere
sh ou ld be t reated w ith th e goal of p reven t ing fu r th er deteriora- classified at th e m ildest level (ASIA grade D) w ere able to w alk
t ion an d secon dar y sp in al cord isch em ic even t s. If p resen t an d in depen den tly or w ith an assist ive device w ith in 4 years.43 An -
am en able to surgical repair, vascular m alform at ion s of th e spin al oth er st udy from th e Mayo Clin ic foun d th at alth ough long-term
cord sh ou ld be rep aired to p reven t fu r th er n eu rologic declin e. outcom e can rem ain poor in pat ien t s w ith com plete or n early
In patients w ith un derlying vascular risk factors or com orbid vas- com plete spinal cord syndrom es, delayed functional recover y w as
cular disease, in parallel w ith th e recom m en dat ion s appropriate possible in up to 58%of patients.44 Substant ial fun ct ional recover y
for pat ien ts w ith cerebrovascular disease, th e use of an an t iplate- m ay occur over t im e even in patien ts w ith ver y severe deficit s
let agen t is recom m en ded for secon dar y st roke p reven t ion . u pon h osp ital disch arge an d at early follow -u p. In t act p roprio-
At later st ages, reh abilitat ive care is an im port an t part of th e cept ion on in it ial n eurologic exam h as also been associated w ith
recover y process in sp in al cord in farct ion . As in cerebral stroke a bet ter ou tcom e.46 W h et h er factors su ch as advan ced age an d
pat ien ts, an effect ive reh abilitat ion p rogram for pat ien ts w h o fem ale sex in fluen ce fun ct ion al outcom e h as been debated.
h ave suffered from spin al cord in farct ion is crit ical to m a xim ize Th e m or t alit y rate after sp in al cord in farct ion ranges from 9
fu n ct ion al recover y an d qu alit y of life w h ile m in im izing t h e to 23%.43,47 Pat ien ts w ith th e greatest risk of death are th ose pre-
excess disabilit y associated w ith im m obilit y, p ain , or auton om ic sen t ing w ith sp in al cord isch em ia in th e con text of acu te aor t ic
dysfu n ct ion . Alth ough th ere are n o con t rolled t rials of th e effi- rupt ure or dissect ion . Th e in -h ouse m ort alit y rate is over 50%
cacy of p hysical an d occu pat ion al th erapy follow ing spin al cord in pat ien t s w h o develop com p licat ion s of spin al cord in farct ion
in farct ion , th e sam e prin cip les th at guide th e t reat m en t of pa- follow ing open surgical repair of a rupt ured abdom in al aor t ic
t ien t s w ith sim ilar n eu rologic deficit s from oth er cau ses app ly an eur ysm .48 Pat ien ts w ith h igh cer vical cord in farct s are also at
in th e care of pat ien t s w ith spin al cord deficit s. In gen eral, com - risk of poten t ially life-th reaten ing com p licat ion s dep en ding on
preh en sive reh abilit at ion p rogram s are effect ive for ret rain ing th e level an d exten t of th e lesion . Exten sive lesion s at C1–C2 can
m otor skills, teach ing com p en sator y st rategies w h en m otor defi- cau se com plete in terru pt ion of descen ding respirator y con t rol
cits can n ot be overcom e, an d preven t ing com plicat ion s such as to th e ph renic n er ves, leading to sudden respirator y arrest an d
falls, con t ract ures, deep ven ous th rom bosis, an d pressure sores. death . Par t ial lesion s at th e C3–C4 level can also cau se select ive
Reh abilitat ion can occu r in several differen t physical set tings in terrupt ion of autom at ic or volun t ar y respirator y p ath w ays.49
an d sh ould be coordin ated by a reh abilitat ion specialist direct ing
a com preh en sive in terdiscip lin ar y team .42

■ Conclusion
Sp in al cord in farct ion is a rare syn d rom e th at occu rs w h en th e
■ Prognosis vascu lar supply to th e spin al cord becom es com prom ised. Th ere
Prognosis for patients suffering from spin al cord infarction seem s are various poten t ial et iologies for spin al cord isch em ia, w ith th e
to be variable depen ding on th e in it ial severit y of n eurologic im - m ore com m on cau ses involving aor t ic vascular su rger y, system ic
pairm ent , especially the m otor deficits.43,44 Neurologic syndrom e hypoten sion , th rom boem bolic disease, an d m ech an ical t rau m a.
an d d egree of in it ial im p air m en t are often d efin ed accord ing Alth ough th e diagn osis of spin al cord in farct ion is usually m ade
to th e Am erican Spin al Inju r y Associat ion (ASIA) criteria, w h ich based on th e clin ical presen tat ion of w eakn ess, sen sor y loss,
classifies th e severit y of im p airm en t based on both sen sor y an d back pain , an d urin ar y dysfun ct ion , diagn ost ic im aging is h elpful
m otor defect s in each low er ext rem it y. ASIA grade A correlates to con fir m t h e d iagn osis an d exclu d e ot h er cau ses of acu te m y-
w ith th e absen ce of m otor or sen sor y fun ct ion in th e sacral seg- elop at hy. MRI is t h e p refer red m et h od of d iagn ost ic im aging.

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30 Spinal Cord Infarction 383

Cu r ren t ly, t h ere are n o sp ecific t reat m en t regim en s for sp in al Sign ifican t m orbidit y an d m or t alit y is associated w ith th is dis-
cord in farct ion s in t h e acu te set t in g, t h ough a p rotocol involv- ease, esp ecially in p at ien t s w it h a severe d egree of n eu rologic
in g in t raop erat ive som atosen sor y evoked p oten t ial m on itor in g, im p air m en t . How ever, su bst an t ial fu n ct ion al recover y m ay st ill
blood pressure augm en tat ion , an d lum bar CSF drain age h as been occur in pat ien ts w h o h ave th e ben efit of aggressive reh abilit a-
sh ow n to red u ce t h e r isk of p roced u re-related cord isch em ia. t ion p rogram s.

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abdom in al aort ic an eur ysm repair w ith bran ch ed sten t-graft s. J En dovasc aging. J Clin Neurosci 2005;12:466–468
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isch em ia follow ing th oracic en dovascular aort ic repair. Neurocrit Care 34. Ban dyopadhyay S, Sh eth RD. Acute spin al cord in farct ion : vascular steal in
2007;6:35–39 arterioven ous m alform at ion . J Child Neurol 1999;14:685–687
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descen ding th oracic an d th oracoabdom in al aor t ic op erat ion s in th e era of sis in 302 diagn ost ic angiogram s. Neurology 2011;77:1235–1240
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15. Geld m ach er DS, Sh ah L. Vascu lar m yelop at h ies. Con t in u u m : Lifelon g in farct ion of th e spin al cord in children . J Neurosurg 1986;65:608–610
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in t ype A aort ic dissect ions. St roke 2007;38:292–297 An n Th orac Surg 2002;74:413–419, discu ssion 420–421
17. Duggal N, Lach B. Select ive vu ln erabilit y of th e lum bosacral spin al cord 38. Woo EY, Mcgar vey M, Jackson BM, Bavaria JE, Fairm an RM, Pochet t in o A.
after cardiac arrest an d hypoten sion . St roke 2002;33:116–121 Spin al cord isch em ia m ay be redu ced via a n ovel techn ique of in tercost al
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43. Nedeltch ev K, Loh er TJ, Stepper F, et al. Long-term outcom e of acu te spin al 47. Salvador de la Barrera S, Barca-Buyo A, Mon toto-Marqués A, Ferreiro-
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45. Kirsh blum SC, Burn s SP, Biering-Soren sen F, et al. In tern at ion al st an dards Sch urin k GW. Open repair for r upt ured abdom in al aort ic an eur ysm an d
for n eurological classificat ion of spin al cord injur y (revised 2011). J Spin al th e risk of spin al cord isch em ia: review of th e literat u re an d risk-factor
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46. Masson C, Pruvo JP, Meder JF, et al; St udy Group on Spin al Cord In farct ion 49. How ard RS, Th orpe J, Barker R, et al. Respirator y in sufficien cy due to h igh
of th e Fren ch Neu rovascu lar Societ y. Spin al cord infarct ion : clin ical and an terior cer vical cord in farct ion . J Neurol Neu rosurg Psych iat r y 1998;64:
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Neurosurg Psych iat r y 2004;75:1431–1435

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31 Medical, Surgical, and Endovascular
Treatment of Claudication
Chelsea A. Dorsey and Jason T. Lee

Clau dicat ion , or in term it ten t clau dicat ion , refers to pain an d dis- St u dy sh ow ed th at th ere w as an in creased risk (3.5 in m en an d
com for t exp erien ced in th e low er ext rem it ies w ith am bu lat ion 8.6 in w om en ) of th e developm en t of claudicat ion in th ose w ith
th at is relieved by rest . Th e origin of th e w ord claudicat ion com es diabetes.8 Earlier st u dies suggested th at w om en m ay be affected
from th e Lat in claudicare, w h ich literally m ean s “to lim p.” In ter- later in life by PAD. More recen t st u dies, h ow ever, h ave dem on -
m it ten t claudicat ion falls w ith in th e spect rum of ch ron ic low er st rated th at th e age-adju sted in cid en ce of in ter m it ten t clau d i-
ext rem it y isch em ia, also kn ow n as low er ext rem it y p erip h eral cat ion is equ ivalen t bet w een gen d ers.9,10 Wor t h n ot in g is t h e
ar terial disease (PAD). Th e classic clin ical presen tat ion t ypically d ecreased prevalen ce of coron ar y ar ter y disease an d cerebrovas-
involves an older adu lt w h o describes calf cram ping an d fat igu e cular disease in w om en w ith PAD com pared w ith th eir m ale
associated w ith w alking a specific distan ce th at is alleviated by cou n terpar t s.10 St udies looking at th e associat ion bet w een PAD
a p er iod of rest . Th ese sym ptom s are rep rod u cible an d often an d race an d ethn icit y h ave also dem on st rated a con n ect ion . In a
w orsen as th e disease p rocess p rogresses. Clau dicat ion is on e of fu r th er exam in at ion of th e NHANES, Ostch ega an d colleagu es 11
th e m ost frequ en t reason s for referral to a vascu lar su rgeon . Leg fou n d t h at n on -Hisp an ic black m en an d w om en along w it h
pain , h ow ever, carries w ith it a broad differen t ial d iagn osis th at Mexican -Am er ican w om en h ad an in creased r isk of d evelop in g
in clu des, but is n ot lim ited to, n eurogen ic claud icat ion (lum bar PAD (19%) over th at of n on -Hispan ic w h ite m en an d w om en
spinal stenosis), arthritis, sym ptom atic Baker’s cyst, popliteal en- (15%). In 1997, Murabito an d colleagu es looked at th e con n ect ion
t rapm en t syn d rom e, fibrom u scu lar dysplasia, ven ou s clau dica- bet w een claudicat ion an d hyperlipidem ia, an d dem on st rated a
t ion , an d en dofibrosis of th e extern al iliac ar ter y. As su ch , care m ore th an t w ofold in creased risk of in term it ten t clau dicat ion in
m ust be taken to gath er a det ailed h istor y th at w ill en able th e m en age 70 w ith a tot al ch olesterol level at or above 240 m g/dL.12
pract it ion er to tease ou t clau dicat ion th at prim arily is of vascu - A m ild associat ion h as also been est ablish ed for p at ien t s w ith
lar origin . Th is ch apter focu ses on th e m edical an d su rgical t reat- hyperh om ocystein em ia.13
m en t of in term it ten t vascu logen ic claudicat ion .

■ Etiology and Pathogenesis


■ Epidemiology and Associated
Un iversal to all form s of PAD is th e deposit ion of ch olesterol in
Risk Factors th e ar terial w all an d th e even t u al form at ion of an ath erosclerot ic
It h as been previously repor ted th at 1 to 2% of pat ien ts younger plaqu e. Th e m ajorit y of th e clin ical m an ifest at ion s of PAD occu r
th an 50 years of age, 5% of th ose ages 50 to 70, an d 10% of th ose as a con sequ en ce of p rogressive at h erosclerot ic n ar row ing of
older th an 70 su ffer from in term it ten t clau dicat ion .1–3 In th e vessels. Th ere h ave been several suggested th eories of ath ero-
Fram ingh am Hear t St u dy, th e average rate of develop m ent of in - gen esis. Th e lipid hypoth esis put for th in th e m id-19th cen t ur y
term it ten t clau dicat ion over a 2-year period in part icipants over by Virch ow poin ts to ath erosclerosis as a react ive respon se to
th e age of 50 w as 0.7% in m en an d 0.4% in w om en .4 Th e Nat ion al lip id in filt rat ion .14 Th is w as in direct opposit ion to th e explan a-
Health and Nutrition Exam ination Sur vey (NHANES) interview ed t ion offered by Rokitan ksy,15 w h o suggested th at it w as th e de-
9,000 adults over th e age of 40 an d obt ain ed dem ograph ic an d gen erat ion of protein s such as fibrin w ith in th e ar terial w all th at
periph eral ar terial disease risk factor in form at ion . In addit ion , led to ath erom atou s lesion s. Su bsequ en t hyp oth eses focu sed on
an kle brach ial in dices (ABIs) w ere obtain ed for over 2,000 pa- sm ooth m u scle cell m igrat ion an d p roliferat ion along w ith con -
t ien ts. Th e overall p revalen ce of periph eral ar terial disease (ABI n ect ive t issue product ion as a “respon se to injur y” leading to
< 0.9) w as 4.3%. Sim ilar to previou s st udies, th e prevalen ce sig- ath erosclerosis. Com m on to all of th e above th eories is recogn i-
n ifican tly in creased w ith age. St u dy par t icipan ts bet w een th e t ion of th e dyn am ic n at u re of p laqu e form at ion , w h ich in clu des
ages of 40 an d 50 h ad a less th an 1% ch an ce of h aving an abn or- progression , regression , r u pt ure, erosion , an d u lcerat ion . In m ost
m al ABI, w h ereas th ose 70 or older h ad a 14.5% ch an ce.5 sit u at ion s, th e evolu t ion of ath erosclerot ic lesion s sp an s m any
Seve ral con d it ion s h ave b e e n est ab lish e d as r isk factor s years. Th e devast at ing effect s of su dden p laqu e ch anges can n ot
for t h e d evelop m e n t of p e r ip h e ral ar te r ial d isease. Cole an d be overlooked as m anifested by m yocardial infarctions, acute lim b
colleagu es 6 d e m on st rate d a 7-fold in crease d r isk of d evelop - isch em ia, isch em ic st roke, and acu te m esen teric isch em ia. Our
in g PAD in ex-sm okers com p ared w it h su bject s w h o h ad n ever understanding of atherosclerotic plaque is still evolving. The spe-
sm oked. Not surprisingly, it h as been est im ated th at upw ard of cialist w ho cares for patients w ith any form of claudication should
90% of pat ien t s referred to a vascular specialist h ave a h istor y of be fam iliar w ith th e n at ural histor y of lesion s w h en m aking deci-
sm oking.7 Fu r th er in form at ion obt ain ed from th e Fram ingh am sion s about th e best m edical or su rgical t reat m en t .

385

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386 III Ischemic Stroke and Vascular Insufficiency

ruling out oth er con dit ion s, an d aid in th e assessm en t of th e pa-


■ Clinical Presentation t ien t as a “good” or “bad” su rgical can didate. Par t icu lar at ten t ion
Patients w ith interm ittent vasculogenic claudication t ypically de- sh ou ld be p aid to th e p u lse exam on ever y p at ien t . Th e p resen ce,
scribe th eir pain as a sen sat ion of calf m u scle cram p s or fat igu e. st rength , an d ch aracter of a pat ien t’s p u lse sh ou ld be clearly doc-
Dep en ding on th e level of disease, som e p at ien t s m ay repor t u m en ted. Tradit ion ally, th e st rength of th e pu lse can be graded
bu t tock or t h igh p ain . Gen erally sp eaking, sym ptom s are exp e- on a scale from 0 to 3, in w h ich 0 represen ts an absen t pulse, 1
r ien ced w ith progressive am bu lat ion an d th ey abate w ith rest . represen t s a dim in ish ed pulse, 2 represen t s a n orm al pulse, an d
Th e dist an ce of “p ain -free” am bu lat ion is qu ite p redict able an d 3 represen ts a “boun ding” or abn orm ally prom in en t pu lse. Pulse
rep roducible. In t r ying to delin eate vascu lar clau dican t s from palp at ion , h ow ever, is su bject ive an d p redisp osed to error. W h en
sym ptom s cau sed by oth er con dit ion s, it is im por t an t to elicit a pu lses are n ot easily palp able, a h an d-h eld Dop pler can be u sed
detailed pat ien t h istor y focu sed on th e fin er p oin ts of th e pa- in th e clin ic to object ively assess blood flow, especially w h en
t ien t’s low er ext rem it y pain . In 2003, th e Tran sAtlan t ic In ter- an kle blood pressures are m easured .
Societ y Con sen su s pu blish ed a list of qu est ion s th at sh ou ld be
in clu ded in t h e in it ial evalu at ion of all pat ien t s w ith susp ected
interm it tent claudication.16 In addition , a com plete histor y sh ould
in clu de in form at ion regarding th e pat ien t’s oth er m edical prob -
lem s, w h ich w ill h igh ligh t poten t ial risk factors th at m ay p redis-
■ Diagnosis and Preoperative Evaluation
pose patients to PAD. Review ing the patient’s current m edications Th e vascu lar laborator y can provide u sefu l diagn ost ic in form a-
enables the practitioner to evaluate w hether or not optim al m edi- t ion regarding low er ext rem it y blood flow. Th e ABI is obtain ed
cal m an agem en t h as already been ach ieved. Fu r th erm ore, it is by dividing th e systolic pressure at th e an kle by th at of th e arm .
crucial to get a sen se h ow m uch of an im pact th e sym ptom s h ave Norm al ABIs range from 1.0 to 1.2 (Fig. 31.1). Pat ien t s w ith clau-
h ad on th e pat ien t’s qu alit y of life. All of th e above queries sh ou ld dicat ion u su ally h ave an ABI of less th an 0.9, an d pat ien ts w ith
en able t h e vascu lar sp ecialist n ot on ly to accu rately d iagn ose t issu e loss w ill h ave an ABI of less th an 0.5. An ABI of less th an
in term it ten t claudicat ion but also to iden t ify pat ien t s w h o are 0.3 suggest s crit ical lim b isch em ia an d w arran ts urgen t evalu a-
can didates for su rgical in ter ven t ion . t ion an d in ter ven t ion . Of n ote, p at ien ts w ith diabetes m ay h ave a
Pat ien t s sh ou ld receive a fu ll h ead-to-toe p hysical exam in a- falsely elevated ABI secon dar y to m edial calcin osis of th e sm all
t ion w h en being evalu ated for clau dicat ion . Vit als m u st be t aken vessels of t h e low er leg. In su ch p at ien t s, a toe brach ial in d ex
an d sh ould in clude a blood pressure reading from both arm s. sh ou ld be obt ain ed . In p at ien t s w it h sym ptom s t h at are d isp ro-
Physical exam fin dings su ch as dim in ish ed sen sat ion in th e fin - p or t ion ate to t h e exam fin d ings (i.e., p alp able p u lses, n or m al
gers an d toes, pulsat ile abdom in al m ass, or sign ifican t w h eezing rest ing ABI), exercise test ing m ay be u sefu l.17 Th is is ach ieved by
w ill suggest th e presen ce an d exten t of com orbidit ies, facilitate com p ar ing th e p at ien t’s rest ing ABI to th e ABI after w alking a

Fig. 31.1 Norm al resting ankle-brachial index (ABI)


dem onstrating m ultiphasic Doppler waveform s.

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31 Medical, Surgical, and Endovascular Treatment of Claudication 387

t readm ill t yp ically at 3.5 km /h at a 12% in clin e an d exp erien cing p lan e, is t rian gu lar an d n arrow est in it s an terop oster ior diam e-
claudication-like sym ptom s. An ABI decrease of 20%or m ore t yp - ter.26 Th e an terop osterior diam eter h as been est im ated to range
ically in dicates th e p resen ce of vascu lar clau dicat ion .18 If th ere is from 15 to 23 m m .27 Th e borders of t h e sp in al can al are as fol-
lit tle to n o decrease, an oth er disease process is m ore likely. low s: an ter iorly by th e p oster ior edge of t h e ver tebral body;
On ce a diagn osis is m ade, im aging m ay be p u rsu ed to fu r th er laterally by th e pedicles, facet join ts, an d ar t icular capsules; an d
clar ify t h e exten t of d isease an d for t h e p u r p oses of su rgical posteriorly by th e lam in a an d ligam en t a flava.26 Th e am ou n t of
p lan n ing. For m al d u p lex u lt rasou n d w it h segm en t al ar ter ial space in th e lum bar spin al can al an d foram in a is prim arily deter-
w aveform an alysis is ext rem ely h elpfu l in d eterm in ing th e de- m in ed by developm en tal variat ion s an d degen erat ive ch anges.25
gree an d locat ion of sten osis. Du plex im aging, h ow ever, is opera- Oth er cau ses in clude local in fect ion , t raum a, or iat rogen ic causes
tor depen den t an d often n ot as readily available as oth er im aging su ch as p rior su rgical in ter ven t ion in th is region . From an em -
m odalit ies. In addit ion , th ese st u dies can be difficu lt to in terpret br yological stan dpoin t , grow th of th e lum bar ver tebrae begin s
in p at ien t s w h o are obese or ed em atou s, or in t h ose w it h ex- after th e seven th w eek of gest at ion . It is at th is st age th at t w o
ten sive ar ter ial w all calcificat ion , w h ich can cau se sh ad ow ing ch on drificat ion cen ters form in each ver tebral arch .28,29 It is n ot
ar t ifacts. u n t il several years after birth th at th e n at ural process of bon e
Tradit ion al diagn ost ic angiography can be p erform ed to de- form at ion an d bony u n ion of th e cen t ru m w ith its n eural arch
lin eate fu r th er th e exten t of disease, an d it h as th e advan tage of is com plete.30
providing access for im m ediate percutaneous endovascular treat- Com prom ise of n eu ral com p on en ts can occu r as a resu lt of
m en t of focal occlu sive disease. Angiography, h ow ever, en tails a progressive hyper t rop hy of surroun ding bony, car t ilagin ous, an d
h igh er r isk of m orbid it y an d m or t alit y t h an d o ot h er im agin g ligam en tou s elem en t s. In ad dit ion , t h e n u cleu s p u lp osu s an d
m odalit ies. Th e r isks of sign ifican t con t rast m ed iu m react ion , an n u lu s fibrosu s of th e in ter ver tebral disks can r u pt u re an d h er-
m ort alit y, an d com plicat ion n egat ively affect ing plan n ed th er- n iate posteriorly to cause com pression . It is w or th w h ile to also
apy are 0.1%, 0.16%, an d 0.7%, respect ively.19 Recen t advan ces in poin t ou t th e term in al en d of th e spin al cord, th e con u s m edu l-
im aging tech n ology h ave m ade com pu ted tom ography angiogra- laris, t ypically en ds at th e level of L1 an d L2 in n orm al adu lt s. Just
phy (CTA) an d m agn et ic reson an ce angiography (MRA) less inva- below it , th e root s of th e cauda equin a are con tain ed w ith in th e
sive m eth ods of determ in ing th e exten t of aor t ic, iliac, an d distal su barach n oid space of t h e t h ecal sac. As su ch , LSS resu lt s in
occlusive ch anges. CTA is faster, requ ires less pat ien t coopera- n er ve root dysfu n ct ion as op posed to spin al cord dysfu n ct ion .26
t ion , an d offers h igh er resolu t ion th an MRA. In th e average adu lt , Mu lt ip le classificat ion sch em es h ave been devised for LSS,
h ow ever, rough ly 100 m L of iodin ated con t rast is often n ecessar y given th e n um erous poten t ial et iologies. Th e sim plest an d m ost
to com plete a CTA th at in cludes th e abdom en , pelvis, an d bilat- in t uit ive sch em e divides et iologies in to congen it al an d acquired
eral low er ext rem it ies. Th is st u dy, th erefore, sh ou ld be lim ited to causes. Congen it al form s of lu m bar sten osis are m u ch less com -
in dividu als w ith n orm al ren al fu n ct ion or in th ose for w h om th e m on . Th is d isease p rocess w as first d escr ibed in ch ild ren by
ben efit ou t w eigh s th e risk. In m any in st it ut ion s, ren al protect ion Sar pyen er an d later in adu lt s by Verbiest . Sh or t th ick p edicles,
p rotocols h ave been est ablish ed t h at in cor p orate in t raven ou s t h icken ed lam in a an d facet s, or excessive scoliot ic or lord ot ic
flu id , sod iu m bicarbon ate, an d acet ylcystein e ad m in ist rat ion . cu r ves are seen in p at ien t s w it h a congen it al cau se of lu m bar
With respect to MRAs, th e pract it ion er m ust keep in m in d th at sten osis.26 In gen eral, th ese an atom ic ch anges on ly becom e clin i-
often pat ien ts w ith m etal im plan t s can n ot be con sidered. In ad- cally sign ifican t w h en accom p an ied by a space-occupying lesion
dit ion , in dividu als w ith severe clau st roph obia m ay requ ire seda- su ch as a h er n iated d isk lead ing to fu r t h er com p ression .26 In
t ion , w h ich en tails its ow n risks. p at ien t s w ith ach on droplast ic dw arfism , developm en tal steno-
sis of th e en t ire sp in al can al is seen , stem m ing from prem at ure
cessat ion of th e grow th of th e paired ver tebral body an d dorso-
lateral n eu ral arch ossificat ion cen ters.31,32 In th ese pat ien ts, an -
teroposterior an d lateral sten osis of th e can al results, leading to
■ Differential Diagnosis progressive com pression of th e spin al cord an d cau da equ in a as
Several oth er disease processes can m im ic in term it ten t clau dica- th ese pat ien t s age.33
t ion .20 Perh ap s th e m ost difficu lt to differen t iate is n eu rogen ic For m ost in d ivid u als w ith LSS, acqu ired d egen erat ive or ar-
clau dicat ion (NC), w h ich is t radit ion ally defin ed as th e classic t h rit ic ch an ges are t h e cau se. Th e an atom ic ch an ges m ost often
clin ical p resen t at ion of lu m bar sp in al sten osis (LSS), a degen era- seen in clu d e hyp er t rop hy of t h e ar t icu lat ion s su r rou n d in g t h e
t ive disease p rocess p rim arily affect ing older adu lt s.21,22 Th ough can al, in ter ver tebral disk h ern iat ion , hyp er t rop hy of th e liga-
it is difficult to determ in e th e prevalen ce of LSS, w ith up to 90% m entum flavum , and osteophyte form ation.26 Degenerative spon-
of th e Un ited States populat ion experien cing low er back pain at dylosis is t yp ically associated w it h hyp er plasia, fibrosis, an d
som e p oin t in th eir life,23 th is is a m edical con dit ion th at can n ot car t ilagin ou s m et ap lasia of th e an n u lu s, p osterior longit u din al
be overlooked. With respect to h ealth care dollars an d lost t im e ligam en t , an d ligam en t u m flavum .25 An in crease in ligam en t um
from w ork, th e fin an cial im pact is st ar t ling.24 In LSS a n arrow ing flavu m t h ickn ess to 5 to 10 m m can be seen , w h ich in m any
of th e n eural can al an d foram in a occurs th at su bsequen tly leads p at ien t s is th e prim ar y cause of lum bar sten osis.28 With degen -
to com pression of th e lum bosacral n er ve roots or cau da equ in a.25 erat ive sp on dylolisth esis th ere is n o n eu ral arch defect th at can
Clin ically th is can m an ifest as back pain or low er ext rem it y fa- su bsequ en tly lead to can al sten osis. Posterior ligam en tou s an d
t igu e, pain , w eakn ess, an d n um bn ess. facet hyper t rophy is seen , w h ich in som e cases can lead to com -
To successfu lly t reat NC, an in -depth un derstan ding of th e plete m yelograph ic block.25
anatom ic relationship of structures w ithin the spinal canal is nec- Micro -in st abilit y at t h e ar t icu lar su r face, or t h e p rocess of
essar y.26 Th e lum bar vertebral can al, w h en view ed in th e axial sm all rep et it ive m ovem en t s of t h e join t s cau sing p rogressive

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388 III Ischemic Stroke and Vascular Insufficiency

arch itect ural ch anges in th e an atom y leading to n arrow ing of th e


lu m bar sp in al can al, h as been lin ked to LSS.34 Wilson 35 classified
■ Open Versus Endovascular
NC in to post u ral versu s isch em ic form s. In p ost u ral NC, th ere is a Intervention
t ran sien t p rot ru sion of com p on en ts (d egen erated in ter ver tebral
Pat ien ts w ith claudicat ion w h o do n ot resp on d to m edical m an -
disks an d th icken ed ligam en t flava) p osteriorly, w ith exten sion
agem en t alon e m ay be can d idates for revascu larizat ion . W h en
of th e spin e, w h ich causes sym ptom s. Altern at ively in th e isch -
th e decision is m ade to m ove for w ard w ith revascu larizat ion , it
em ic varian t , brief isch em ia of t h e lu m bar n er ve vascu lat u re is
is im port an t to w eigh th e risks of t h e p rocedure, w h eth er it be
in du ced w h en oxygen dem an d in creases du ring am bu lat ion .
open or en dovascular, again st th e degree of im provem en t th at
Th ough m u ch less com m on , ot h er acqu ired con d it ion s as-
is an t icipated. A clear dist in ct ion sh ou ld be m ade bet w een clau-
sociated w ith LSS in clude hyperparathyroidism , Paget’s disease,
dican t s an d th ose w ith crit ical lim b isch em ia. For clau dican ts,
an kylosing spon dylit is, Cu sh ing’s disease, acrom egaly, disk-space
in ter ven t ion sh ould on ly be pu rsu ed if th eir sym ptom s sign ifi-
in fect ion , osteom yelit is, Pot t’s disease, surgical procedures (lam -
can tly in terfere w ith th eir lifest yle. For exam p le, if a p at ien t is
in ectom y or spin al fu sion ), t rau m a, rh eum atoid arth rit is, pseu-
severely disabled, can n ot perform act ivit ies of daily living, or
dogou t , an d ren al osteodyst rop hy.36–46
can n ot w ork, th en revascularizat ion sh ou ld be con sidered.
Th e t yp ical op en op erat ion s for clau d icat ion d ep en d on t h e
level of ar ter ial blockage. You ng sm okers w h o d evelop classic
proxim al aor toiliac occlu sive disease w ith h igh -grade sten oses
■ Medical Management or occlu sion s are can d idates for aor tofem oral byp ass. Th is op -
Patien ts w ith in term it ten t vasculogen ic clau dication sh ould h ave erat ion involves an open abdom in al explorat ion , eith er t ran s-
a com preh en sive m edical t reat m en t plan aim ed at aggressive risk periton eal or ret rop eriton eal, an d clam ping of th e in fraren al or
factor reduct ion . An t iplatelet th erapy con t in ues to be th e m ain - su p raren al aor ta. En d–side or en d–en d an astom oses can be cre-
st ay of cardiovascu lar risk redu ct ion . Sm oking h as been sh ow n ated to est ablish in flow, an d ou tflow is t yp ically at th e level of
to in crease th e in ciden ce of death du e to coron ar y ar ter y disease the fem oral bifurcations. Long-term results from th ese operations
an d poten t iates graft failure follow ing low er ext rem it y revascu - are excellen t in term s of relief of sym ptom s an d w oun d h ealing.
larizat ion .47,48 As su ch , sign ifican t em ph asis sh ou ld be p laced on Morbidit y rates from open su rger y are in th e range of 2 to 6%,
sm oking cessat ion . With resp ect to hyp erlipid em ia, all pat ien ts w it h p ossible com p licat ion s in clu d ing m yocard ial in farct ion ,
w ith in term it ten t claudicat ion sh ould be placed on a stat in , w ith bleeding, w ou n d in fect ion s, graft in fect ion or th rom bosis, an d
a low -den sit y lipoprotein goal of less th an 100 m g/dL. In pat ien t s lim b loss. In pat ien ts w h o are too elderly or too frail to u n dergo
w ith ot h er card iovascu lar r isk factors su ch as coron ar y ar ter y open abdom in al explorat ion , th e axillar y ar ter y provides a use-
disease, a goal of less t h an 70 m g/d L sh ou ld be set . Ot h er goals fu l in flow for th e fem oral arteries. Th e so-called axillofem oral
sh ou ld in clu de in creased exercise, w eigh t loss, blood p ressu re bypass is t ypically ch osen on th e side w ith th e h igh er arm blood
con t rol, an d t igh t glu cose con t rol for th ose w ith diabetes. pressu re, an d th en a fem oral–fem oral crossover graft is also im -
A st rictly super vised exercise regim en h as been foun d to be plan ted. Th e risk of cardiopu lm on ar y m orbidit y is low er sim p ly
the on ly con sistent therapy th at increases the pain -free and m axi- becau se open ing th e abdom en is un n ecessar y. Careful graft su r-
m al w alking distan ce.49 Th e Am erican Hear t Associat ion recom - veillan ce after bypass w ith duplex ult rasoun d is an im por tan t
m en ds w alking 30 to 45 m in u tes p er session th ree to fou r t im es adjun ct to m ain tain long-term paten cy of graft s. Th e 5-year pa-
a w eek for at least 12 w eeks. Pat ien ts sh ould w alk un t il th eir pain ten cy rates for both of th ese t ypes of recon st ruct ion s described
is proh ibit ive, rest u n t il pain relief is ach ieved, an d th en con t in u e are over 80%, an d pat ien ts can be expected to enjoy long periods
w alking.20 Th ough foun d to be efficacious, th is st rategy is often of freedom from rein ter ven t ion for open recon st r uct ion . Syn -
lim ited by poor patient com pliance. Num erous studies have looked th et ic graft is m ost often u sed for th ese recon st ruct ion s.
at variou s m edicat ion s for th e t reat m en t of clau dicat ion , all w ith If th e occlu sive disease in th e vascular claudican t is located in
con flict ing an d often sh or t-term su ccess. Pen toxifyllin e w as th e th e fem oral region , as is often seen in sm okers, diabet ics, an d th e
first Food an d Dr ug Adm in ist rat ion (FDA)-approved m edicat ion elderly, th en th e t ypical open operat ion con sists of fem oral en d-
used in th e t reat m en t of clau dicat ion . Th is m edicat ion is a m eth - ar terectom y an d patch angioplast y of th e vessel. Th e operat ion
ylxan t h in e d er ivat ive believed to low er blood viscosit y an d in - th u s rem oves th e p laqu e, an d th e patch is p laced to w iden th e
h ibit p latelet aggregat ion . St u d ies h ave sh ow n a st at ist ically vessel. Th is operat ion is w ell tolerated, as it is often perform ed
sign ifican t im provem en t in m axim al w alking dist an ce w ith th e in th e groin on ly, an d th e risks of su rger y are m ain ly related to
use of p en toxifyllin e.50 Th e clin ical sign ifican ce, h ow ever, h as w ou n d-h ealing issu es. Paten cy rates of over 70% at 5 years are
been h arder to iden t ify. Altern at ively, cilost azol, a p h osph odies- exp ected for th ese t ypes of recon st ru ct ion s, an d often requ ire
terase in h ibitor th at w orks by in h ibit ing sm ooth m uscle cell con - exten sion of th e recon st ru ct ion d ow n to first- or secon d-ord er
t ract ion an d p latelet aggregat ion , w as FDA ap p roved in 1999. bran ch es of th e deep fem oral system . Fin ally, claudican ts w h o
Addit ion al effects in clu de a reduct ion in sm ooth m u scle cell pro- h ave superficial fem oral disease can un dergo classic fem oral–
liferat ion an d ser u m t riglycer id es w h ile in creasing p rotect ive pop liteal byp ass if th e clau dicat ion is lifest yle lim it ing. Gen eral
h igh -den sit y lipoprotein levels. Barn et t an d colleagues 51 dem on - prin cip les dict ate th at th e vein h as m u ch bet ter p aten cy rates
st rated a 50% in crease in m axim al w alking dist an ce along w ith over prosth et ic bypasses, t ypically a 5-year paten cy of 60% ver-
im provem en t in qu alit y of life. Alth ough resu lts w ith th ese m ed- su s 30 to 40%for below -kn ee bypasses. With th e adven t of en do-
icat ion s are variable, a t rial of 6 to 8 w eeks of th erapy shou ld be vascu lar in ter ven t ion s an d less invasive tech n iques, th e overall
at tem pted along w ith th e exercise regim en . Th e m ajor con t rain - volum e of low er ext rem it y bypasses for clau dicat ion h as been
dicat ion to cilostazol is congest ive h ear t failure. declin ing in th e p ast decad e.

Neurosurgery Books Full


31 Medical, Surgical, and Endovascular Treatment of Claudication 389
Fig . 31.2a– c Endovascular reintervention for fem oral
artery stenosis. (a) Anteroposterior (AP) angiogram dem -
onstrates restenosis at the proxim al left superficial femo-
ral artery after stenting. (b) AP angiogram dem onstrates
balloon angioplast y at the site of stenosis. (c) Completion
AP angiogram following angioplast y.

a b c

En dovascu lar in ter ven t ion s of th e low er ext rem it ies t yp ically
in clude angioplast y, sten t ing, or ath erectom y. Th ese procedu res
■ Conclusion
are m ost successful in cases involving sh or t sten oses of th e iliac Clau dicat ion is a m ult ifactorial, disabling, an d ch allenging prob -
ar teries, w ith 5-year paten cies equivalen t to th ose of open aor to- lem for the specialist to treat. Clearly delineating neurogenic from
fem oral bypass—greater than 80%. As the disease enters the m ore vascu logen ic claudicat ion is of param ou n t im por tan ce prior to
distal vessels, th ere is a sign ifican t decrease in th e d u rabilit y of proceeding w ith any in ter ven t ion . Neu rogen ic clau dicat ion often
t radit ion al angiop last y an d sten t ing, an d th e lack of clear gu ide- is w orse in th e m orn ing, im proves w ith am bu lat ion , an d is re-
lines for best procedures for certain patients leaves vascular clau- lieved in cer tain p osit ion s. Rep air often requ ires decom pression
dicat ion as on e of th e m ore ch allenging diseases to t reat . Fu t u re of com pressed n er ve roots or region s in th e lum bosacral an at-
im provem ents in the technology and developm ents such as drug- om y th at are m alalign ed. Vascu lar claudicat ion is a problem of
elut ing sten t s m ay im prove fu t u re u se of en dovascu lar in ter ven - m uscle isch em ia, an d get s w orse w ith act ivit y, im p roves w ith
t ion s in th e low er ext rem it ies in th e search for th e m ost du rable, rest , an d can progress to gangren e, rest p ain , an d t issue loss if
cost-effect ive t reat m en t opt ion . As w ith op en su rgical revascu - ign ored. Procedu res to im prove vascular flow can be divided in to
larizat ion , th e im por t an ce of long-term su r veillan ce w ith du plex t radit ion al open su rgical recon st r u ct ion s or m in im ally invasive
ult rasou n d facilitates rein ter ven t ion (Fig. 31.2) w h en resten osis en dovascu lar angioplast y or sten t ing. Deciding on w h ich t ype of
occurs. In con t rast to failed su rgical revascularizat ion , failed en - procedu re is best for w h ich lesion rem ain s a vexing p roblem in
dovascu lar revascu larizat ion s can lead to w orsen ed an d m ore th e vascu lar su rger y com m u n it y, an d is in flu en ced greatly by
acute lim b isch em ia. Alth ough percut an eous m eth ods appear to p at ien t p referen ces, availabilit y of n at ive con du it s, an d local ex-
be less invasive, th ey are clearly n ot less risky, an d ideally sh ould p er t ise w it h less invasive tech n iqu es. Overall, t h e d ist in ct ion
be perform ed by vascular specialists dedicated to caring for all of n eurogen ic from vascular claudicat ion is key to direct ing th e
aspect s of p at ien t s w ith low er ext rem it y occlu sive d isease. m ost opt im al th erapy for th ese sym ptom at ic pat ien ts.

References
1. Criqui MH, Fron ek A, Barret t- Con n or E, Klauber MR, Gabriel S, Goodm an 8. Kan n el W B, McGee DL. Diabetes an d cardiovascular disease. Th e Fram ing-
D. Th e prevalen ce of p erip h eral ar terial d isease in a defin ed p op u lat ion . h am st udy. JAMA 1979;241:2035–2038
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t ion . In t Angiol 1992;11:218–229 riph eral ar terial disease an d risk factors in person s aged 60 an d older:
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m it ten t claudicat ion: th e Fram ingh am St udy. J Am Geriat r Soc 1985;33: 2004. J Am Geriat r Soc 2007;55:583–589
13–18 12. Murabito JM, D’Agost in o RB, Silbersh at z H, Wilson W F. In term it ten t clau-
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Exam in ation Survey, 1999–2000. Circulation 2004;110:738–743 13. Darius H, Pittrow D, Haberl R, et al. Are elevated hom ocysteine plasm a levels
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occlusive disease. Surgery 1993;114:753–756, discussion 756–757 of 6880 prim ar y care pat ien t s. Eur J Clin Invest 2003;33:751–757
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15. Rokit an sky C. A Man ual of Pathological An atom y. Lon don : Syden ham So- 30. Angevin e JB Jr. Clin ically relevant em br yology of th e ver tebral colum n an d
ciet y; 1852 spin al cord. Clin Neurosurg 1973;20:95–113
16. Dorm andy JA, Ruth erford RB. Managem en t of periph eral ar terial disease 31. Morgan DF, Young RF. Spin al n eurological com plicat ion s of ach on dropla-
(PAD). TASC Working Group. TransAtlantic Inter-Societ y Consensus (TASC). sia. Result s of surgical t reat m en t . J Neurosurg 1980;52:463–472
J Vasc Su rg 2000;31(1 Pt 2):S1–S296 32. Don at h J, Vogal A. Un tersu ch u ngen u ber d en ch on drodyst rop h isch en
17. Gah t an V. Th e n on invasive vascular laborator y. Surg Clin Nor th Am Zw erguch s. Gesam te Neu rol Psych iat r y 1927;111:333–335
1998;78:507–518 33. Epstein JA, Malis LI. Com pression of spin al cord an d cauda equin a in
18. Nordn ess PJ, Mon ey SR. Evalu at ion of clau d icat ion . In Man sou r, MA, ach on drop last ic dw arfs. Neu rology 1955;5:875–881
Labrop ou los, N, ed s. Vascu lar Diagn osis. Ph ilad elp h ia: Sau n d ers; 2005: 34. Jan e JA Sr, Jan e JA Jr, Helm GA, et al. Acquired lum bar spin al sten osis. Clin
207–214 Neurosu rg 1996;43:275–299
19. Bet t m an n MA, Heeren T, Green field A, Goudey C. Adverse even t s w ith 35. Wilson CB. Sign ifican ce of th e sm all lum bar spin al can al: cau da equin a
radiograph ic cont rast agen t s: result s of th e SCVIR Con t rast Agen t Regis- com pression syn drom es due to spon dylosis. 3: In term it ten t claudicat ion .
t r y. Radiology 1997;203:611–620 J Neu rosu rg 1969;31:499–506
20. Hirsch AT, Haskal ZJ, Her t zer NR, et al; Am erican Associat ion for Vascular 36. Wein stein P. Lum bar disc disease. In: Hardy RW Jr, ed. Lum bar Disc Dis-
Su rger y; Societ y for Vascu lar Su rger y; Societ y for Card iovascu lar An gi- ease. New York: Raven ; 1982:257–276
ography and In ter ven t ion s; Societ y for Vascular Medicin e an d Biology; 37. Grabias S. Curren t con cept s review. Th e t reat m ent of spin al sten osis.
Societ y of In ter ven t ion al Radiology; ACC/AHA Task Force on Pract ice J Bon e Join t Su rg Am 1980;62:308–313
Guidelin es; Am erican Associat ion of Cardiovascu lar an d Pulm on ar y Re- 38. Hasue M, Kikuch i S, In oue K, Miura H. Post t rau m at ic spin al sten osis of th e
habilitation; Nation al Heart, Lung, and Blood In stit ute; Societ y for Vascular lum bar spin e: repor t of a case caused by hyperexten sion injur y; review of
Nu rsing; Tran sAtlan t ic In ter-Societ y Con sen su s; Vascu lar Disease Fou n - literat ure. Spin e 1980;5:259–263
dat ion . ACC/AHA 2005 guidelin es for th e m an agem en t of pat ient s w ith 39. Weisz GM. Lum bar spin al can al sten osis in Paget’s disease. Spin e 1983;
peripheral arterial disease (low er extrem it y, renal, m esenteric, and abdom - 8:192–198
inal aortic): executive sum m ar y a collaborative report from the Am erican 40. Wein stein PR, Karpm an RR, Gall EP, Pit t M. Spin al cord injur y, spin al frac-
Associat ion for Vascular Surger y/Societ y for Vascular Surger y, Societ y for t ure, an d spin al sten osis in an kylosing spon dylit is. J Neurosurg 1982;57:
Cardiovascu lar Angiograp hy an d In ter ven t ion s, Societ y for Vascu lar Med- 609–616
icine an d Biology, Societ y of In ter vent ion al Radiology, an d th e ACC/AHA 41. Luken MG III, Patel DV, Ellm an MH. Sym ptom atic spinal stenosis associated
Task Force on Pract ice Guidelin es (Writ ing Com m it tee to Develop Guide- w ith an kylosing spon dylit is. Neurosurger y 1982;11:703–705
lines for th e Man agem en t of Pat ien t s With Periph eral Arterial Disease) 42. Karpm an RR, Wein stein PR, Gall EP, Joh n son PC. Lu m bar spin al sten osis in
en dorsed by th e Am erican Associat ion of Cardiovascular and Pulm on ar y a p at ien t w ith diffu se idiopath ic skelet al hyper t rop hy syn drom e. Sp in e
Reh abilit at ion ; Nat ion al Hear t , Lu ng, an d Blood In st it u te; Societ y for Vas- 1982;7:598–603
cular Nursing; Tran sAtlan t ic In ter-Societ y Con sensu s; an d Vascu lar Dis- 43. Magn aes B, Hauge T. Rheu m atoid ar th rit is con t ribut ing to lum bar spin al
ease Fou n dat ion . J Am Coll Cardiol 2006;47:1239–1312 sten osis. Neu rogen ic in term it ten t clau dicat ion . Scan d J Rh eu m atol 1978;
21. Verbiest H. Ch apter 16. Neu rogen ic in term it ten t claudicat ion in cases 7:215–218
w ith absolute an d relat ive sten osis of th e lum bar ver tebral can al (ASLC 44. Epstein N, W h elan M, Benjam in V. Acrom egaly an d spin al sten osis. Case
an d RSLC), in cases w ith n arrow lu m bar in ter ver tebral foram in a, an d in report . J Neurosurg 1982;56:145–147
cases w ith both en t it ies. Clin Neurosurg 1973;20:204–214 45. Morelan d LW, López-Mén dez A, Alarcón GS. Spin al stenosis: a com pre-
22. Boden SD, Davis DO, Din a TS, Pat ron as NJ, Wiesel SW. Abn orm al m ag- hensive review of the literat ure. Sem in Arthritis Rh eum 1989;19:127–149
n et ic-reson an ce scan s of th e lum bar spin e in asym ptom at ic subject s. A 46. Lipson SJ, Nah eedy MH, Kaplan MM, Bien fang DC. Spin al sten osis caused
prosp ect ive invest igat ion . J Bon e Join t Su rg Am 1990;72:403–408 by epidural lipom atosis in cush ing’s syn drom e. N Engl J Med 1980;302:36
23. Wein stein P. Lum bar sten osis. In : Hardy RW Jr, ed. Lu m bar Disc Disease, 47. Kabir Z, Con n olly GN, Clan cy L, Koh HK, Capew ell S. Coron ar y h ear t dis-
2nd ed. New York: Raven ; 1993:241–255 ease death s an d decreased sm oking p revalen ce in Massach u set t s, 1993–
24. Rober t s M. Com plicat ion s of lum bar disc surger y. In : Hardy RW Jr, ed. 2003. Am J Public Health 2008;98:1468–1469
Lum bar Disc Disease, 2n d ed. New York: Raven ; 1993:161–169 48. Willigen dael EM, Teijink JA, Bartelink ML, Peters RJ, Bü ller HR, Prins MH.
25. Ciricillo SF, Wein stein PR. Lum bar spin al sten osis. West J Med 1993;158: Sm okin g an d t h e p aten cy of low er ext rem it y byp ass graft s: a m et a-
171–177 an alysis. J Vasc Surg 2005;42:67–74
26. Alvarez JA, Hardy RH Jr. Lum bar spin e sten osis: a com m on cause of back 49. Gardn er AW, Poeh lm an ET. Exercise reh abilitat ion program s for th e t reat-
an d leg pain . Am Fam Physician 1998;57:1825–1834, 1839–1840 m en t of clau d icat ion p ain . A m et a-an alysis. JAMA 1995;274:975–980
27. Wein stein P. Anatom y of th e lum bar spin e. In : Hardy RW Jr, ed. Lum bar 50. Por ter JM, Cutler BS, Lee BY, et al. Pen toxifylline efficacy in th e t reat m en t
Disc Disease, 2n d ed. New York: Raven ; 1993:5–13 of in term it ten t claudicat ion: m ult icen ter con t rolled double-blin d t rial
28. Wein stein PR. Th e applicat ion of an atom y an d path ophysiology in th e w ith object ive assessm ent of chron ic occlusive ar terial disease pat ien t s.
m an agem en t of lum bar spin e disease. Clin Neurosu rg 1980;27:517–540 Am Heart J 1982;104:66–72
29. Epstein BS, Epstein JA, Lavin e L. Th e effect of an atom ic variat ion s in the 51. Barn et t AH, Bradbur y AW, Brit ten den J, et al. Th e role of cilost azol in th e
lum bar vertebrae an d spin al can al on cauda equin a an d ner ve root syn - t reat m en t of in term it ten t clau dicat ion . Curr Med Res Opin 2004;20:
drom es. Am J Roen tgen ol Radiu m Th er Nu cl Med 1964;91:1055–1063 1661–1670

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32 Medical, Surgical, and Endovascular
Treatment of Arterial Injury
Benjam in D. Fox and Adam S. Arthur

occur in th e t un ica m edia an d can lead to n arrow ing or occlusion


■ Relevant Anatomy and of th e vessel lum en .
Pathophysiology Alth ough n ot fully u n derstood , ext racran ial SADs likely result
from a com bin at ion of m in or t rau m a an d an u n derlying in h eren t
Cerebrovascu lar ar terial inju ries are often en cou n tered by n eu ro
st ru ct u ral abn orm alit y in th e ar terial w all. Th ere is an associa
surgeons, neurologists, traum a surgeons, and in ter ventional neu
t ion bet w een ext racran ial SAD an d con n ect ive t issu e d isord ers
roradiologists. Th ese vascular injuries can occur spon tan eously;
su ch as fibrom u scu lar dysp lasia, Mar fan’s syn d rom e, p olycyst ic
iat rogen ically follow ing percu tan eous, surgical, or en dovascular
kidn ey disease, α 1-an t it r ypsin deficien cy, osteogen esis im per-
procedu res; or as a resu lt of blu n t or p en et rat ing t rau m a to th e
fecta I, Eh lers Dan los syn drom e IV, an d cyst ic m edial n ecrosis.
h ead or n eck. Th ese injuries can in clude ar terial dissect ion , lac
Apar t from th ese system ic con n ect ive t issu e disord ers, skin bi
erat ion , avu lsion , th rom bosis, an d occlu sion . A cerebrovascu lar
opsies in pat ien ts w ith SADs h ave revealed oth er n on syn drom ic
inju r y (CVI) can occu r in t h e ext racran ial carot id or ver tebral
con n ect ive t issu e abn orm alit ies.1 Oth er poten t ial associated fac
ar teries or in t racran ially.
tors are in fect ion , in flam m at ion , an d a fam ily h istor y of spon t a
n eous dissect ion s. W h en pat ien t s w ith th ese in h eren t st ruct ural
abn orm alit ies are exposed to m inor t raum a or th e rapid m ot ion s
Spontaneous Cerebrovascular Injuries of sn eezing, cough ing, or t u rn ing on e’s h ead, th is com bin at ion is
Sp on t an eou s CVIs are prim arily ar terial dissect ion s, an d th ey th eorized to result in dissect ion .
occur m ore frequen tly in th e ext racran ial vessels. “Spon t an eous” In t racran ial ar teries differ an atom ically from ext racran ial ar
refers to th e absen ce of blu n t or p en et rat ing t rau m a. How ever, teries in several w ays. In t racran ial ar teries do n ot h ave an exter
spon tan eou s cer vical vascular inju ries are often repor ted follow n al elast ic lam in a, th e in tern al elast ic lam in a is m ore developed,
ing m in or or t rivial in ciden t s su ch as sn eezing, cough ing, t u rn ing an d th ere is less m edia an d advent it ia.1 In addit ion , in t racran ial
th e h ead , or after m in or t rau m a. It is est im ated th at th e an n u al vessels for th e m ost par t are float ing in th e su barach n oid space
in ciden ce of ext racran ial cerebrovascu lar spon t an eou s arterial an d do n ot h ave adjacen t con n ect ive t issue layers for suppor t .
dissect ion s (SADs) is th ree to five cases p er 100,000 p erson s, an d Th ese differen ces accou n t for t h e fact th at dissect ing an eu r ysm s
th ey occu r m ore com m on ly in th e in tern al carot id ar ter y (ICA) occur an d rupt ure (ext ravascular h em orrh age) m ore frequen tly
th an in th e ver tebral ar ter y (VA).1 In t racran ial SADs are m u ch in t racran ially th an ext racran ially. Sim ilar to ext racran ial SADs,
less frequ en t . A large ser ies d escr ibing cer vicocep h alic ar ter ial in t racran ial SADs are also th ough t to be related to un derlying
d issect ion s over a 10 year sp an rep or ted an in cid en ce of on ly vessel st r uct ural con dit ion s or defects as listed above. Oth er re
0.04% in t racran ial SADs.2 por ted associated con dit ion s or fin dings are in t racran ial ath ero
In gen eral, an ar terial d issect ion begin s w it h a d isr u pt ion , sclerosis, m u coid degen erat ion of th e t un ica m edia, h epat it is C,
tear, or d efect in on e or m ore of t h e ar ter ial vessel w all layers. m igraines, periarteritis nodosa, m oyam oya disease, Guillain Barré
Th ese d issect ion s are t yp ically classified an atom ically as su b syn d rom e, an d hyp er ten sion (sp ecifically w it h ver tebrobasilar
in t im al or su badven t it ial. A d isr u pt ion in t h e in t im a exp oses dissect ion s).1
in t ralu m in al blood to th e su bin t im al space (bet w een th e in t im a Ext racran ial SADs classically occu r in m obile segm en t s of th e
an d m edia) an d act ivates th e clot t ing cascade, w h ich can lead ICA an d VA, in th e ICA a few cen t im eters dist al to th e carot id bi
to th rom bus an d em bolu s form at ion . Th ese em boli can propel fu rcat ion , an d in th e secon d (foram en t ran sversarium ) an d th ird
dow n st ream an d resu lt in em bolic st rokes. In addit ion , as blood segm en t s (C1–C2) of th e VA. Th ese dissect ion s can exten d in to
is prop elled un der pressu re in to th e su badven t it ial sp ace, th is in t racran ial vessels in 10 to 17% of cases.1 In t racran ially, SADs
lam in ar flow can cau se progression of th e dissect ion , flap s, an d ten d to occur m ore frequ en tly in th e ver tebrobasilar system th an
in t ram ural h em atom as (Figs. 32.1 an d 32.2). Large dissect ion in th e an terior circu lat ion . In tot al, 54 to 76% of all in t racran ial
plan es, flaps, an d h em atom as can decrease or occlu de th e fu n c VA dissect ion s h ave a dissect ing an eu r ysm as com pared w ith 10
t ion al diam eter of th e vessel, w h ich can h ave p erfu sion related to 57% of carot id/an terior circulat ion dissect ion s.3–5 In a Japa-
(h em odyn am ic) con sequ en ces. Dissect ion s can also exten d in to n ese coh or t of pat ien ts w ith dissect ing in t racran ial an eur ysm s,
th e su badven t it ial layer bet w een th e t u n ica m edia an d adven t i 93% w ere in th e ver tebrobasilar dist ribu t ion .6
t ia. Th is dam age to th e vessel w all can lead to th e form at ion of Cerebrovascu lar SADs in ch ildren are differen t from th ose in
dissect ing an eu r ysm s, also referred to as p seu doan eu r ysm s (Fig. adults. Th ey are m ore frequen tly in t racran ial th an ext racran ial,
32.3). Isolated intram ural hem orrhages and hem atom as can occur an d are m ore com m on ly seen in th e an terior circulat ion th an th e
spon tan eously or secon dar y to direct vessel t rau m a. Th ese often posterior circu lat ion .7

391

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392 III Ischemic Stroke and Vascular Insufficiency

Fig. 32.1 Axial computed tom ography angiogram in a


patient with an acute right-sided internal carotid artery
dissection who presented with a stroke. *Dissection flap.

Fig. 32.2 Anteroposterior (AP) cerebral angiogram after a right com m on Fig. 32.3 Magnified anteroposterior (AP) cerebral angiogram demonstrates
carotid artery injection in a patient with a right com m on carotid artery dis- a right internal carotid artery dissecting aneurysm (pseudoaneurysm ).
section. *Dissection flap.

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32 Medical, Surgical, and Endovascular Treatm ent of Arterial Injury 393

Traumatic Cerebrovascular Injuries su ch as t h e falx cerebr i (affect ing t h e an ter ior cerebral ar ter y
[ACA]), sp h en oid w ing (m iddle cerebral ar ter y [MCA]), an d ten
Cerebrovascu lar inju ries can occu r follow ing iat rogen ic inju ries
tor iu m (p oster ior cerebral ar ter y [PCA]).8 Dist al cor t ical in t ra
or blu n t/p en et rat ing t rau m a to th e h ead or n eck.
cran ial t rau m at ic an eur ysm s result w h en sku ll fract ures (e.g.,
convexit y) inju re dist al cort ical vessels.10 Traum at ic in t racran ial
an eur ysm s are n ot t ypically foun d at bran ch ing poin t s an d do
Blunt-Trauma Cerebrovascular Injuries
n ot h ave an an atom ic “n eck.”8
Th e in ciden ce of CVI follow ing blu n t t rau m a is 1%, w ith th e cer Th e m ost com m on in t racran ial fist u la resu lt ing from blu n t
vical ICA being m ore frequ en tly involved th an th e VA, an d th e h ead t raum a is th e carot id cavern ous sin u s fist ula (CCF), w h ich
ext racran ial vessels m ore com m on ly affected th an in t racran ial occurs in 3 to 5% of all pat ien ts w ith sph en oid bon e fract ures.8
vessels.8 Th e m ost com m on cause of blun t t raum a–related CVI is Trau m at ic CCFs are con n ect ion s bet w een th e in t racavern ou s ICA
m otor veh icle acciden t s follow ed by assault an d auto pedest rian or on e of its bran ch es an d th e cavern ous (ven ous) sin us. Th ese
inju ries. More th an on e ext racran ial vessel is affected in 18 to can occu r sp on t an eou sly, follow ing blu n t or pen et rat ing t rau m a,
38% of the cases, an d bilateral VA inju res h ave been repor ted in an d follow ing surgical procedures (iat rogen ic). Th ese fist ulas can
up to 28% of cases. Sim ilar to sp on tan eou s vascu lar inju ries, it is be eith er direct (ICA to th e cavern ous sin us—usually t raum at ic)
gen erally believed th at m ost isch em ic even t s an d n eurologic in or in direct (bran ch es off th e ICA or extern al carot id ar ter y to th e
juries related to t raum at ic CVIs also result from dissect ion s or cavern ou s sin u s). Loss of vision is th ough t to resu lt from ven ou s
th rom boem bolic even t s. Trau m at ic CVI can also resu lt in ar terial congest ion an d t ypically occu rs in a delayed fash ion . Th is is u su
occlusion or high grade stenosis secondar y to vessel injur y, w hich ally t h e m ost ser iou s con sequ en ce of a CCF. How ever, d esp ite
can also produ ce h em odyn am ic related st rokes. How ever, w h en t h e cavern ou s sin u s being invested w ith d u ra, th ese an eu r ysm s
dealing w ith t rau m a, it is difficu lt to adequ ately an d accu rately can rarely ru pt u re in to t h e su barach n oid space, cau sing a su b
est im ate t h e in ciden ce an d at t ribu te t h e et iology w h en th ere are arach n oid h em orrh age (SAH) or m edially in to th e sph en oid sin us
con fou n ding inju ries w ith in t racran ial or sp in al t raum a. cau sing severe ep istaxis.8,10
In general, ext racran ial blun t t raum a CVIs occur from four
m ech an ism s: vessel st retch ing, bon e t raum a/fract ures injuring
Penetrating-Trauma Cerebrovascular Injuries
adjacen t vessels, direct vascular t raum a, an d in t raoral t rau m a.8
Vessel st retch ing occurs w h en hyperexten sion an d rotat ion or Pen et rat in g CVIs com m on ly occu r secon dar y to in ten t ion al or
lateral flexion of th e n eck forces th e ICA again st th e cer vical ver accid en t al p u n ct u re, lacerat ion , or im p alem en t as w ell as from
tebral bodies or lateral m asses an d t ypically occu rs in th e C1–C3 project ile m issile inju ries. In th e m odern era, pen et rat ing CVIs
region . Direct vascu lar t raum a is less frequ en t an d results from are prim arily th e result of gun sh ot w oun ds. Pen et rat ing injuries
direct blu n t t rau m a to a vessel. In addit ion , hyperflexion of th e to th e h ead an d n eck can result in com plete or par t ial disru pt ion
n eck can cau se com p ressive inju r y to t h e ICA bet w een t h e cer of an ar ter y, h em odyn am ic in st abilit y, in t ra arterial th rom bus or
vical spin e an d m an dible. Cer vical sp in e inju ries su ch as ver te occlusion , an d ar terial com pression from adjacen t h em atom as.
bral fractures, sublu xation, and foram en transversarium fractures Due to th e h em odyn am ic con sequen ces of m ajor ar terial bleed
are a com m on sou rce of ext racran ial CVIs, in p ar t icu lar to t h e ing, m ost of th ese inju ries are obvious at th e t im e of presen t a
VA. Du e to it s in t im ate relat ion sh ip w ith th e cer vical spin e, VA t ion . Un exp lored part ial or occu lt inju ries m ay resu lt in su bacu te
inju r ies m ost com m on ly occu r in t h e secon d an d t h ird VA seg or even d elayed (m on t h s) p resen t at ion s of ar ter ial d issect ion s
m en t s. In t raoral t raum a occurs p rim arily in ch ildren an d results or in th e form at ion of dissect ing an eu r ysm s or ar terioven ous
w h en a pat ien t h as a foreign object in h is or h er m outh an d th en (AV) fist ulas. Ju st as in blun t t raum a CVIs, it is also im por t an t to
falls or experien ces t rau m a. Traum at ic ext racran ial an eur ysm s evalu ate th e ven ous system in pen et rat ing injuries to th e h ead
h ave been repor ted in th e ICA in 15 to 33% an d in th e VA in 4 to an d n eck.
8% of all t rau m at ic h ead/n eck inju r ies. Trau m at ic ext racran ial Th e lateral n eck is divided an atom ically in to t h ree zon es.
fist u las are m ost com m on ly seen in t h e exter n al carot id ar ter y Zon e 1 exten ds from th e clavicle to t h e cricoid car t ilage, zon e 2
bran ch es. exten d s from th e cricoid car t ilage to th e angle of th e m an dible,
Th e m ost com m on in t racran ial vessel inju red follow ing blu n t an d zon e 3 exten ds from th e angle of th e m an dible to th e skull
t rau m a to th e h ead is th e ICA. Blu n t t rau m a to th e h ead can re base. Th ese zon es h ave been used h istorically to h elp determ in e
su lt in in t racran ial dissect ion s, t rau m at ic an eu r ysm s, vessel oc th e risk of m ajor vessel inju r y in p at ien t s w ith ou t over t sign s of
clu sion s, an d fist u las. Th e in t racran ial ICAs are m ost frequ en t ly h em odyn am ic in st abilit y w ith p en et rat ing inju r ies d eep to t h e
inju red follow ing sku ll base fract ures, an d can be seen in u p to p lat ysm a an d to d eter m in e t r iage an d t reat m en t st rategies. Al
11% of carotid canal fractures.9 Traum atic intracranial aneurysm s th ough th ese zon es are st ill u sed to describe p en et rat ing inju r y
represen t < 1% of all in t racran ial an eu r ysm s in adu lts an d 20% in locat ion , in t h e m od er n im aging era t h ey are less frequ en t ly
pediat rics.10 u sed alon e w ith ou t vascu lar im aging (com pu ted tom ograp hy
In t racran ial t raum at ic an eur ysm s are divided in to th ree t ypes angiography [CTA] or angiogram ) to determ in e th e m an agem en t
based on locat ion : skull base, su bcor t ical, an d distal cor t ical.10 st rategy in h em odyn am ically st able pat ien t s. For th is reason ,
Trau m at ic in t racran ial an eu r ysm s of t h e sku ll base m ost com th ese zon es are n ot described in det ail h ere.
m on ly occu r secon dar y to sku ll base fract u res, w it h t h e cav Vascu lar com p licat ion s resu lt in g from p en et rat in g inju r ies
er n ou s segm en t of th e ICA being th e m ost com m on site (48%). to th e h ead occur in 5 to 40% of cases.11 Ap ar t from h em atom as
Su bcort ical in t racran ial an eu r ysm s resu lt w h en blu n t t rau m a cau sed by vessel disru pt ion , dissect ing an eu r ysm s are th e m ost
cau ses accelerat ion an d d ecelerat ion of th e m obile brain (an d com m on ly repor ted vascu lar inju r y follow ing p en et rat ing inju r y
p en et rat ing an d su r rou n d in g ar ter ies) again st fixed st r u ct u res to th e h ead.11

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394 III Ischemic Stroke and Vascular Insufficiency

Venous Cerebrovascular Injuries m ore com m on in th e VA th an in th e ICA, occurs in 42 to 68% of


cases, an d t yp ically occurs soon er th an 6 m on th s.1
Injuries to in t racran ial an d ext racran ial ven ou s system can h ave
In gen eral, spon tan eou s ext racran ial dissect ing an eur ysm s
sign ifican t n eu rologic sequ elae, p ar t icu larly in p at ien t s w it h
are n ot con sidered to be h igh risk an eur ysm s, an d th ey h ave a
con com it an t h ead inju ries. CVIs to th e ven ou s system can affect
low risk of cau sing isch em ic cerebral sym ptom s.1 In th ree large
th e d u ral ven ou s sin u ses an d oth er m ajor drain ing vein s, cau se
ret rosp ect ive st udies, th ese an eur ysm s rem ain ed st able in size
ven ou s th rom bosis, an d affect th e m ajor cer vical ven ous ou tflow
in 59 to 100%of th e cases, decreased in 5 to 30%of cases, an d h ad
p ath w ays. Th ese ven ou s inju r ies can resu lt in cerebral ven ou s
n o eviden ce of ru pt u re or st rokes.15–17
in farct ion s or elevated in t racran ial p ressu re secon dar y to in
Sp on t an eou s in t racran ial dissect ion s an d an eu r ysm s are dif
creased ven ous congest ion . W h en evaluat ing t raum at ic vascular
feren t from th eir correspon ding ext racran ial lesion s. Given th e
injuries to th e h ead an d n eck, th e ven ou s system sh ould n ot be
rarit y of th ese lesion s, lit tle is w rit ten an d kn ow n abou t th eir
overlooked.
n at u ral h istor y. In a Jap an ese coh or t of dissect ing in t racran ial
an eur ysm s m an aged by m edical th erapy alon e, a good Glasgow
Iatrogenic Cerebrovascular Injuries Outcom e Scale recover y w as ach ieved in 79% of pat ien t s.6 It is
clear, h ow ever, t h at sp on t an eou s in t racran ial d issect in g an eu
Iat rogen ic CVIs h ave been repor ted in associat ion w ith various r ysm s are n ot as ben ign as th eir ext racran ial coun terpart s, an d
en d ovascu lar (Fig. 32.4), percut an eous, open surgical, an d en do are associated w ith a sign ifican t risk of h em orrh age an d an eu
scopic procedu res. It is difficu lt to calcu late th e act u al in ciden ce r ysm grow th . Naito et al18 repor ted th ree cases of SAH in th eir
of th ese vessel injuries becau se m ost of th e m in or, in adver ten t series of 21 pat ien ts w ith ver tebrobasilar dissect ion s. Th ey also
injuries h ave a good n at u ral h istor y of recover y w ith out fu rth er n oted progression of dissect ion or an in crease in an eur ysm size
sequ elae. Th e in ciden ce of u n in ten t ion al carot id ar ter y p u n ct u re in an oth er fou r pat ien ts.
du ring at tem pted in tern al jugu lar vein cen t ral lin e p lacem en t It is difficult to evaluate the n atural h istor y of traum atic extra
u sing lan dm arks in adu lt s is 5%. Th is rate is h igh er in em ergen an d in t racran ial CVIs. Typically t h ese p at ien t s p resen t w ith
cies an d in ch ildren an d can be reduced by u sing u lt rasoun d p olyt raum a an d in t racran ial fin dings, w h ich m ay com plicate th e
guidan ce.12 Despite un in ten t ion al carot id ar ter y pun ct ure, th ere exam an d m ake it difficu lt to at t ribu te a specific cau se or t im e
are few repor ts of st rokes or oth er serious com plicat ion s from lin e to th e p at ien t’s n eurologic injur y. Th is is fu r th er con foun ded
th ese pu n ct u res. by t h e fact t h at m any p at ien t s w it h t rau m at ic in t ra an d ext ra
In an terior cer vical spin e surgeries, VA injuries are fairly rare cran ial CVIs p resen t in a delayed fash ion or after in it ial “n or
w ith an in ciden ce of 0.3 to 0.5%. Th e in ciden ce of CVI from pos m al” vascu lar st u dies.
terior cer vical spin e surger y is h igh ly depen den t on th e proce Trau m at ic in t racran ial an eu r ysm s also app ear in a delayed
du re. C1–2 t ran sar t icu lar facet screw s h ave an in ciden ce of CVI fash ion . But th ese an eur ysm s are kn ow n to h ave a 50% risk of
of 4.1 to 8.2%, w h ereas th ere are few to n o repor ted CVIs from rupt ure in th e first w eek after diagn osis.19 Th ese lesion s are con
th e p lacem en t of su baxial lateral m ass screw s.13 sidered u n st able, an d rep or ts on con ser vative m an agem en t h ave
Alth ough som ew h at con t roversial, cer vical spin al m an ipu la revealed a m or talit y rate of 50%.8
t ive th erapies, such as ch irop ract ic th erapy, h ave been sh ow n to Th e CCFs do n ot t ypically h ave an in creased m or t alit y rate,
be an in depen den t risk factor for cerebrovascular dissect ion s. bu t in rare cases th ey can r u pt ure in tracran ially. Th e m ajor con
Dissect ion s in th e ver tebrobasilar system h ave been m ore fre cern is vision loss, w h ich can occur in 20 to 30% of pat ien ts.20
qu en tly rep or ted th an in th e an terior circu lat ion . Th e repor ted Th ese lesion s h ave been repor ted to progress in severit y an d
frequ en cy for vertebrobasilar dissect ion is on e in 10,000 to on e sym ptom atology as w ell as even sp on tan eou sly resolve in 20 to
in 2 m illion , an d for isch em ic st roke it is on e in 100,000 to on e in 50% of cases.20
200,000 cer vical sp in al m an ip u lat ion s.8

■ Clinical Presentation
■ Natural History of the Disease
Spontaneous Extracranial Arterial Dissections
A review of publish ed m or talit y rates in pat ien ts w ith spon tan e
ous ext racran ial ar terial dissect ion s from th e last decade sh ow s Pat ien ts w ith spon t an eou s ext racran ial arterial dissect ion s can
a m or talit y rate of 3 to 7%, w h ich is im proved from previou s an d presen t w ith sign s or sym ptom s of cerebral isch em ia, p ain (h ead
h istorical repor t s.1 Th ese im p roved m or talit y resu lts likely re or n eck), or Horn er syn drom e.1 Cerebral isch em ia, m an ifest as
flect earlier an d bet ter detect ion due to advan ces an d availabilit y t ran sien t isch em ic at tacks or isch em ic st rokes, occu rs in 67% of
of m edical im aging an d gen eral acceptan ce of an t icoagu lat ion or patients w ith extracranial SADs.21 These ischem ic events are m ost
an t ip latelet t reat m en t for th ese p at ien t s. Alt h ough n eu rologic often em bolic in n at ure, but can be perfusion related if th ere is
ou tcom es are good to excellen t in t h e vast m ajor it y of t h ese com plete or near com plete vessel occlusion w ith poor collaterals.
p at ien t s, n early h alf are disch arged w ith a persisten t n eurologic Pain can be presen t in up to 70% of SADs an d is t yp ically as
deficit .1,14 Th e rate of st roke after a spon t an eou s ext racran ial dis sociated w ith a fron totem p oral h eadach e in ICA dissect ion s an d
sect ion is 0.3 to 3.4% per year, w ith th e greatest risk occurring in parietal occipit al h eadach es in VA dissect ion s.1 Neck pain is less
th e first m on th after inju r y.1 Healing of dissect ion s is th ough t to frequ en t th an h eadach es, bu t m ore com m on in VA dissect ion s
occur w ith in 3 to 6 m on th s and occurs m ore in th e VA th an in th e th an ICA dissect ion s. Horn er’s syn drom e is th e presen t ing sym p
ICA. Recan alizat ion of dissect ion related sten osis or occlusion is tom in 10 to 12%of ICA SAD pat ien ts an d is found in 28 to 58%of

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32 Medical, Surgical, and Endovascular Treatm ent of Arterial Injury 395

a b

d
c

Fig. 32.4a–e Cerebral angiogram in a patient with an iatrogenic direct


carotid-cavernous sinus fistula (CCF) following m echanical throm bectomy
for acute stroke. (a) Anteroposterior and (b) lateral projection angiogram s
dem onstrate the fistula. (c) Lateral projection angiogram showing place-
ment of an intra-arterial balloon at the fistulous point. (d) Lateral projection
angiogram showing the intra-arterial balloon inflated in the right internal
carotid artery (ICA) for flow arrest and parent lum en protection with a m i-
crocatheter through the fistulous point into the cavernous sinus (for Onyx
[ev3, Irvine, CA] injection). (e) Postprocedural lateral projection angiogram
dem onstrates preservation of the parent vessel and complete occlusion of
the previously visualized CCF via a transarterial approach. e

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396 III Ischemic Stroke and Vascular Insufficiency

ICA SAD patien ts. Because SADs occur m ore frequen tly in the ICA, is less appropriate for unstable patients. In addition, DSA can m iss
Horn er’s syn drom e is th ird order, w h ich m ean s th at th e p hysical th rom bosed d issect ing an eu r ysm s. DSA is app rop riate in cases
presen tat ion u su ally in clu des eyelid ptosis an d p ap illar y m iosis w h ere an en dovascu lar procedu re m ay be in dicated an d w h en
but n ot an h idrosis, as th e sym path et ic n er ves to th e sw eat glan ds oth er cross sect ion al im aging is eith er n on diagn ost ic or u n clear.
follow th e extern al carot id ar ter y. Oth er p resen t ing sym ptom s of Noninvasive cross sectional vascular im aging is becom ing m ore
SAD in clude pu lsat ile t in n it us, cran ial n europath ies, spin al cord sen sit ive an d accu rate an d can be con sidered a valid altern at ive
isch em ia, an d cer vical radicu lop athy. Pat ien t s w ith SAD h ave an to DSA in m any cases w h en h igh qualit y, good resolut ion im ages
in creased in ciden ce of ar terial dissect ion s in oth er region s of th e are obtain ed. Th e Eu ropean Federat ion of Neurological Societ ies
body an d m ay presen t w ith oth er system ic sym ptom s. Pat ien t s recom m en ds m agn et ic reson an ce im aging (MRI)/m agn et ic reso
w ith spon tan eous in t racran ial ar terial dissect ion s t ypically pre n an ce angiography (MRA) for diagn osing ar terial dissect ion s.22
sen t w ith h ead or n eck p ain , isch em ic sym ptom s, flu ct u at ing W h en com p ared w ith DSA, th e sen sit ivit y of MRI or MRA in de
n eu rologic sym ptom s, or SAH (from a dissect ing an eur ysm ). tect ing spon tan eous ICA an d VA dissect ion s is 87 to 99%an d 60%,
respect ively.1 An advan t age of MRI is th at it also gives th e m ost
accurate in form at ion regarding isch em ic dam age to th e brain an d
Traumatic or Penetrating Arterial Injuries d oes n ot requ ire con t rast ad m in ist rat ion . In ad d it ion , MR p er
Pat ien t s w ith m ajor t rau m at ic an d pen et rat ing arterial injuries fu sion an d diffusion sequen ces give valuable in form at ion con
presen t w ith h em odyn am ic in stabilit y or vessel occlu sion . Th e cern ing an isch em ic pen u m bra, w h ich in fluen ces decision s about
presen tat ion of th ose w ith t rau m at ic in t ra an d ext racran ial ar p er for m ing n eu roin ter ven t ion s. Also, MRI is an excellen t m o
terial inju ries, w h ich are n ot h em odyn am ically com prom ising, dalit y for detect ing th rom bosed dissect ing an eu r ysm s th at are
are sim ilar to th ose w ith spon tan eous injuries (listed above) but n ot w ell seen on DSA. MRI/MRA is n ot ideal for sm all or distally
also in cludes hem orrhage, h em atom a, and traum atic fistulas. The located an eu r ysm s, or for p at ien t s w ith severe or m u lt ip le sys
m ajor differen ce bet w een t raum at ic an d spon tan eou s arterial tem ic injuries or t raum a. It also h as lim itat ion s associated w ith
injuries is th at pat ien ts w ith t rau m at ic inju ries t ypically presen t t im e an d availabilit y at som e cen ters.
in a delayed fash ion an d in som e cases after a n orm al vascular Com pu ted tom ograp hy angiography of th e h ead an d n eck is
st udy. Ap proxim ately 90% of t rau m at ic in t racran ial an eu r ysm s a n on invasive altern at ive to DSA. It can be perform ed rapidly,
are associated w ith a cran ial fract ure. Traum at ic in t racran ial an is available at m ost cen ters, h as a sen sit ivit y sim ilar to th at of
eu r ysm s h ave been rep or ted to ap p ear days to w eeks after in it ial MRI/MRA in diagn osing ICA dissect ion s, an d h as a sen sit ivit y
injur y. Th ose w ith CCFs can p resen t w ith a cavern ou s sin us syn an d specificit y in detect ing VA dissect ion s of 100% an d 98%, re
drom e ch aracterized by cran ial n eu rop ath ies, conju n ct ival ch e sp ect ively, w h ich is su perior to th ose of MRI/MRA.1 Th e m ain
m osis, pain fu l exoph th alm os or proptosis, an d ocu lar br u it .20 advan t ages of CTA are th at it can be perform ed rapidly, it is avail
able at n early all cen ters, an d it can give sign ifican t inform at ion
about th e spin e an d cran iu m , w h ich m akes it th e preferred im ag
ing m odalit y for evaluating acute vascular injuries associated w ith
blunt and penetrating head and neck traum a. Lim itations include
■ Imaging of Cerebrovascular Injuries th e n eed for con t rast adm in ist rat ion an d exp osu re to radiat ion .
Im aging m odalit ies are n ot a subst it u te for a th orough an d com An oth er disadvan t age w h en com pared w ith MRI is the accuracy
plete h istor y an d p hysical exam in at ion . Fin d ings an d clu es from of iden t ifying areas of isch em ia. How ever, CT perfu sion im aging
the histor y and physical, including m echanism of injur y in traum a, can be p erform ed at th e sam e t im e as CTA on m any of th e n ew er
sh ou ld direct th e w orku p an d diagn osis of cerebrovascu lar inju CT scan n ers. CT perfusion can reveal in form at ion about isch em ia
ries, n ot th e reverse. an d p en u m bra, w h ich aid s t h e clin ician in t h e t reat m en t d eci
A n on con t rast com p u ted tom ography (CT) scan of th e h ead is sion process.8
rout in ely th e first im aging st u dy ordered in p at ien t s presen t ing Du p lex u lt rason ograp hy is a less u sefu l im aging m odalit y
w ith isch em ic sym ptom s. In addit ion , a n on con t rast CT of th e in t h e set t in g of acu te t rau m at ic an d sp on t an eou s vascu lar in
h ead an d n eck is also par t of th e stan dard evaluat ion for blun t ju ries.1,8 Th e m ain cr it icism is t h at u lt rasou n d ap p ears to h ave
an d pen et rat ing h ead/n eck t raum a. Th e h istor y an d physical, as lim ited accu racy in detect ing sm all spon t an eous dissect ion s.23
w ell as th ese n on con t rast CT im age fin dings, can h elp guide fu How ever, m ost au t h ors agree t h at u lt rasou n d m ay h ave u t ilit y
t u re vascu lar w orku ps as cer t ain CT fin dings in crease su spicion in lon g ter m follow u p of ext racran ial vascu lar inju r ies an d
of a poten t ial vascu lar inju r y. Im aging fin dings such as st roke, lesion s.1,8
in t racran ial h em orrh age, sku ll base or cran ial fract ure, cer vical
spin e inju r y or fract u re, an d pen et rat ing h ead inju ries th at cross
th e m idlin e or involve th e ven ou s sin u ses all in crease th e su sp i
cion of a CVI an d w arran t fu r th er vascu lar w orku p. ■ Treatment
Cerebral d igit al su bt ract ion angiograp hy (DSA) is th e gold
st an dard test for evalu at in g an d d iagn osin g cerebrovascu lar in
Hemodynamically Unstable Injuries
juries. DSA en ables th e detect ion of vessel inju ries such as in t im al Pat ien ts p resen t ing em ergen tly w ith h em odyn am ic in stabilit y
injur y (dissect ion ), in t im al flap, a false or dou ble lu m en , vessel u su ally h ave severe ext racran ial vascu lar injuries, w h ich in gen
sten osis or occlu sion , in t ralu m in al th rom bu s, collateral circu la eral w arran t su rgical exp lorat ion . Treat m en t of th ese m ajor inju
t ion , an d an eu r ysm s or fist u las. DSA h as lim it at ion s in th at it ries by a t rau m a or vascu lar su rgeon can occu r via direct vessel
is m ore invasive th an oth er im aging m odalit ies, it is n ot alw ays repair, placem en t of an in terposit ion al vascu lar graft , or vessel
available at all centers, it is expensive and tim e consum ing, and it occlusion w ith or w ith ou t revascularizat ion .

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32 Medical, Surgical, and Endovascular Treatm ent of Arterial Injury 397

Hemodynamically Stable Injuries be follow ed w ith serial vascular st udies to m on itor for th e devel
opm en t of dissect ing an eu r ysm s.
Arterial Dissection
Treat m en t st rategies for ar terial dissect ion s focu s on p reven t ion
Dissecting Aneurysms
of th rom boem bolic com plicat ion s an d m ain tain ing paten cy in
areas of vessel sten osis.10 Th ere is n o cu rren t con clusive eviden ce Dissect ing an eu r ysm s can occur in associat ion w ith spon tan eous
favoring eith er an t iplatelet agen ts over an t icoagulat ion for t reat or t raum at ic ar terial dissect ion s. Th e ideal t reat m en t st rategy
m en t of asym ptom at ic or sym ptom at ic ar terial dissect ion s. Sys for dissect ing an eur ysm s h as n ot been est ablish ed. St u dies h ave
tem at ic review s, as w ell as th e Coch ran e Review, h ave failed to sh ow n th at spon t an eou s dissect ing an eu r ysm s w ith ou t eviden ce
fin d a th erapeut ic superiorit y of on e t reat m en t over th e oth er. of in t racran ial h em or rh age can be m an aged su ccessfu lly con
Exp er t s agree th at a large ran dom ized con t rolled t rial is n eeded ser vat ively.6 Oth er st u dies h ave dem on st rated an in creased risk
to h elp an sw er th is qu est ion .1,24 Th ere is cu rren tly on e ongoing of progressing to SAH in th ese an eur ysm s.18 W h en th ese an eu
ran dom ized clin ical t rial (th e Cer vical Arter y Dissect ion in St roke r ysm s r u pt u re, t h ey h ave a h igh in cid en ce of rebleed ing an d
St u dy [CADISS]) th at h op es to address som e of th e qu est ion s.25 d efin itely w arran t t reat m en t . In con t rast , it is gen erally accepted
Th e m ost com m on an t iplatelet th erapy for ar terial dissect ion s th at t rau m at ic dissect ing an eu r ysm s are u n st able lesion s an d
is asp irin . Th is is likely du e to it s low cost , w ide availabilit y, an d w arran t t reat m en t .
ease of access; h ow ever, dipyridam ole, clopidogrel, prasugrel, an d Dissect ing an eur ysm s are an atom ically dist in ct from saccular
t iclopidin e are oth er poten t ial altern at ives. An t iplatelet agen t s an eur ysm s, an d th eir t reat m en t is also dist inct . As th ese an eu
h ave som e ben efits over an t icoagulan t s. An t iplatelet agen t s are r ysm s lack a dist in ct n eck, surgical opt ion s are lim ited an d in
associated w ith few er risks of h em orrh agic com plicat ion s, w h ich clude aneur ysm w rapping, vessel occlusion, vessel reconst ruction
m akes th em at t ract ive in cases of t raum at ic an d in t racran ial dis or bypass, an d t rapping of th e an eur ysm . En dovascular t reat
sect ion s. In addit ion , aspirin is less expen sive an d does n ot re m en t opt ion s in clu d e vessel occlu sion /t rap p in g (w ith balloon
qu ire frequen t laborator y draw s to ch eck levels. test occlu sion ), coiling of an eur ysm s w ith or w ith out sten t or
An t icoagulan t th erapy rout in ely con sist s of an in it ial h eparin balloon assistan ce, sten t placem en t across the area of dissect ion
drip w ith bridging th erapy to w arfarin w ith a targeted in tern a alon e, Onyx (liqu id em bolic) em bolizat ion , an d p lacem en t of
t ion al n orm alized rat io (INR) of 2 to 3. An t icoagu lat ion is t yp i flow diverting stents. Because dissecting aneur ysm s are generally
cally con t in u ed for 3 to 6 m on th s, after w h ich a vascu lar st u dy irregularly shaped an d lack a defined neck, the m ost com m only
is perform ed to evalu ate th e h ealing of th e lesion . If th e lesion is u sed en dovascular t reat m en t opt ion s are vessel occlusion /t rap
h ealed, th en an t icoagulat ion can be stopped; if n ot , th erapy is ping an d sten t assisted coiling to protect th e p aren t vessel from
con t in u ed an oth er 3 m on th s an d th e lesion is reim aged. Lim it a coil m ass h ern iat ion . W h en occluding a paren t vessel in a dis
t ion s to an t icoagu lat ion in clu de a h igh er risk of in t racran ial an d sect ing an eu r ysm , t yp ically th e an eu r ysm n eeds to be exclu ded
system ic h em orrh age, a p oten t ial risk of en larging an in t ram u ral com pletely from circu lat ion via t rapping of the an eur ysm proxi
h em atom a, an d t h e n eed for frequ en t blood ch ecks. An t icoagu m ally and distally. This prevents recanalization, grow th, or rupture
lat ion h as a t h eoret ical ben efit w h en a free float ing t h rom bu s from flow reversal. In addit ion to preser ving th e p aren t vessel,
is seen . sten t assisted coiling offers th e ben efit of placing a sten t scaffold
System ic th rom bolyt ic agen t s u sed in pat ien ts w ith st roke across th e dissected por t ion of th e vessel onto w h ich th e en do
an d ar terial dissect ion s h ave sh ow n a com plicat ion rate sim ilar th elium can grow an d repair both th e an eu r ysm an d dissect ion .
to th at of system ic th rom bolysis for pat ien ts w ith st rokes an d n o Rupt u red dissect ing an eur ysm s pose a sign ifican t t reat m en t
eviden ce of dissect ion .1 In a review of 50 p at ien t s w ith ar terial ch allenge. Vessel occlu sion /t rapping is gen erally p referred w h en
dissect ion an d st roke t reated w ith th rom bolyt ic agen ts, 40% of occlusion of th e vessel is an acceptable opt ion an d w ill n ot result
p at ien t s h ad a m od ified Ran kin scale score of 0 to 2 (a good in sign ifican t m orbidit y or m oralit y.27 Alth ough con t roversial in
outcom e).25 th e acu te su barach n oid p eriod, som e advocate sten t assisted coil
En dovascu lar th erapies for ext racran ial ar terial dissect ion s em bolizat ion in t h ese cases. Oth er opt ion s in clu d e Onyx (ev3,
h ave been sh ow n to be successfu l at repairing dissect ion s. Typi Ir vin e, CA) em bolizat ion , flow d iversion (also con t roversial be
cally th is in clu des p ercu t an eou s t ran sar terial sten t placem en t cau se of t h e n eed for d u al an t ip latelet agen t s), vessel occlu sion /
across th e inju red segm en t . In sten osed segm en t s, angioplast y trapping w ith bypass, surgical w rapping, and surgical recon struc
can be u sed, bu t is n ot n ecessar y if th ere is n o sign ifican t lu m in al t ion of th e vessel.
sten osis. Don as an d colleagu es 26 review ed t h e literat u re an d
rep or ted tech n ical su ccess in 100% of p at ien t s u n dergoing en
Carotid-Cavernous Sinus Fistulas
dovascu lar th erapy for dissect ion s. Th e rate of paten cy at 1 year
w as 100%. How ever, adverse even ts w ere seen in 11% of th e p a As described above, spontaneous, indirect fistulas can som etim es
t ien t s u n dergoing en dovascu lar th erapy. Altern at ively, th e ICA spon tan eou sly resolve. Trau m at ic fist ulas ten d to be direct CCFs
can be sacrificed in cases th at are n ot am en able to sten t ing or an d do n ot spon tan eously resolve. Treat m en t of CCFs involves
m edical th erapy. Vessel sacrifice can be perform ed using en do closing th e com m u n icat ion th at exist s bet w een th e cavern ou s
vascu lar or op en su rgical tech n iqu es; h ow ever, a balloon test ICA an d th e cavern ous sin us. Obliterat ion of th e CCF is t ypically
occlusion an d p rovocat ive test ing sh ou ld p recede it . p er for m ed via a t ran sar ter ial or t ran sven ou s en d ovascu lar ap
Th ere is n o good eviden ce su p por t ing th e ideal t reat m en t of proach . Detach able balloon occlu sion , on ce th e m ain st ay of en
in t racran ial dissect ion s. In gen eral, st u dies h ave su pported th e dovascular t reat m en t , is n o longer available in th e Un ited St ates.
use of an t icoagulan ts an d an t ip latelet agen t s as u sed in ext racra Tran sven ou s obliterat ion is an excellen t m ode of occlu ding CCFs.
n ial dissect ion s.1 All pat ien ts w ith in t racran ial dissect ion s sh ou ld Th e t ran sven ou s rou te to th e cavern ou s sin u s can be from eith er

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398 III Ischemic Stroke and Vascular Insufficiency

a p oster ior or an ter ior ap p roach . A p oster ior ap p roach to t h e w it h or w it h ou t byp ass. We p refer conven t ion al cerebral DSA
cavern ous sin u s is t yp ically th rough th e in tern al jugu lar vein an d for diagn osing acute dissect ion s an d ten d to follow th e lesion s
th e in ferior pet rosal sin u s. An an terior ap proach to th e cavern w ith serial im aging (eith er cross sect ion al or dyn am ic DSA) un t il
ous sin us is t ypically th rough th e facial vein an d th e superior th e dissect ion is h ealed. On e year follow u p im aging is also rec
ophthalm ic vein. Direct percutaneous orbital approaches through om m en ded. In sym ptom at ic pat ien t s w ith flow lim it ing sten o
th e su p erior op h th alm ic vein , as w ell as oth er t ran sven ou s rou tes sis, w e advocate en d ovascu lar in ter ven t ion s via eith er sten t ing
su ch as th e su perior pet rosal sin u s, th e pter ygoid p lexu s, an d w ith or w ith out angioplast y or vessel occlusion w ith or w ith ou t
cor t ical vein s, h ave also been described.28 On ce in th e cavern ou s bypass.
sin u s, detach able coils can be dep loyed or em bolic m aterials can A con cer n ing t ren d em erging at som e cen ters across t h e
be injected to obliterate th e CCF. cou n t r y is aggressive sten t in g of asym ptom at ic p at ien t s w it h
Tran sar terial th erapy con sists of carefu lly placing a m icro n on –flow lim it ing t raum at ic carot id or VA dissect ion s. In gen
cath eter th rough th e ar terial defect in to th e cavern ou s sin u s eral, th e rat ion ale is th at th ese p at ien t s also h ave a n eed for oth er
(Fig. 32.4). Obliterat ion th en occurs by placing detach able coils su rgical procedu res (t ypically or th opedic) for w h ich th e p at ien t
or inject ing em bolic agen t s in to th e cavern ous sin us. W h en em can n ot be kept on h ep arin . Th is lin e of th in king is flaw ed. Th e
bolic agen ts are injected, a balloon can be tem porarily in flated m ajor cause of m orbidit y from ext racran ial vessel dissect ion s is
w ith in th e cavern ous ICA to preven t em bolic m aterial from re em bolic st roke. Biologically, both th e dissect ion it self an d m et al
flu xing in to th e ICA an d dow n st ream . Altern at ively, th e CCF can lic sten t s can be th rom bogen ic u n t il en doth elialized. Both an t i
be t reated via ICA occlu sion . Typically th is is preceded by balloon coagu lat ion (h eparin in th e acu te set t ing follow ed by w arfarin )
test occlu sion . Oth er described an d poten tial off label t ran sar te an d an t iplatelet agen ts h ave been sh ow n to be effect ive in reduc
rial t reat m en t s opt ion s for CCFs in clu de th e u se of covered sten t s, ing th ese com p licat ion s. Alth ough sten t ing can effect ively “t ack
w h ich m ay be difficult to place in th e cavern ous ICA given th eir dow n ” an adven t it ial flap an d decrease th e sou rce of th rom
rigidit y, an d flow diver t ing sten t s. boem boli, th e sten t it self is th rom boem bolic an d requires dual
an t iplatelet coverage. We are aw are of n o eviden ce th at su ppor ts
th e n ot ion th at a sten t is su p erior to m ed ical t reat m en t in n on –
flow lim iting extracranial arterial dissections. As discussed above,
in cert ain t rau m a scen arios th ere is n o ideal sit uat ion or t reat
■ Conclusion m en t plan . In gen eral, an t iplatelet agen t s are felt to be less risky
Both an t icoagu lat ion an d an t iplatelet agen t s offer good em bolic for system ic an d in t racran ial bleed ing com p licat ion s t h an are
protect ion to pat ien ts w ith dissect ion s. In gen eral, w e ten d to an t icoagu lan t s in t rau m a p at ien t s.8 It is ou r belief t h at t h ese
prescribe aspirin m ore frequently because of its low cost and w ide asym ptom at ic pat ien t s w ith out flow lim it ing dissect ion s sh ould
availabilit y an d th e th eoret ical low er risk of in t racran ial h em or be p laced on asp ir in t h erapy an d t h en u n d ergo t h e n ecessar y
rh ages in t h is p at ien t p op u lat ion . In p at ien t s w it h recu r ren t or t h opedic an d gen eral su rger y p rocedu res. Sten t ing sh ou ld be
isch em ic sym ptom s despite aspirin t reat m en t , w e recom m en d reser ved for sym ptom at ic pat ien t s and th ose w ith flow lim it ing
du al an t iplatelet agen ts or con sider sw itch ing to an t icoagu lat ion . dissect ion s, w h ich can cau se h em odyn am ic or p erfu sion related
If sym ptom s persist , th e pat ien t sh ould be reevaluated for pos even ts, an d sh ould be con sidered in pat ien t s w h o con t in u e to
sible en d ovascu lar t reat m en t via sten t ing or vessel occlu sion h ave th rom boem bolic st rokes desp ite an t iplatelet th erapy.

References
1. Fusco MR, Harrigan MR. Cerebrovascular dissect ion s—a review par t I: 9. Resn ick DK, Subach BR, Marion DW. Th e sign ifican ce of carot id can al
Sp on t an eou s d issect ion s. Neu rosu rger y 2011;68:242–257, d iscu ssion involvem en t in basilar cran ial fract ure. Neurosurger y 1997;40:1177–
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2. Biller J, Hingtgen W L, Adam s HP Jr, Sm oker W R, Godersky JC, Toffol GJ. 10. Krings T, Geibpraser t S, Lasjaun ias PL. Cerebrovascular t raum a. Eur Radiol
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3. Ch aves C, Estol C, Esn aola MM, et al. Spon t an eous in t racranial in tern al pen et rat ing brain injur y. J Em erg Traum a Sh ock 2011;4:395–402
carot id ar ter y dissect ion : repor t of 10 pat ien t s. Arch Neurol 2002;59:977– 12. Reu ber M, Du n kley LA, Tu r ton EP, Bell MD, Bam ford JM. St roke after
981 in ter n al jugular ven ous can n ulat ion . Act a Neurol Scan d 2002;105:235–
4. Oh kum a H, Suzuki S, Ogan e K; St udy Group of the Associat ion of Cerebro 239
vascu lar Disease in Toh oku , Jap an . Dissect ing an eu r ysm s of in t racran ial 13. Peng CW, Ch ou BT, Ben do JA, Spivak JM. Ver tebral ar ter y inju r y in cer vical
carot id circulat ion. St roke 2002;33:941–947 sp in e su rger y: an atom ical con siderat ion s, m an agem en t , an d preven t ive
5. Sh in JH, Suh DC, Ch oi CG, Leei HK. Ver tebral ar ter y dissect ion : spect r um m easures. Spin e J 2009;9:70–76
of im aging fin dings w ith em phasis on angiography an d correlat ion w ith 14. Ch an dra A, Su lim an A, Angle N. Spon t an eous dissect ion of th e carot id an d
clin ical presen t at ion . Radiograph ics 2000;20:1687–1696 vertebral arteries: the 10 year UCSD experien ce. An n Vasc Su rg 2007;
6. Yam aura A, Ono J, Hirai S. Clin ical pict ure of int racran ial n on t raum at ic 21:178–185
dissect ing an eu r ysm . Neu ropath ology 2000;20:85–90 15. Guillon B, Brun ereau L, Biousse V, Djouh ri H, Lévy C, Bousser MG. Long
7. Fullerton HJ, Joh n ston SC, Sm ith WS. Arterial dissect ion an d st roke in ch il term follow up of an eur ysm s developed during ext racran ial in tern al ca
dren . Neurology 2001;57:1155–1160 rot id ar ter y dissect ion . Neurology 1999;53:117–122
8. Fusco MR, Harrigan MR. Cerebrovascular dissect ions: a review. Part II: 16. Ben n inger DH, Gan djour J, Georgiadis D, Stöckli E, Arn old M, Baum gar t n er
blu n t cerebrovascular injur y. Neurosurger y 2011;68:517–530, discussion RW. Ben ign long term ou tcom e of con ser vat ively t reated cer vical an eu
530 r ysm s due to carot id dissect ion. Neurology 2007;69:486–487

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17. Touzé E, Randou x B, Méar y E, Arquizan C, Meder JF, Mas JL. An eur ysm al 23. Arn old M, Baum gar t n er RW, St apf C, et al. Ult rasoun d diagn osis of spon
form s of cervical artery dissect ion: associated factors and outcom e. Stroke t an eous carot id dissect ion w ith isolated Horn er syn drom e. St roke 2008;
2001;32:418–423 39:82–86
18. Naito I, Iw ai T, Sasaki T. Managem en t of in t racran ial vertebral arter y dis 24. Donn an GA, Davis SM. Ext racran ial ar terial dissect ion : ant icoagulat ion is
sect ion s in it ially presen t ing w ithou t subarach n oid h em orrh age. Neuro th e t reat m en t of ch oice. St roke 2005;36:2043–2044
su rger y 2002;51:930–937, discussion 937–938 25. Cer vical Ar ter y Dissect ion in St roke St u dy Trial Invest igators. An t iplatelet
19. Uzan M, Can t asdem ir M, Seckin MS, et al. Traum at ic in t racran ial carot id th erapy vs. an t icoagu lat ion in cer vical ar ter y dissect ion : rat ion ale an d
t ree an eu r ysm s. Neu rosu rger y 1998;43:1314–1320, d iscu ssion 1320– design of th e Cer vical Arter y Dissect ion in St roke St udy (CADISS). In t J
1322 St roke 2007;2:292–296
20. Miller NR. Diagn osis an d m anagem en t of dural carot id cavern ou s sin us 26. Donas KP, Mayer D, Guber I, Baum gar t n er R, Gen on i M, Lach at M. En do
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21. Lee VH, Brow n RD Jr, Man drekar JN, Mokri B. In ciden ce an d outcom e of an d level of eviden ce. J Vasc In ter v Radiol 2008;19:1693–1698
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1809–1812 vertebrobasilar arter y an eur ysm s in pat ien t s presen t ing w ith acute sub
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33 Pituitary Apoplexy
Ram i O. Alm eft y, Andrew S. Lit tle, Shih Sing Liu, and W illiam L. W hite

Pit u itar y ap op lexy h as a vascu lar et iology. It occu rs as a resu lt of an d visu al loss. Au topsy fin dings in cluded recen t h em orrh age in
h em orrh age or in farct ion in to a pit uit ar y t um or or n orm al glan d. th e in t rasellar aden om a, en dar terit is of n u m erou s vessels w ith in
Sym ptom s com m on ly in clu de h eadach e, visual acuit y an d visual th e aden ohypophysis, an d preser vat ion of th e p osterior lobe.
field dist urban ces, ext raocular m uscle palsies, an d an im paired Bailey believed th at th e diseased vessels w ith in th e hypophysis
level of con sciousn ess. Th e sym ptom s m ay be sim ilar to th ose of w ere th e source of th e h em orrh age.
rupt u red an eu r ysm s or oth er vascu lar d iseases of th e brain . In 1905, Bleibt reu 19 described a case of pit uitar y apoplexy in
W ith it s p rotean clin ical m an ifest at ion s, p it u it ar y ap op lexy an aden om a. He repor ted th e n ecropsy fin dings in a 21-year-old
becam e associated w it h sym ptom at ic h em or rh age or in farct ion acrom egalic m an w h ose pit u itar y glan d w as replaced by an or-
in an exist ing pit u it ar y aden om a. Sin ce it s or igin al descr ipt ion ange am orphous m aterial. The Polish pathologist Glinski, in 1913,
at th e en d of th e 19th cen t u r y u n t il Brough am an d cow orkers 1 first described exten sive acute n ecrosis of th e an terior pit uitar y
p resen ted t h eir m ileston e p ap er in 1950, t h is clin ical en t it y glan d iden t ified in t w o pat ien t s at n ecropsy.20 Th e first case w as
rem ain ed obscu re. Th ey rep or ted five cases of acu te degen era- a 37-year-old w om an w h o died 9 days after a cesarean sect ion
t ive ch anges in pit u it ar y aden om as an d review ed seven oth er for post par t um h em orrh age secon dar y to u terin e atony. Th e sec-
cases from th e literat u re. Th ey described a clin ical path ological on d case w as a 33-year-old w om an w h o died from congest ive
syn drom e ch aracter ized by an abr u pt on set of h eadach e, am - h ear t failure 6 w eeks after a spon tan eous abor t ion at 6 m on th s
blyop ia, d ip lop ia, d row sin ess, or com a an d ter m ed it pit uitary of gestation. Glinski believed that the necrosis was caused by vas-
apoplexy. cular th rom bosis of th e arteries th at supply the pit uitar y glan d.
We believe t h at t h e ter m pit uitary apoplexy sh ou ld be ap - Sim ilar repor t s associated w ith p ost par t u m h em orrh age, sh ock,
p lied to a clin ical syn drom e th at con sists of a su dden on set of or sepsis follow ed.
any n eurologic or en docrin ologic abn orm alit ies at t ribut able to
h em orrh age or in farct ion in a pit uitar y t u m or or n orm al glan d.
Typ ically, th is syn drom e is ch aracterized by su dden h eadach e, an
alterat ion in m en tal stat us, an im pairm en t of visual field or acu -
it y, ocu lom otor palsies, an d m en ingism us. Fever, acute p it uitar y
■ Pathology
failu re, hyp ot h alam ic dysfu n ct ion , an d d eath m ay follow . Th e Pit u it ar y ap op lexy h as been associated w ith ch rom op h obe ade-
term apoplexy sh ould n ot be used for asym ptom at ic h em orrh age nom as,21–27 acidophilic adenom as 1,11,28–33 basophilic adenom as,34
or in farct ion w ith in a pit u itar y t u m or or glan d. p it u it ar y carcin om as,35 Rat h ke’s cleft cyst s,36 an d m et ast at ic
carcin om as to a p it u itar y aden om a.36 Brough am an d cow orkers 1
suggested th at acidop h ilic ad en om as h ad an in creased propen -
sit y to hem orrh age. Rovit an d Fein 37 suggested that pat ients w ith
en docrinologically active adenom as (acrom egaly or Cushing’s
■ Incidence syn drom e) w ere at in creased risk for th e develop m en t of pit u -
Th e in ciden ce of pit u it ar y t u m or h em orrh ages ranges bet w een it ar y apop lexy com pared w ith th ose w ith n on secret ing ch rom o-
7% an d 25.7% in several series.2–9 Th e in cid en ce of p it u itar y apo- ph obe aden om as. Lop ez 38 an d Wrigh t an d colleagues 35 review ed
plexy ranges bet w een 1% an d 20% (Table 33.1). th e literat u re an d fou n d a h igh er in ciden ce of apop lexy am ong
Th ere ap p ears to be a sligh t m ale predom in an ce (m ale/fem ale p at ien t s w it h ch rom op h obe ad en om as. How ever, t h e associa-
rat io of 1.3:1). A sligh t m ale p redom in an ce am ong 241 pat ien t s t ion of ap oplexy w ith cer t ain h istological t u m or t ypes h as been
w ith pit uit ar y apoplexy w as repor ted in th e literat u re 10 ; 141 pa- refu ted by several au th ors.3,9,10,21,36,39 Th is ap p aren t p referen t ial
t ien ts (58.5%) w ere m ale an d 100 (41.5%) w ere fem ale. Th eir ages associat ion m erely reflects th e dist ribut ion of th e differen t h is-
ranged from 6 to 88 years (m ean age, 46.7 years).11–13 Th is dist ri- tological t yp es of p it u it ar y t u m ors. Moreover, m ost of t h ese
but ion w ould be expected because pit uit ar y aden om as are usu- st u d ies w ere based on t u m or t yp es id en t ified by ligh t m icros-
ally n eoplasm s of adults.14,15 Ch ildren an d adolescen t s represen t copy rat h er th an elect ron m icroscop ic an d im m u n oh istoch em i-
10% of th e total in ciden ce.16,17 cal st u dies.17,40–42 Th e curren t classificat ion of aden om as based
Pit u it ar y ap op lexy in a pit u it ar y aden om a w as first described on elect ron m icroscopy an d im m u n oh istoch em ist r y 17,40,43 h as
by t h e n eu rologist Pearce Bailey 18 in 1898. Th e p at ien t w as a sh ow n th at en docrin ologically act ive aden om as con st it u te 75%
50-year-old alcoh olic an d acrom egalic m an w h o presen ted w ith of all pit uitar y t um ors, w ith a predom in an ce of prolact in om as
su d den h eadach e, n au sea, vom it ing, fever, ocu lom otor p alsies, (in ciden ce ranges from 36 to 46%).

400

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33 Pituitary Apoplexy 401

Table 33.1 The Incidence of Pituitary Apoplexy

Mean Age Apoplexy Headache


Study Cases (Years) Incidence M:F (%)

Onesti et al 1990 36 16 48 2 8:8 88


Ebersold et al 1983 12 13 55 1 8:5 92
Fraioli et al 1990 2 13 3 9:4 62
McFadzean et al 1991 46 15 52 3 8:7 100
Laws and Ebersold 1982 45 11 1.5 7:4 91
Tsitsopoulos et al 1986 101 13 49 17 5:8 85
Hickstein et al 1986 3 10 40 6 5:5 90
Wakai et al 1981 9 51 38 9 28:23 63
Semple et al 2005 56 62 51 4 38:24 87
Lubina et al 2005 52 40 51 2.5 27:13 63
Seuk et al 2011 96 31 42 6 21:8 100
Bills et al 1993 50 37 57 2 25:12 95
Randeva et al 1999 53 35 50 3 21:14 97

or severe en ough to cause un ilateral or bilateral blin dn ess an d


■ Clinical Presentation m ay evolve over h ou rs or days. Vision m ay rem ain n or m al in
It h as lon g been recogn ized t h at a p recip itou s en largem en t of som e pat ien ts.
a pit uitar y aden om a after h em orrh age an d in farct ion causes a Visu al d efects are n ot path ogn om on ic of pit uitar y ap oplexy.
spect r um of clin ical presen tat ion s ranging from th e acute on set Th ey can be d iverse in p at ien t s w it h p it u it ar y ad en om as an d
of h eadach e to d eat h . Th e salt ator y p rogression of sign s an d can m an ifest as bitem p oral, h om onym ou s, or n asal h em ian opsia
sym ptom s in p it u it ar y ap op lexy is com m on an d can evolve an d cen t ral scotom ata,47,48 alth ough bitem poral h em ian opsia is
w it h in h ou rs or w eeks. Weisberg 44 argu ed th at t h e d iagn osis th e m ost frequ en t fin ding in m any series.36,39,44 McFadzean an d
of pit uit ar y apoplexy sh ould be rest ricted to pat ien ts w h ose cow orkers 46 fou n d th at am ong 15 pat ien t s, t w o h ad n orm al vi-
sym ptom s evolve in less th an 48 h ou rs. Alth ough th e p ath ogen - su al fields bilaterally an d on e h ad a fu ll visu al field in on e eye.
esis is en igm at ic, th e var ying clin ical m an ifest at ion s reflect acu te Nin e p at ien t s h ad cen t ral scotom at a an d six p at ien t s h ad classi-
com pression of th e sellar an d p arasellar st r u ct u res; ext rasellar cal bitem p oral field defect s. Petersen an d cow orkers 49 iden t ified
ext ravasat ion of blood or n ecrot ic t issu e in to t h e adjacen t su b - three pat ients w ith pit uitar y apoplexy w ho presented w ith acute
arach n oid spaces an d, rarely, in to th e ven t ricles; an d dest r uct ion m on ocular cen t ral scotom ata an d h eadach es. Th e in it ial diagn o-
of aden o- an d n eurohypophyseal t issues w ith result an t en do- sis w as opt ic n eu rit is. Involvem en t of an opt ic n er ve leading to a
crin opathy. cen t ral un ilateral scotom a is rare. Th e in ciden ce is 1%in pat ien t s
w h o h arbor pit uitar y aden om as. Th e scotom at a m ay be caused
by an an terior exten sion of th e aden om a or a postfixed ch iasm .
Headache Moh r an d associates 48 foun d visual defect s in 74 of 77 pat ien ts
Su dden on set of h eadach e or acu te exacerbat ion of p reexist ing (96%) w ith large pit uitar y aden om as. Fun duscopic fin dings in -
h eadach e is th e m ost com m on sym ptom an d often precedes th e clude a n orm al fu n dus, opt ic at rophy, an d papilledem a. An oth er
appearan ce of any ocular sign s an d sym ptom s. Th e h eadach e is early clin ical sign of opt ic n er ve com p ression m ay be im p air-
often accom p an ied by n au sea an d vom it ing. Headach e is t h e m en t of red vision in the tem p oral field (red desat urat ion ).
m ost com m on sym ptom an d h erald ed th e on set of ap op lexy Lateral exten sion of th e t u m or in to th e cavern ous sin us m ay
in rough ly 80% of cases (Table 33.1).2,6,9,12,36,45,46 Th e h eadach e cau se diplop ia an d op h th alm op legia, involvem en t of th e sym pa-
resem bles th at associated w ith su barach n oid h em orrh age (SAH) th et ic ch ain along th e carot id ar ter y w ith resu lt an t Horn er’s syn -
an d is described as excr uciat ing w ith an abrupt on set . Locat ion drom e, t rigem in al n er ve dysfu n ct ion , n arrow ing or occlu sion of
m ay be fron totem poral, ret ro-orbital, un ilateral, or diffuse, an d th e cavern ou s in tern al carot id ar ter y, an d im pairm en t of ven ous
is seldom localized in th e occip ital region . Th e h eadach e is usu - ret u rn from th e orbit s. Im p airm en t of ven ous ret u rn from th e
ally at t ribu table to m en ingeal irritat ion , disten t ion of th e dura, orbit s cau ses proptosis an d sw elling of th e eyelid.
an d possible irritat ion of th e first division of th e t rigem in al n er ve
in th e cavern ou s sin u s.
Cranial Nerve Palsies
Isolated or m ult iple cran ial n er ve palsies an d un ilateral or bilat-
Visual Deterioration eral op h th alm oplegia m ay occu r.8,35,50–58 Th e th ird cran ial n er ve
Abrupt deteriorat ion of visual acuit y an d fields is often regarded is the m ost frequently involved,12,36,43,51,53–56 follow ed by the sixth
as a h allm ark of pit u itar y apoplexy. Th e visu al loss m ay be m ild cranial ner ve.10,43,51,53–56 Th e trochlear ner ve is involved less often

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402 III Ischemic Stroke and Vascular Insufficiency

an d is difficu lt to access in pat ien t s w h o are drow sy.7,36,58 Im - t ion 9,21,24,27,36,44,56,75 ; bou t s of cough ing 21 ; an t icoagu lat ion 25,37,57 ;
pingem en t on th e op h th alm ic division of th e t rigem in al n er ve th rom bocytopen ia 57,76 ; brom ocript in e th erapy 36 ; pregn an cy 4,36 ;
can cau se u n ilateral facial pain , hyp esth esia, an d loss of corn eal gast roen terit is 24,38 ; TRH-st im u lat ion test 24 ; oral surger y 15 ; dia-
reflexes.29,35,58 betic ketoacidosis 1,13 ; adren alectom y 34,37 ; hypotension 1 ; and TRH
Con cu rren t ocu lom otor p alsies m ay be con fu sed w ith cavern - an d gon adot ropin -releasing h orm on e (Gn RH) test ing.23
ous sin us th rom bosis or carot id cavern ous fist ula.59 Coexisten t
pit u it ar y aden om a an d carot id cavern ous fist ula are rare.60 Ocu -
lar m otor p alsies m ay be associated w ith a gradu al en largem en t Ischemia and Hemorrhage
of th e pit uitar y aden om a.47,58,61,62 Trau t m an n an d Law s 63 fou n d In terest ing but con t roversial th eories h ave been for w arded to ac-
p reop erat ive ext raocu lar m u scle p alsies in on ly 12 of 851 p a- cou n t for th e path ogen esis of pit u itar y ap oplexy. Th e roles of
t ien t s w it h p it u it ar y ad en om as; t h e t h ird cran ial n er ve w as ischem ia and hem orrhage in apoplexy, both of w hich are com m on
affected in 11 pat ien t s an d th e sixth cran ial n er ve w as affected path ological findings, are debatable.28,29,58,59 In his classic descrip -
in on e pat ien t . Wilson an d Dem p sey 42 reported im paired ocu lar tion of pit u itar y ap oplexy, Bailey 18 im p licated th e en darterit is
m ot ilit y in 12 of 250 p at ien t s (4.8%). fou n d w ith in th e hypophysis as th e source of th e h em orrh age.
Dip lop ia is a com m on com p lain t in aler t p at ien t s an d im - Brough am an d cow orkers 1 p roposed th at both h em orrh age an d
p licates involvem en t of t h e ocu lom otor, t roch lear, an d abd u - n ecrosis are caused by th e rapid grow th of th e aden om a, w h ich
cen t n er ves.8,37,43,44,49,58,64,65 Rarely is it secon dar y to n onp aret ic ou tst rips its vascular su pply.
diplop ia.66 Rovit an d Fein 37 suggested th at t h e com p ression of th e p it u -
it ar y stalk an d portal vessels at th e diaph ragm at ic n otch by ex-
pan ding th e t u m or is th e in it iat ing even t . Th e com p ression leads
Hypotension to isch em ia of th e glan d an d aden om a. Th e cavern ous sin us is
Hypoth alam ic involvem en t can cause hypoten sion ,1,8,27,31 fever,27 d istor ted , an d t h e in t racaver n ou s carot id ar ter y an d in fer ior
hypotherm ia,44 cardiac arrhyth m ias, and respirator y difficult ies.10 hypophyseal arteries are com pressed. Furth er isch em ia of th e
Hypoten sion m ay in dicate a cor t icot ropin (adren ocor t icot ropic pit u it ar y, aden om a, dien ceph alon , an d visual apparat u s develop .
h orm on e [ACTH])-adren al in su fficien cy or a fluid an d elect ro- Ebersold an d colleagues 12 su p por ted th is th eor y becau se th rom -
lyte im balan ce.25 bosis w ith in th e sin usoids of th e pit u itar y aden om a w as a con -
sisten t feat u re in th eir p atien ts w ith p it uitar y apoplexy.
Alth ough both vascular in sufficien cy 1 an d com pression 37 m ay
Meningismus, Fever, and Altered Mental Status be involved w h en pit uitar y apoplexy is associated w ith large t u -
Meningism us, ph otophobia, fever, an d alteration in m en tal stat us m ors, n eith er exp lain s th e occu rren ce of h em orrh age an d in farc-
are com m on .5,27,30,44 Th e cerebrosp in al flu id (CSF) is frequ en tly t ion in sm all aden om as.3 Th e con cept of vascu lar in sufficien cy
bloody, xan th och rom ic, or clou dy du e to ext ravasat ion of blood h as also been refu ted by oth ers based on t h e blood su p p ly to
or n ecrot ic t issue into th e subarach n oid spaces.5,35,67 How ever, pituitary adenom as and norm al pituitary glands as dem onstrated
th e CSF is clear if th e h em orrh age rem ain s con fin ed w ith in th e angiograph ically an d at autopsy.2,10,58
t u m or.32,37,58 Pleocytosis in th e CSF is com m on ,68–74 an d its p ro- Moh an t y an d cow orkers 5,8 believe th at t h e p rop en sit y for
tein con ten t is often raised.27,30 h em orrh age an d in farct ion is directly related to th e size an d vas-
Alteration in m ental status m ay range from lethargy to com a.31 cularit y of th e t u m or. Oth ers have con cluded th at h em orrh age
Ch anges in m en t al stat u s h ave been at t ribu ted to involvem en t of an d n ecrosis are related to th e fragilit y of th e t u m oral vessels.3,5,8
th e hyp oth alam u s, SAH, u n cal h ern iat ion , an d in creased in t ra- Un der elect ron m icroscopy, th e basal m em bran e of t um or ves-
cran ial pressu re from a rapid expan sion of th e t um or, elect rolyte sels can ap p ear th icken ed an d m u lt ilayered, an d th e en d oth elial
im balan ce, an d en docrin op athy.29 Frequ en tly th ese pat ien t s cells are often sw ollen w it h loss of fen est rat ion .77 Gorczyca
h ave n o over t eviden ce of en docrinopathy.10,27,31,32,37,60 Cardoso an d Hardy 78 fur th er post ulated th at th ese t um oral vessels, h av-
an d Peterson 10 foun d th at 64%w ere un aw are of h arboring a pit u- ing origin ated from th e in ferior hyp ophyseal arteries, are un der
itar y aden om a. h igh er pressu re com pared w ith th e pressure in th e sin usoids of
th e aden ohypop hysis. Th is h igh p ressu re m ay be resp on sible for
sp on t an eou s h em orrh ages w ith in pit u itar y aden om as.

■ Other Presentations
Pathogenesis ■ Radiological Studies
Desp ite th e est ablish ed m an ifestat ion s of p it u itar y apoplexy, its Th e cu rren t n eu roradiological st u dy of ch oice for evalu at ion of
path ogen esis rem ain s u n cer tain . Most cases are n ot associated th e sellar an d p arasellar region is m agn et ic reson an ce im aging
w it h an teced en t even t s, alth ough a w id e sp ect r u m of p red is- (MRI). Abn orm al skull radiograph s an d tom ogram s can provide
p osing factors h ave been rep or ted in t h e literat u re. Th ese fac- a diagn ost ic clue of a pit uit ar y disorder, especially in pat ien ts
tors in clu de cardiac su rger y 55–57 ; pn eu m oen ceph alogram 8,27,31,37 ; w ith out any prem orbid en docrin ologic disorder, but such path o-
carot id an giograp hy 12 ; t r ip le b olu s t est w it h in su lin , t hyro - logical fin dings are n ot sp ecific for p it uitar y ap oplexy.79 Th ese
t rop in -releasin g h or m on e (TRH), an d lu t ein izin g h or m on e – n on specific fin dings in clude en largem en t of th e sella, a dou ble
releasing horm one (LHRH)22 ; closed head injur y 1,15,36,56,58 ; radia- floor of th e sella, erosion an d dem in eralizat ion of th e dorsum

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33 Pituitary Apoplexy 403

sellae th at u n derm in es th e an terior clin oids, a soft t issu e m ass scans did not reveal h em orrhages. Rachlin and cow orkers 76 foun d
w ith in th e sph en oid sin u s, an d path ological calcificat ion s.4,21,27,31 th at MRI dem on st rates areas of h em orrh ages w ith in th e t u m or
Occasionally, pituitar y apoplexy is associated w ith a norm al sella m ore often th an do CT scan s (100% versus 38%).
t urcica.34

Computed Tomography ■ Differential Diagnosis


Com pu ted tom ograp hy (CT) scan s often sh ow en largem en t or An accurate an d prom pt diagn osis is cr ucial in th e m an agem en t
dest ru ct ion of th e sella, w ith or w ith ou t sp h en oid sin u s opacifi- of p it u it ar y ap op lexy. Er rors in d iagn osis h ave been com m on ,
cat ion . Oth er abn orm alit ies th at m ay suggest p it u itar y apoplexy esp ecially before th e availabilit y of CT an d MRI. A failu re to diag-
dep en d on w h eth er th e cau se is h em orrh age or in farct ion in th e n ose pit uitar y apoplexy can lead to un favorable outcom es, espe-
p it u it ar y glan d or t h e t u m or, an d on t h e in ter val bet w een t h e cially w h en vision is th reaten ed. An eur ysm al SAH an d m en ingit is
ict us an d th e CT scan .26 are th e t w o m ost com m on con dit ion s con sidered in th e differen -
Com pu ted tom ograp hy scan s sh ou ld be p erform ed w ith an d t ial diagn osis. Oth er less com m on path ologies in clu de p it u itar y
w ith ou t con t rast in t h e a xial sect ion s an d in 1.0- or 1.5-m m abscess, postoperative intrasellar hem atom a, cerebrovascular ac-
d irect coron al sect ion s follow ing in t raven ous con t rast adm in is- cidents, cavernous sinus throm bosis, intrachiasm atic vascular m al-
t ration . If in t rat u m oral h em orrh age is p resen t , th e CT scan s ob - form at ion , com plicated m igrain es, ver tebrobasilar in sufficien cy,
tained during th e acute ph ase (~ 3 days) m ay sh ow hyperden se tem poral ar terit is, an d cen t ral ret in al ar ter y or vein occlusion .
sign al w it h in t h e ad e n om a (Fig. 33.1a,b).1 2,36 ,60 Th is acu te
h e m orrh age can exten d in to th e su prasellar cistern s an d su b -
arach n oid spaces, resem bling SAH from a rupt ured an eu r ysm 60 ; Aneurysm
occasion ally it can exten d in to th e ven t ricles 80–82 or th e brain Th e su d d en on set of h eadach e often associated w it h n au sea
paren chym a.83 an d vom it ing is th e m ost com m on sym ptom in pit uitar y apo-
W h en ap op lexy is cau sed by a blan d in farct ion or in th e p res- plexy.13,27,58,76 It m ay be associated w ith alterat ion in m en tal sta-
en ce of a resolving h em atom a, th e m ass m ay be hypoden se or t u s 31,80 an d n eck st iffn ess.12,21,36 Th ese sym ptom s can be difficu lt
isod en se, often w it h a r in g en h an cem en t .80 Th is ap p earan ce, to differen t iate from a presen tat ion associated w ith a rupt ured
h ow ever, is n ot p at h ogn om on ic of ap op lexy an d is easily con - an eur ysm . Alth ough visu al field defect s an d oculom otor palsies
fu sed w it h cyst ic d egen erat ion , abscesses, an d u n com p licated are frequ en t fin dings associated w ith p it uitar y apoplexy, th ey
aden om as.84 can also be cau sed by large an eu r ysm s th at involve th e an terior
circulat ion .

Magnetic Resonance Imaging


Pituitary Abscess
Magn et ic reson an ce im agin g is th e st u dy of ch oice for eval-
u at in g t h e p it u it ar y glan d an d t h e p arasellar st r u ct u res (Fig. Pit u it ar y abscesses are rare; m ost becom e sym ptom at ic w ith
33.1c– e ).85,86 On T1-w eigh ted im ages, m icroaden om as are u su - h eadach e, decreased visu al acu it y, visu al field defects (u sually
ally hypoin ten se relat ive to th e pit uitar y glan d an d isoin ten se bitem poral h em ian opsia), an terior an d posterior lobe dysfun c-
relat ive to th e gray m at ter. On T2-w eigh ted im ages, m icroaden o- t ion , n eck st iffn ess, an d fever. Recu r ren t m en in git is w it h CSF
m as appear hyperintense. The signal intensit y of m acroadenom as rh in orrh ea is com m on am ong affected pat ien ts.87 Most of th ese
is often h eterogen eous du e to areas of h em orrh age, in farct ion , or pat ien ts h ave an in dolen t an d prot racted cou rse.87 In rare cases,
cyst ic form at ion . pit u it ar y abscesses m ay evolve rap idly in a fu lm in at ing cou rse
Pituitar y infarction w ith subsequent cystic ch anges can be dif- th at sim u lates p it uit ar y apoplexy.71,88 In th ese cases, th e sym p -
ferentiated from chronic h em orrhages on MRI st udies. The cystic tom s are alterat ion of m en tal st at u s, n ausea an d vom it ing, acute
areas are hypoin ten se or sligh tly hyperin ten se on T1-w eigh ted on set or severe exacerbat ion of h eadach e, fever, n eck st iffn ess,
im ages, depending on the protein content in the fluid, and hyper- h em ip aresis,87 sixt h cran ial n er ve p alsy,88 t h ird n er ve p alsy,87
in ten se on T2-w eigh ted im ages. Un like CT scan s, MRI is sen sit ive op h t h alm op legia,71 dysest h esia in t h e d ist r ibu t ion of t h e first
in detect ing subacu te an d ch ron ic h em orrh ages w ith in th e p it u- an d secon d divisions of th e t rigem in al n er ve,71 an d blin dn ess.88
itar y aden om a.36 Th e h em orrh age in to a pit u itar y aden om a re- Th ese pat ien t s ten d to h ave an associated in t rasellar t u m or, u su -
sem bles th at associated w ith in t racerebral h em atom as. An acu te ally a pit u itar y aden om a.71,87,88
(less th an 7 days old) h em atom a is isoin ten se or sligh tly hypo- Dist ingu ish ing bet w een pit u itar y apoplexy an d a pit uitar y
in ten se relat ive to gray m at ter on T1-w eigh ted im ages an d hypo- abscess can be difficu lt , as th e clin ical h istor y, a physical exam i-
in ten se on T2-w eigh ted im ages. A su bacu te h em atom a (greater n at ion , presen ce of CSF pleocytosis, an d CT scan fin dings can be
th an 7 days bu t less th an 1 m on th old) is in it ially hyp erin ten se identical. This difficult y is further com pounded by the propensit y
on T1-w eigh ted im ages an d th en is hyperin ten se on T2-w eigh ted of pituitar y abscesses to be associated w ith pituitary adenom as.
im ages becau se of th e p aram agn et ic effects of m eth em oglobin . Bot h are for m idable lesion s an d requ ire p rom pt an d accu rate
On est i an d cow orkers 36 rep or ted th at in th eir 16 p at ien t s w ith d iagn osis. It is th erefore reason able to com m en ce preoperat ive
pituitary apoplexy, nine of 10 MRIs and six of 15 CT scans showed an tibiot ics an d st ress dose cor t icosteroids if pit uitar y apoplexy
ch anges con sisten t w ith h em orrh age. Th e MRIs id en t ified h em - is con sidered likely before proceeding to su rgical in ter ven t ion . If
orrh ages in th e pit uit ar y aden om as of four pat ien ts w h ose CT th ere is n o p rom pt im provem en t w ith app ropriate an t ibiot ic an d

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404 III Ischemic Stroke and Vascular Insufficiency

a b

c d e

Fig. 33.1a–e A 50-year-old woman who presented with headache of 2 (c), T2 (d), and contrasted T1 (e) m agnetic resonance im aging scans bet ter
days’ duration and a left third nerve palsy. (a,b) Noncontrasted computed delineate a heterogeneous sellar m ass extending into the cavernous sinus
tomography scan findings include a sellar m ass extending into the cavern- and suprasellar area with areas of T1 hyperintensit y. (Courtesy of Barrow
ous sinus with intrinsic hyperdensit y suggestive of hem orrhage. Coronal T1 Neurological Institute.)

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33 Pituitary Apoplexy 405

cor t icosteroid th erapy, explorat ion an d drain age via th e t ran s- 33.2 details th e recover y rates in recen t series. Of par t icular in -
sph en oidal ap proach are m an dator y. terest is the prognosis of blind eyes in pit uitar y apoplexy. Agrawal
an d Mah apat ra 90 st udied 14 blin d eyes in eigh t pat ien ts, repre-
sen t ing 35% of their apoplexy p op ulat ion . Neu rosurgical con sul-
Ischemic Necrosis in a Normal Pituitary Gland tat ion w as delayed a m ean of 10 days. All pat ien t s w ere operated
(Sheehan’s Syndrome) on w ith in 24 h ours of adm ission . Th ree eyes (from t w o pat ien ts)
h ad com plete recover y of vision . An addit ion al four eyes (from
Isch em ic n ecrosis in a n orm al pit uitar y glan d rarely becom es
t w o patients) recovered to greater th an 2/60. All of th ese patients
dram at ically sym ptom at ic. Most of th e p at ien t s exh ibit variou s
w ere operated on w ith in 7 days. Muth ukum ar et al91 review ed
degrees of pit uit ar y dysfu n ct ion if th ey su r vive th e in it ial in su lt .
th e cases of fou r p at ien t s—th ree w ith u n ilateral blin dn ess an d
Ap oplexy, in th e absen ce of a p it u it ar y t u m or, is best st udied in
on e w ith bilateral blin dn ess. Th e on e pat ien t w h o w as blin d in
pat ien ts w ith Sh eeh an’s syn drom e.
both eyes un der w en t surger y 7 days follow ing apoplexy an d re-
Th e diagn osis of Sh eeh an’s syn d rom e in pregn an t w om en is
covered to 6/9 an d 6/12 vision . Tw o p at ien t s operated 2 an d 3
frequ en tly delayed. Th e in ter val bet w een deliver y of a ch ild an d
w eeks after th e even t both recovered to 6/60 vision . On e pat ien t
diagn osis h as ranged from 1 h ou r to 47 years (m ean , 6.8 to 10.5
operated on 2 m on th s after apoplexy h ad 1/60 vision on follow -
years).89 In the vast m ajorit y of cases, pan hypopit uitarism occurs
u p . In Sem p le et al’s 56 ser ies of 62 p at ien t s, six p at ien t s w ere
if th e an terior pit u it ar y glan d h as been dest royed. Th e h orm on al
blin d an d n on e recovered . Sp ecifics on t h ese p at ien t s are n ot
loss u su ally occu rs in th e follow ing sequ en ce: grow th h orm on e,
provided; h ow ever, th e average delay in n eu rosu rgical con su lta-
lu tein izing h orm on e, follicle-st im u lat ing h orm on e, thyrot ropin
t ion w as 14 days. Th ere is a con sen su s th at recover y of ocu lom o-
(thyroid-st im u lat ing h orm on e [TSH]), ACTH, an d p rolact in .
tor deficits is m ore predict able an d occurs earlier th an recover y
Alth ough Sh eeh an’s syn drom e is rare in developed coun t ries,
of visual acuit y an d field deficits.3,8,24,39,45,60
it sh ould be con sidered in th e differen t ial diagn osis of w om en
Long-ter m follow -u p of p at ien t s w it h p it u it ar y ap op lexy
w ith eviden ce of en docrin e failure an d a h istor y of a com plicated
t reated con ser vat ively h ave sh ow n eith er involu t ion or recu r-
deliver y. Th e m ain d ifferen t ial diagn osis of p ost part u m hypopi-
ren ce of th e t um or,54,55,57,92 en docrin op athy,27,32 an d recu rren t
t u itarism is lym p h ocyt ic hyp op hysit is, an au toim m u n e disorder
apoplexy w ith in days to years of th e in it ial ict us.27,31 Th e involu -
th at occurs du ring or after deliver y.
t ion of th e t u m or can cau se a com p letely or par t ially em pt y sella.
Pit u it ar y ap op lexy often occu rs in previou sly un diagn osed
cases of p it u it ar y aden om as.10,12 Approxim ately 30 to 50% h ave
a p reexist ing en docrin op athy,12 w h ich often con t ribu tes to th e
■ Prognosis m or talit y an d m orbidit y. Norm al pit uit ar y fun ct ion seldom fol-
Th e clin ical cou rse of pit u it ar y ap op lexy is u np redict able. It can low s p it u it ar y ap op lexy. Det ailed evalu at ion of t h e h or m on al
be m ild, w ith spon t an eous resolut ion of th e preexist ing en docri- st at u s in th ese p at ien t s often reveals a h igh p revalen ce of m on o-
n opathy 13 an d visu al p roblem s, in clu ding visu al acu it y, visu al t rop ic, m u lt it rop ic, or p an t rop ic failu re of th e an ter ior lobe of
field defects, an d oculom otor palsies.35 It can also be leth al.27,80,82 t h e p it u itar y glan d. Horm on al ou tcom es in recen t series are re-
Recen tly, th e m or talit y an d m orbidit y associated w ith th is con - view ed in Table 33.3.
dit ion h ave decreased as a resu lt of im p roved, faster, an d m ore In a review of th e w orld literat u re, Veldh uis an d Ham m on d 33
accurate radiological diagn osis, surgical tech n iques, an d steroid fou n d th at 88% of pat ien t s w ith pit uitar y apoplexy h ad grow th
replacem en t . h orm on e deficien cy, 66% h ad ACTH-adren al in sufficien cy, 44%
In 1970, Lopez 38 iden t ified 135 cases of pit u itar y apoplexy in w ere hypothyroid, an d 67% h ad hypogon adot ropic hypogon ad-
th e w orld literat u re. Seven t y-five cases w ere w ell described, an d ism . Of th eir ow n fou r pat ien t s, t w o h ad hyperprolact in em ia,
h e fou n d th at 29 of th ese 75 pat ien ts died w ith out surger y. Of on e h ad hypoprolact in em ia, an d th e four th did n ot secrete pro-
th e 46 pat ien t s w h o u n der w en t su rger y, 39 su r vived. Th e over- lact in . Rach lin an d colleagu es 76 reported th at n in e of 32 pat ien ts
all m or t alit y rate w as 48%, an d th e su rgical m ort alit y w as 15%. (28%) required h orm on al replacem en t . Arafah an d associates 93
Taylor an d colleagues 13 fou n d six death s in 25 p at ien t s w ith as- reported significant im provem ent in pituitary function after early
sociated acrom egaly an d ap oplexy. Law s an d Ebersold 45 rep orted surgical decom pression .
n o m or t alit y or m orbid it y in t h eir series, bu t On est i an d asso - Involve m e n t of t h e p ost e r ior lobe is u n u su al (Table
ciates,36 Hickstein an d cow orkers,3 an d oth ers h ave rep or ted a 3 3.3).4 ,1 3 ,2 5,3 4 ,42 ,76 ,9 3 Veldh uis an d Ham m on d 33 rep or ted a 4% in -
m or talit y rate bet w een 3.1% an d 21.4%.2,12,44,76 cid en ce of t ran sien t d iabetes in sip id u s an d a 2% in cid en ce of
Visu al field, visual acu it y, an d ocu lar m ot ilit y deficits are p er m an en t diabetes in sipidu s after p it uitar y apoplexy. Rach lin
com m on in pit uit ar y ap op lexy. Im p rovem en t of visu al loss is of and cow orkers 76 ident ified 10 patients (31%) w h o developed tran -
prim ar y im por tan ce in th e m an agem en t of p it uitar y apop lexy. sien t diabetes in sip idu s after su rger y an d on e pat ien ts (3%) w h o
In m ost cases som e degree of recover y is accom p lish ed. Table developed perm an en t diabetes in sip idus.

Neurosurgery Books Full


406

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III Ischemic Stroke and Vascular Insufficiency

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33 Pituitary Apoplexy 407

Table 33.3 A Summary of Endocrinologic Outcomes After Pituitary Apoplexy

Patients: Panhypopituitary Hypothyroid at Hypoadrenal at Hypogonadal at Hormone


Total/ at Presentation/ Presentation/ Presentation/ Presentation/ Replacement on Diabetes
Study, Year Surgery Follow -Up (%) Follow -Up (%) Follow -Up (%) Follow -Up (%) Follow -Up (%) Insipidus (%)

Semple et al 62/58 ?/? 55/? 38/? 25/? 77 Transient, 5


2005 56 Permanent, 9
Gruber et al 30/10 ?/? ?/69 ?/66 ?/82 90 Permanent, 28
2006 57
Bills et al 1993 50 37/36 ?/? ?/89 ?/82 ?/64 ≥ 89 Transient, 20
Permanent, 11
Lubina et al 40/34 ?/27 52/54 15/40 ?/79 86 Transient, 35
2005 52 Permanent, 8
Arafah et al 8/8 25/0 38/12 88/12 75/38 ? Transient, 50
1989 93 Permanent, 0
Ayuk et al 2004 54 33/15 ?/? 37/67 50/79 72/76 ≥ 79 ?
Randeva et al 35/31 ?/? 50/45 76/58 79/43 ≥ 58 Transient, 16
1999 53 Permanent, 6
Sibal et al 2004 55 45/27 ?/? 57/? 60/? 76/? 84 ?

com e. Th ree p at ien t s died, an d h em ip aresis resolved in t w o of


■ Treatment th e six pat ien ts w h o h ad th is sym ptom .
Medical Th e t ran ssph en oidal ap p roach is recom m en ded in m ost cases
of p it u it ar y ap op lexy,4,42,43 as it is associated w it h a low m or-
Th e m an agem en t of pit u it ar y ap op lexy dep en ds on th e t yp e an d t alit y an d m orbid it y.42,63 Cran iotom y m ay be con sid ered for
severit y of sym ptom s, p ar t icu larly th e rate of progression of th e p at ien ts w ith large suprasellar exten sion s, n on aerated sph en oid
n eu rologic deficit s.3,21,80,93 Con sidering th e h igh prevalen ce of sin u ses, n orm al sellae t u rcica, coexisten t an eu r ysm s, or com p li-
adren al in su fficien cy, h igh doses of steroids sh ou ld be adm in is- cations from in tracerebral hem atom as.44 In the 1970s, Zervas and
tered.33,93 Steroid th erapy m ay also im prove visual fu n ct ion .13,27 Men delson 100 an d Ber t i an d cow orkers 21 advocated stereotact ic
Becau se m ost pat ien t s h ave variable an terior p it uitar y dysfu n c- t ran ssph en oidal aspirat ion of th e n ecrot ic t u m or in seriou sly ill
t ion , t h e p at ien t ’s en d ocr in ologic st at u s sh ou ld be assessed , pat ien ts.
w it h t h e ap p rop riate rep lacem en t t h erapy adm in istered w h en
possible.3,30,33
Fluid and electrolyte im balance should be m onitored carefully. Surgery Versus Conservative Therapy
Tran sien t diabetes in sip idu s 4,24,43,76 an d rarely th e syn drom e of
Su rger y h as t rad it ion ally been recom m en ded in th e set t ing of
in appropriate secret ion of an t idiabet ic h orm on e (SIADH)3 m ay
pit u it ar y ap op lexy w ith visu al or n eu ro-oph th alm ologic deficits.
occur secon dar y to involvem en t of th e hypoth alam ic-pit uit ar y
In th e absen ce of any n eurologic deficit , n on operat ive m an age-
axis. Th e serum glucose an d in sulin requirem en ts of patien ts
m en t involving steroids, elect rolyte an d fluid replacem en t , an d
w ith diabetes m ellit us sh ou ld be m on itored closely, because the
h em odyn am ic su ppor t is appropriate. How ever, an in creasing
diabetes m ellit us often regresses.1,13 Brom ocript ine has also been
n um ber of st udies suggest a t rial of con ser vat ive th erapy can be
used as an adjun ct in patien ts w ith hyperprolactin em ia.49,100
at tem pted , even in th e presen ce of visu al loss.54,55,57,95 Th ere is
addit ion al support for th is in th e set t ing of cran ial n europath ies
alon e. Sibal et al55 review ed 45 pat ien t s, 18 being m an aged con -
Surgical ser vat ively, an d fou n d th at all pat ien t s w h o did n ot un dergo su r-
Desp ite rep or t s of sp on t an eou s recover y w it h con ser vat ive ger y h ad com plete or n ear-com p lete resolut ion of visual acuit y,
t reat m en t ,27,54,55,57,94,95 m ost au t h ors advocate su rgical d e- visu al field d eficit s, an d cran ial n eu rop at h ies. Th ey con clu d ed
com p ression in p at ien t s w it h visu al loss or n eu rologic d efi- t h at p at ien t s w it h m ild , n onp rogressive n eu ro -op h t h alm ologic
cit s.4,10,37,43,46,50–53,56,59,76,93,96 Th e t im in g of su rger y rem ain s sign s can be m an aged con ser vat ively. Maccagn an et al95 in it iated
con t roversial. Most agree th at em ergen t su rgical in ter ven t ion con ser vat ive m easu res in each of th eir 15 pat ien t s. Su rger y w as
sh ou ld be reser ved for m edically st able p at ien t s w it h severe reser ved for pat ien t s w h o failed to im prove in term s of visual
n eu rologic dysfun ct ion an d severe visual loss.10,43–45,76 In con - loss or im pairm en t of con sciou sn ess w ith in th e first w eek or
t rast , oph th alm oplegia an d isolated or m u lt iple cran ial n er ve th ose w h ose sign s or sym ptom s ret u rn ed on discon t in uat ion of
p alsies are n ot absolu te cr iter ia for em ergen t su rgical in ter ven - d exam et h ason e. Visu al acu it y (n = 2) an d cran ial n eu rop ath ies
t ion , as t h ey often resolve sp on t an eou sly.10,13,27,60 Su rgical ex- (n = 7) im proved in each pat ien t in cluding com plete resolut ion in
p erien ce w ith focal h em isph eric deficits an d occlusion of th e each of th e p at ien t s w ith visu al acu it y deficit an d six of th ose
in tern al carot id, an terior, an d m iddle cerebral arteries is lim - w ith cran ial n europath ies. Ayuk et al54 m an aged 18 of 33 pa-
ited.34,37,69,70,83,97–99 Em ergen t su rger y w as perform ed in five of t ien t s w ith st able or im p roving visu al fun ct ion con ser vat ively.
th e seven rep or ted cases an d h ad a gen erally u n favorable ou t- Visu al deficit s (n = 6) an d cran ial n eu ropath ies (n = 7) resolved in

Neurosurgery Books Full


408 III Ischemic Stroke and Vascular Insufficiency

all of th e p at ien t s m an aged con ser vat ively. In Gr u ber et al’s 57 to delay su rger y, prom pt decom pression is recom m en ded. How -
series of 30 pat ien ts, 20 w ith stable or im proving vision w ere ever, th ose pat ien t s w h o are deem ed un stable or h igh risk in th e
m an aged w ith out surger y. Loss of visu al acu it y, field, an d op h - early period m ay st ill ben efit from delayed surger y.
th alm op legia im p roved in seven of seven , th ree of fou r, an d 12 of
12 p at ien ts, respect ively, w h ich w as com p arable to th e su rgical
resu lt s. Radiation
Desp ite in creasing su p p or t for a t rial of con ser vat ive th erapy, Rad iat ion t h erapy h as been advocated for t h e m an agem en t of
m any auth ors st ill advocate early surgical decom pression w h en p it uitar y apop lexy, especially in pat ien ts w h o are too ill to w ith -
visu al dist u rban ces are p resen t .46,50–53,56,93,96 How ever, th ere are st an d su rgical in ter ven t ion .30,37,98 It h as been recom m en d ed as
con flict ing resu lts on w h eth er th e t im ing of su rger y affects ou t- an adjun ct after surgical decom pression , because t um or recur-
com e. Seu k et al,96 in a series of 31 pat ien ts t reated surgically, rence is com m on.24,45,71,76,100 Others believe that radiation therapy
foun d a sign ifican t differen ce in visual outcom e in pat ien t s oper- sh ould be reser ved for t um or recu rren ce.10
ated on w ith in 48 h ou rs. Bills et al50 foun d a sign ifican t differ-
en ce in visu al acu it y ou tcom e in 36 su rgically t reated p at ien t s
w h en surger y w as perform ed w ith in 7 days. Th is series in cluded
th ree p at ien t s w h o recovered from blin dn ess, t w o of w h om did
so com pletely.50 Muth ukum ar et al,91 in th eir st u dy of recover y
■ Conclusion
from blin d eyes, fou n d on ly excellen t ou tcom es in th ose op er- Pit u it ar y apop lexy is a clin ical syn drom e th at occu rs as a resu lt
ated on w ith in 1 w eek. In 31 su rgically t reated pat ien ts, Ran deva of h em orrh age or in farct ion in to a pit uitar y aden om a or, less
et al53 fou n d a sign ifican t d ifferen ce in t h ose t reated w it h in com m on ly, in to a n orm al pit u it ar y glan d. It is associated w ith a
8 days. Conversely, in relat ively large series, McFadzean et al,46 w ide spect ru m of sign s an d sym ptom s th at range from h ead-
Sibal et al,55 an d Ayuk et al54 did n ot fin d th at t im ing of surger y ach e, visu al loss, oph th alm oplegia, an d acu te pit uit ar y failure to
m ade a sign ifican t differen ce in visual outcom e. Few cases h ave su dden death . Alth ough su rgical an d m edical t reat m en ts for pi-
been described in w h ich em ergen t surger y h as been perform ed; t u itar y apop lexy h ave im proved over th e years, it s p ath ophysiol-
as a result , it is difficult to m ake recom m en dat ion s regarding it s ogy rem ain s con t roversial. CT an d preferably MRI sh ould be u sed
n ecessit y or ben efit . How ever, m any auth ors st ill recom m en d to evaluate these patients. Lum bar puncture an d angiography are
em ergen t decom p ression in th e case of blin dn ess or severe vi- seldom in dicated. Exten sive p re- an d p ostop erat ive evalu at ion s
su al deficit . of th e pat ien t’s en docrin ologic stat us are n eeded, an d t ran ssph e-
Based on t h e available evid en ce, an in it ial t r ial of con ser va- n oidal decom pression sh ould be perform ed prom ptly in cases of
t ive m easu res in p at ien t s w ith m ild deficits is likely to be a safe w orsen ing vision or n eu rologic deficit . Radiat ion th erapy sh ou ld
st rategy. Pat ien t s w h o do n ot im p rove or w h o w orsen sh ou ld be be con sidered for recu rren ces or in com plete rem oval of t u m or.
t reated surgically. Given th at th ere is som e eviden ce th at early Vasospasm sh ould be suspected in pat ien t s w ith a n ew n euro-
su rger y im p roves ou tcom e, in th e absen ce of com pelling reason s logic deficit or a prot racted cou rse after pit u it ar y ap oplexy.

References
1. Brough am M, Heu sn er AP, Adam s RD. Acu te d egen erat ive ch anges in 12. Ebersold MJ, Law s ER Jr, Sch eith auer BW, Ran dall RV. Pit uit ar y apoplexy
ad enom as of th e pit uit ar y body—w ith special referen ce to pit uit ar y apo- t reated by t ran ssph enoidal surger y. A clin icopath ological and im m un ocy-
plexy. J Neu rosurg 1950;7:421–439 toch em ical st udy. J Neurosurg 1983;58:315–320
2. Fraioli B, Esposito V, Palm a L, Can tore G. Hem orrh agic pit uit ar y aden o- 13. Taylor AL, Fin ster JL, Raskin P, Field JB, Min t z DH. Pit uit ar y apoplexy in
m as: clin icopath ological feat ures and surgical t reat m ent . Neurosurger y acrom egaly. J Clin Endocrin ol Met ab 1968;28:1784–1792
1990;27:741–747, discussion 747–748 14. Bakay L. Th e result s of 300 pit uit ar y adenom a operat ion s (Prof. Herber t
3. Hickstein DD, Ch an dler W F, Marsh all JC. Th e spect rum of pit uit ar y ade- Olivecron a’s series). J Neu rosu rg 1950;7:240–255
n om a h em orrhage. West J Med 1986;144:433–436 15. Jefferson AA. Som e clin ical feat ures of th e pit uit ar y ch rom oph obe aden o-
4. Lun ardi P, Rizzo A, Missori P, Fraioli B. Pit uit ar y apoplexy in an acrom e- m at a an d of th e Rathké pou ch cyst s. An n R Coll Surg Engl 1957;21:358–
galic w om an operated on du ring pregn an cy by t ran sp h en oidal ap p roach . 381
In t J Gynaecol Obstet 1991;34:71–74 16. Paren t AD, Bebin J, Sm ith RR. In ciden t al pit uit ar y aden om as. J Neurosurg
5. Moh an t y S, Tan don PN, Ban erji AK, Prakash B. Haem orrh age in to pit uit ar y 1981;54:228–231
ad en om as. J Neu rol Neu rosu rg Psych iat r y 1977;40:987–991 17. Russell DS, Rubin stein LJ. Secon dar y t u m ours of th e n er vous system . In :
6. Muller W, Pia HW. [Clin ical aspect s an d et iology of m assive h em orrh age Russell DS, Rubin stein LJ, eds. Path ology of Tum ours of the Ner vous Sys-
in pit uit ar y aden om a] Dt sch Z Ner ven h eilkd 1953;170:326–336 tem . Balt im ore: William s & Wilkin s; 1989:809–817
7. Mü ller-Jensen A, Lü decke D. Clin ical aspect s of spon t an eous n ecrosis of 18. Bailey P. Path ological repor t of a case of akrom egaly, w ith especial refer-
pit uitar y t um ors (pit uitar y apoplexy). J Neurol 1981;224:267–271 en ce to t h e lesion s in t h e hyp op hysis cerebr i an d in t h e t hyroid glan d ;
8. Sym on L, Moh an t y S. Haem orrh age in pit uit ar y t um ou rs. Act a Neuroch ir an d a case of h em orrh age in to th e pit u it ar y. Ph iladelph ia Med J 1898;1:
(Wien ) 1982;65:41–49 789–792
9. Wakai S, Fuku sh im a T, Teram oto A, San o K. Pit uit ar y apoplexy: it s in ci- 19. Bleibt reu VL. Ein fall von akrom egalie (zerstor ung der hypophysis durch
den ce an d clin ical sign ifican ce. J Neu rosu rg 1981;55:187–193 blut ung). Mun ch Med Wochen sch r 1905;52:2079–2081
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1984;14:363–373 teriol 1937;45:189–214
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to pit uitar y apoplexy. Br Med J (Clin Res Ed) 1983;287:1007–1008 t ransph enoidal aspirat ion . Cleve Clin Q 1974;41:163–175

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33 Pituitary Apoplexy 409

22. Ch apm an AJ, William s G, Hockley AD, Lon don DR. Pit uit ar y apoplexy 49. Petersen P, Ch rist ian sen KH, Lin dholm J. Acute m on ocular dist u rban ces
after com bin ed test of an terior p it u it ar y fu n ct ion . Br Med J (Clin Res Ed) m im icking opt ic n eurit is in pit uit ar y apoplexy. Act a Neurol Scan d 1988;
1985;291:26 78:101–103
23. Dr ur y PL, Belch et z PE, McDon ald W I, Th om as DG, Besser GM. Tran sien t 50. Bills DC, Meyer FB, Law s ER Jr, et al. A ret rospect ive an alysis of pit uit ar y
am au rosis an d h eadach e after thyrot ropin releasing h orm on e. Lan cet apoplexy. Neurosurger y 1993;33:602–608, discussion 608–609
1982;1:218–219 51. Woo HJ, Hw ang JH, Hw ang SK, Park YM. Clin ical ou tcom e of cran ial
24. Hu tch in son DO, Aver y SF. Pit uit ar y apoplexy. N Z Med J 1989;102:158– n eu ropathy in pat ien t s w ith pit uit ar y apoplexy. J Korean Neurosurg Soc
160 2010;48:213–218
25. Nou rizad eh AR, Pit t s FW. Hem orrh age in to p it u it ar y ad en om a d u r in g 52. Lubin a A, Olch ovsky D, Berezin M, Ram Z, Hadan i M, Sh im on I. Man age-
an t icoagu lan t th erapy. JAMA 1965;193:623–625 m en t of pit uit ar y apoplexy: clin ical experience w ith 40 pat ien t s. Act a
26. Rau h u t F, Clar HE. [Hem or rh age in hyp op hyseal t u m ors an d in t h e Neuroch ir (Wien ) 2005;147:151–157, discussion 157
ch iasm area—u rgen t su rgical in d icat ion s]. Ner ven arzt 1982;53:584– 53. Ran deva HS, Sch oebel J, Byrn e J, Esiri M, Adam s CB, Wass JA. Classical pi-
588 t uit ar y apoplexy: clin ical feat ures, m anagem en t an d outcom e. Clin En do-
27. Sach dev Y, Gopal K, Garg VK, Mongia SS. Pit u it ar y apoplexy (spon t an eous crin ol (Oxf) 1999;51:181–188
pit uit ar y n ecrosis). Postgrad Med J 1981;57:289–293 54. Ayu k J, McGregor EJ, Mitch ell RD, Git toes NJ. Acute m an agem ent of pit u-
28. Kirsh baum JD, Ch apm an BM. Subarach n oid h em orrh age secon dar y to a it ar y apoplexy—surger y or con ser vat ive m an agem en t? Clin En docrinol
t um or of th e hypophysis w ith acrom egaly. An n In tern Med 1948;29:536– (Oxf) 2004;61:747–752
540 55. Sibal L, Ball SG, Con nolly V, et al. Pit uit ar y apoplexy: a review of clin ical
29. Locke S, Tyler HR. Pit u it ar y apoplexy. Rep or t of t w o cases, w ith path ologi- present at ion , m anagem en t an d outcom e in 45 cases. Pit uit ar y 2004;7:
cal verificat ion . Am J Med 1961;30:643–648 157–163
30. Rigolosi RS, Sch w art z E, Glick SM. Occu rren ce of grow th -h orm on e defi- 56. Sem ple PL, Webb MK, de Villiers JC, Law s ER Jr. Pit uit ar y apoplexy. Neuro-
cien cy in acrom egaly as a resu lt of p it u it ar y ap op lexy. N Engl J Med surger y 2005;56:65–72, discussion 72–73
1968;279:362–364 57. Gruber A, Clayton J, Kum ar S, Robert son I, How let t TA, Man sell P. Pit u it ar y
31. Sach dev Y, Evered DC, Hall R. Spon t an eous pit u it ar y n ecrosis. BMJ 1976; apoplexy: ret rospect ive review of 30 pat ien t s—is surgical in ter ven t ion
1:942 alw ays n ecessar y? Br J Neurosu rg 2006;20:379–385
32. Tsem en t zis SA, Loizou LA. Pit uit ar y apoplexy. Neurochir urgia (St ut tg) 58. Sym on d SC. Ocular palsy as th e presen t ing sym ptom of pit uit ar y ade-
1986;29:90–92 n om a. Bull Joh n s Hopkin s Hosp 1962;111:72–82
33. Veldhu is JD, Ham m ond JM. En docrin e fu n ct ion after spont an eous in farc- 59. Kosar y IZ, Brah am J, Tadm or R, Goldh am m er Y. Tran s-sph en oidal surgical
t ion of th e h um an pit u it ar y: repor t , review, an d reappraisal. En docr Rev approach in pit uit ar y apoplexy. Neuroch irurgia (St u t tg) 1976;19:55–58
1980;1:100–107 60. Majch rzak H, Wen cel T, Dragan T, Bialas J. Acute h em orrh age in to pit u-
34. Cardoso ER, Peterson EW. Pit uit ar y apoplexy an d vasospasm . Surg Neurol it ar y aden om a w ith SAH an d an terior cerebral ar ter y occlusion . Case re-
1983;20:391–395 port . J Neurosurg 1983;58:771–773
35. Wrigh t RL, Ojem an n RG, Drew JH. Hem orrh age in to pit uit ar y aden om at a. 61. David NJ, Gargan o FP, Glaser TS. Pit uit ar y apoplexy in clin ical perspect ive.
repor t of t w o cases w ith spon t an eous recover y. Arch Neurol 1965;12: In : Glaser TS, Sm ith JL, eds. Neurooph th alm ology, VII. St . Louis: Mosby;
326–331 1975:140–165
36. Onest i ST, Wisn iew ski T, Post KD. Clin ical versus subclin ical pit uit ar y apo- 62. Wein berger LM, Adler FH, Gran t FC. Prim ar y pit uit ar y aden om a an d th e
plexy: present at ion , surgical m an agem en t , an d outcom e in 21 pat ient s. syn drom e of th e cavern ous sin us. A clin ical an d an atom ic st udy. Arch
Neurosurger y 1990;26:980–986 Oph th alm ol 1940;24:1197–1236
37. Rovit RL, Fein JM. Pit uit ar y apoplexy: a review an d reappraisal. J Neu ro- 63. Trau t m an n JC, Law s ER Jr. Visu al st at u s after t ran ssp h en oidal su rger y
surg 1972;37:280–288 at t h e Mayo Clin ic, 1971–1982. Am J Op h t h alm ol 1983;96:200–208
38. Lop ez IA. Pit uit ar y apoplexy. J Oslo Cit y Hosp 1970;20:17–27 64. Purnell DC, Randall RV, Rynearson EH. Postpart um pituitar y insufficiency:
39. Kaplan B, Day AL, Quisling R, Ballinger W. Hem orrh age in to pit uit ar y ad- (Sh eeh an’s syn d rom e): review of 18 cases. Mayo Clin Proc 1964;39:321–
en om as. Surg Neurol 1983;20:280–287 331
40. Kovacs K, Hor vath E, Ezrin C. Pit uit ar y aden om as. Path ol An n u 1977;12 65. Tam asaw a N, Ku rah ash i K, Baba T, et al. Spon t an eous rem ission of acro-
(Pt 2):341–382 m egaly after p it u it ar y ap op lexy follow ing h ead t rau m a. J En d ocr in ol
41. Wilson CB. A decade of pit uit ar y m icrosurger y. Th e Herber t Olivecron a Invest 1988;11:429–432
lect ure. J Neurosurg 1984;61:814–833 66. Lyle TK, Clover P. Ocular sym ptom s an d sign s in pit uit ar y t um ours. Proc R
42. Wilson CB, Dem p sey LC. Tran ssph en oidal m icrosurgical rem oval of 250 Soc Med 1961;54:611–619
pit uit ar y aden om as. J Neu rosurg 1978;48:13–22 67. Dan iel PM, Prich ard MM. An terior pit uit ar y necrosis; in farct ion of th e
43. Paw likow ski M, Kun ert-Radek J, Radek M. plurih orm on alit y of pit uit ar y pars dist alis produced experim ent ally in th e rat . Q J Exp Physiol Cogn Med
ad eon om as in ligh t of im m u n oh istoch em ical st u d ies. En d okr yn ol Pol Sci 1956;41:215–229
2010;51(1):63–66 68. Cooperm an D, Malarkey W B. Pit uit ar y apoplexy. Hear t Lung 1978;7:450–
44. Weisberg LA. Pit uit ar y apoplexy. Associat ion of degen erat ive ch ange in 454
pit uit ar y adem on a w ith radioth erapy and detect ion by cerebral com - 69. Fong LP, Fabinyi GC. Oph th alm ic m an ifest at ion s of pit uit ar y apoplexy.
puted tom ography. Am J Med 1977;63:109–115 Med J Au st 1985;142:142–143
45. Law s ER Jr, Ebersold MJ. Pit uit ar y apop lexy—an en docrin e em ergen cy. 70. Goodm an JM, Gilson M, Sh apiro B. Pit uit ar y apoplexy—a cause of su dden
World J Su rg 1982;6:686–688 blin dn ess. J In dian a St ate Med Assoc 1973;66:320–321
46. McFadzean RM, Doyle D, Ram pling R, Teasdale E, Teasdale G. Pituitary apo- 71. Guarn asch elli JJ, Talalla A. Pit uit ar y apoplexy: a case repor t . Bull Los An -
plexy and its effect on vision. Neurosurger y 1991;29:669–675 geles Neu rol Soc 1972;37:12–18
47. Meadow s SP. Un usual clin ical feat u res an d m odes of presen t at ion in pit u- 72. Reuten s DC, Edis RH. Pit uit ar y apoplexy presen t ing as asept ic m en ingit is
it ar y aden om a, in clu ding pit uit ar y apoplexy. In : Sm ith JL, ed. Neurooph - w ith out visual loss or oph th alm oplegia. Aust N Z J Med 1990;20:590–
th alm ology, IV. St . Louis: Mosby; 1968:178–189 591
48. Moh r G, Hardy J, Com tois R, Beauregard H. Surgical m an agem en t of gian t 73. Sussm an EB, Porro RS. Pit u it ar y apoplexy: th e role of ath erom atous em -
pit uit ar y aden om as. Can J Neu rol Sci 1990;17:62–66 boli. St roke 1974;5:318–323

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410 III Ischemic Stroke and Vascular Insufficiency

74. Winer JB, Plan t G. St ut tering pit uit ar y apoplexy resem bling m en ingit is. 91. Mu th u ku m ar N, Rosset te D, Sou n daram M, Sen th ilbabu S, Bad rin aray-
J Neu rol Neu rosu rg Psych iat r y 1990;53:440 an an T. Blin dn ess follow ing pit u it ar y ap oplexy: t im ing of su rger y an d
75. Law ren ce AM, Gordon DL, Hagen TC, Sch w ar t z MA. Hypoth alam ic hypo- n eu ro-oph thalm ic ou tcom e. J Clin Neu rosci 2008;15:873–879
pit uitarism after pituitar y apoplexy in acrom egaly. Arch Intern Med 1977; 92. Baker HL Jr. Th e angiograph ic delin eat ion of sellar an d p arasellar m asses.
137:1134–1137 Radiology 1972;104:67–78
76. Maitlan d CG, Abiko S, Hoyt W F, Wilson CB, Okam ura T. Ch iasm al apo- 93. Arafah BM, Har r in gton JF, Mad h ou n ZT, Selm an W R. Im p rovem en t of
plexy: rep or t of fou r cases. J Neu rosug 1982;56(1):118–122 p it uit ar y fu nct ion after surgical decom pression for pit uit ar y t um or apo-
77. Tom iyasu U, Hiran o A, Zim m erm an HM. Fin e st ruct ure of h um an pit u - plexy. J Clin En docrin ol Met ab 1990;71:323–328
it ar y aden om a. Arch Path ol 1973;95:287–292 94. Bjerre P, Lin dh olm J, Vid ebaek H. Th e sp on t an eou s cou rse of p it u it ar y
78. Gorczyca W, Hardy J. Microaden om as of th e h um an pit uit ar y an d th eir adenom as an d occurren ce of an em pt y sella in un t reated acrom egaly.
vascularizat ion . Neurosurger y 1988;22(1 Pt 1):1–6 J Clin En docrin ol Met ab 1986;63:287–291
79. Ku rn ick JE, Har t m an CR, Lu fkin EG, Hofeldt FD. Abn orm al sella t urcica. 95. Maccagn an P, Maced o CL, Kayath MJ, Nogu eira RG, Abu ch am J. Con ser va-
A t um or board review of th e clin ical sign ifican ce. Arch Intern Med t ive m an agem en t of pit uit ar y apoplexy: a prospect ive st udy. J Clin En do-
1977;137:111–117 crin ol Met ab 1995;80:2190–2197
80. Ch alla VR, Richards F II, Davis CH Jr. Int raven t ricu lar hem orrh age from 96. Seu k JW, Kim CH, Yang MS, Ch eong JH, Kim JM. Visu al ou tcom e after
pit uit ar y apoplexy. Surg Neu rol 1981;16:360–361 t ranssph en oidal surger y in pat ien t s w ith pit uit ar y apoplexy. J Korean
81. Kalyan aram an UP. Clinically asym ptom at ic pit uit ar y aden om a m an ifest- Neurosu rg Soc 2011;49:339–344
ing as pit u it ar y apoplexy an d fat al th ird-ven t ricu lar h em orrh age. Hu m 97. Itoyam a Y, Goto S, Miu ra M, Ku rat su J, Ush io Y, Mat su m oto T. In t racra-
Path ol 1982;13:1141–1143 n ial ar terial vasospasm associated w ith p it u it ar y ap op lexy after h ead
82. Patel DV, Sh ields MC. In t raven t ricular h em orrh age in pit uit ar y apoplexy. traum a—case report. Neurol Med Ch ir (Tokyo) 1990;30:350–353
J Com p u t Assist Tom ogr 1979;3:829–831 98. Min er ME, Fields WS, Walker J. Pit u it ar y apop lexy com p licat ing ch ron ic
83. Ch en ST, Ch en SD, Ryu SJ, Hsu TF, Heim burger RF. Pit u it ar y apoplexy w ith secon dar y am en orrh ea. J Fam Pract 1982;14:873–877
in t racerebral h em orrh age sim ulat ing ru pt u re of an an terior cerebral ar- 99. Pozzat i E, Frank G, Nasi MT, Giuliani G. Pit uit ar y apoplexy, bilateral ca-
ter y an eur ysm . Surg Neurol 1988;29:322–325 rot id vasospasm , an d cerebral infarct ion in a 15-year-old boy. Neurosur-
84. Sakoda K, Mukada K, Yon ezaw a M, et al. CT scan of pit u it ar y aden om as. ger y 1987;20:56–59
Neuroradiology 1981;20:249–253 100. Zer vas NT, Men delson G. Treat m en t of acute h aem orrh age of pit uit ar y
85. Scot t i G, Triulzi F, Ch ium ello G, Din at ale B. New im aging tech n iques in t um ours. Lan cet 1975;1(7907):604–605
en docrinology: m agn et ic reson an ce of th e pit u it ar y glan d an d sella t ur- 101. Tsit sopoulos P, An drew J, Harrison MJ. Pit uit ar y apoplexy an d h aem or-
cica. Act a Paediat r Scan d Suppl 1989;356:5–14 rh age in to ad en om as. Postgrad Med J 1986;62:623–626
86. Wilkin s RH. Hypoth alam ic dysfun ct ion an d in t racran ial ar terial spasm s. 102. Takeda N, Fujit a K, Kat ayam a S, Akut u N, Hayash i S, Koh m ura E. Effect of
Surg Neu rol 1975;4:472–480 t ran ssph en oidal surger y on decreased visual acuit y caused by pit uit ar y
87. Nelson PB, Haverkos H, Mar t inez AJ, Robin son AG. Abscess form at ion apoplexy. Pit uit ar y 2010;13:154–159
w ithin pit uit ar y t um ors. Neurosurger y 1983;12:331–333 103. Arafah BM, Taylor HC, Salazar R, Saadi H, Selm an W R. Apoplexy of a pi-
88. W h alley N. Abscess form at ion in a pit uit ar y aden om a. J Neurol Neurosurg t uit ar y aden om a after dyn am ic test ing w ith gon adot ropin -releasing
Psych iat r y 1952;15:66–67 h orm on e. Am J Med 1989;87:103–105
89. Slee PH, Ren sm a PL. Hypopit uit arism follow ing com plicated ch ild bir th
(Sh eeh an’s syn drom e). Neth J Med 1990;37:120–123
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2005;63:42–46, discussion 46

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IV Cerebral and Spinal
Cavernous Malformations

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Neurosurgery Books Full
34 Cavernous Malformations: Natural
History, Epidemiology, Presentation,
and Treatment Options
Hasan A. Zaidi and Joseph M. Zabram sk i

Cerebral cavern ou s m alform at ion s, also kn ow n as cavern om as, an ce as a resu lt of un dulat ing episodes of th rom bosis an d recan -
cavern ou s h em angiom as, an d cavern ou s angiom as, are low -flow alization. They are distinguish ed from capillar y telangiectasias by
vascular lesion s com posed of th in , dilated vascular ch an n els w ith th e absen ce of brain t issu e bet w een in ter ven ing vascu lar ch an -
a variable propen sit y for h em orrh age. Th ese lesion s can becom e n els. Alth ough th ey are n ot en capsu lated, th ey are surroun ded
sym ptom at ic at n early any age; h ow ever, an in creasing n u m ber by a t h in gliot ic bord er. Classically, t h e lesion s are associated
of pat ien t s presen t w ith in ciden tal, asym ptom at ic lesion s th at w it h lit t le or n o m ass effect , an d ten d to d isp lace su r rou n d ing
are iden t ified w h en m agn et ic reson an ce im aging (MRI) is per- n or m al brain t issu e rat h er t h an d est roy it . Su r rou n d ing ed em a
form ed for workup of unrelated com plaints. This chapter discusses is rare except in cases w ere h em orrh age h as exten ded outside
th e n at ural h istor y, epidem iology, presen tat ion , an d t reat m en t th e lesion . Recu rren t ep isodes of th rom bosis w ith in th e d ilated
of th ese com plex lesion s. ch an n els an d su bclin ical episodes of m icroh em orrh age resu lt in
th e dep osit ion of h em osiderin an d in th e adjacen t gliot ic brain .
Long th ough t to be stat ic, m ore recen t im aging st udies h ave
con firm ed th at cavern ou s m alform at ion s exh ibit a range of dy-
■ Epidemiology n am ic pat tern s in cluding grow th , regression , an d even de n ovo
form at ion in both th e fam ilial an d sporadic cases.6–8 As a resu lt ,
Cavern ou s m alform at ion s are m u ch m ore com m on th an gen er-
pat ien ts w ith th ese lesion s requ ire ongoing obser vat ion an d a
ally realized. Th eir repor ted prevalen ce based on t w o large post-
th orough evalu at ion of any ch ange in n eu rologic sym ptom s.
m ortem n europath ology st u dies (n = 30,269),1,2 an d t w o large
in st it ut ion al MRI scan review s (n = 22,166) 3,4 is 0.34 to 0.53%
(m ean 0.49%). Taken togeth er, th ese st udies suggest th at n early 1
in 200 in dividu als is affected by cavern ou s m alform at ion s.
Cavern ou s m alform at ion s occu r in t w o form s, sp oradic an d
■ Natural History
fam ilial, w ith th e fam ilial form represen t ing n early 6% of all Th e n at u ral h istor y of cavern ou s m alform at ion s varies con sider-
cases.5 In th e sp oradic form , p at ien ts u sually h ave on e or t w o le- ably am ong th e lit any of pu blish ed repor t s, depen ding largely on
sion s an d n o fam ily h istor y of n eu rologic disease. In con t rast , th e the m ethodology utilized by the authors and w h ether the lesions
fam ilial form is ch aracterized by m u lt iple lesion s an d a st rong are incidental or sym ptom atic. Retrospective studies report hem -
fam ily histor y of seizures. Given th at m ore th an 40% of pat ien ts orrh age rates of 0.25 to 2.3%per pat ien t per year; h ow ever, th ese
w ith the fam ilial form of cavern ous m alform at ion s are asym p - st u dies likely u n d erest im ate th e risk of bleeding as th eir au th ors
tom at ic, sporadic cases h aving th ree or m ore lesion s sh ou ld be assu m ed th at all lesion s are presen t from bir th .3,9,10 Prospect ive
viewed w ith suspicion; w ith careful history and MRI screening, as st u dies n ote th at sym ptom at ic lesion s in pat ien t s w ith a h istor y
m any as 50% of th ese cases are foun d to be fam ilial, w h ereas th e of prior h em orrh age h ave a h igh er rebleeding rate (4.5%per year)
rem ain ing cases likely rep resen t n ew sp on t an eous m u tat ion s. th an in ciden t al lesion s (0.6% per year) or lesion s in pat ien t s pre-
Cavern ou s m alform at ion s occu r th rough ou t th e cen t ral n er- sen t ing w ith seizu res (0.4%).9,11 Por ter et al12 repor ted th at th e
vous system in rough propor t ion to th e volum e of n eural t issue: location of the lesion w as the m ost im portant factor in predicting
80% supraten torial, 15% in th e brain stem an d basal ganglia, an d fut ure bleeding even ts, w ith deep -seated lesions in the brainstem
5% in the spin al cord. Alth ough th e prevalen ce of th ese lesion s is or basal ganglia h aving a n otably h igh er rate (10.6% per pat ien t
approxim ately equivalen t in th e pediat ric an d adult populat ion s, per year) th an m ore su p erficial lesion s (0% p er p at ien t p er year).
m ost pat ien t s presen t clin ically in th e th ird to fou r th decade of Mult iple auth ors have published st udies noting that those lesions
life.5 Wom en an d m en ap p ear to be affected equ ally, alth ough th at ru pt u re ou t side of th e lesion capsu le, th e so-called over t or
th ere is som e debate as to w h eth er w om en h ave a h igh er in ci- extralesional hem orrhage effect described by Zabram ski et al,6 can
den ce of sym ptom at ic h em orrh age. h ave reh em orrh age rates as h igh as 25.2% p er pat ien t p er year.13

■ Pathophysiology ■ Diagnostic Imaging Studies


Cavern ou s m alform at ion s are t yp ified by en doth eliu m -lin ed, si- In gen eral, caver n ou s m alform at ion s are low -flow lesion s t h at
n usoidal blood cavit ies w ith out eviden ce of n orm ally developed are poorly visu alized by angiography. On occasion , angiography
vessel layers such as tight junctions, sm ooth m uscle, or adventitia. exh ibit s d elayed ven ou s pooling w ith in th e lesion or, m ore fre-
On gross exam in at ion , th ey appear to be “m ulberr y” in appear- qu en tly, an adjacen t developm en tal ven ous an om aly. Com puted

413

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414 IV Cerebral and Spinal Cavernous Malformations

tom ography (CT) im aging is h elpful in dem onstrating evidence of be associated in n early on e-t h ird of all caver n ou s m alfor m a-
acute h em orrh age in pat ien ts presen t ing w ith th e sudden on set t ion s.16 Id en t ificat ion of t h is associated lesion is an im p or t an t
of focal neurologic deficit s. Oth er fin dings in clu de focal areas of con siderat ion in su rgical plan n ing.17
calcificat ion ; h ow ever, th e overall sen sit ivit y is n o m ore th an Caver n ou s m alfor m at ion s w ere or igin ally classified by Za-
50%, an d th e fin dings, w h en presen t , are n on sp ecific. bram ski et al6 in to fou r t yp es (Table 34.1). Alt h ough in it ially
Magn et ic reson an ce im aging is t h e gold st an dard for th e eval- d escribed in a coh or t of fam ilial cavern ous m alform at ion s, th is
uat ion of pat ien t s w ith su sp ected cavern ou s m alform at ion s. Th e categorizat ion h as been gen eralizable to n on fam ilial lesion s as
MRI ch aracter ist ics of t h is lesion are h igh ly sp ecific an d w ell w ell. Hem orrh age risks h ave been n oted to be sign ifican tly ele-
d escribed in th e literat u re. Classically, th e lesion s h ave a focal, vated in t ype I an d t ype II lesion s, an d sh ou ld prom pt th e su r-
reticulated “salt-and-pepper” pat tern on T2-weighted sequences, geon to in ter ven e w h en clin ically w arran ted.18,19 Type I lesion s
an d are surroun ded by a ring of hypoin ten sit y con sisten t w ith con t ain focal areas of acu te/su bacu te h em orrh age, an d are su b -
h em osiderin deposit ion . Surroun ding edem a an d m ass effect are divided in to t w o grou p s: t ype IA, in w h ich th ere is ext ralesion al
rare except in th e presen ce of ext ralesion al h em orrh age. Dedi- hem orrhage, frequently associated w ith surroun ding edem a; and
cated im aging w ith gradien t-ech o sequ en ces is valu able w h en t ype IB, in w h ich th e h em orrh age is in t ralesion al. Type IA lesion s
evaluating patients w ith suspected fam ilial disease. Gradient-echo are n early alw ays sym ptom at ic an d are associated w ith a h igh
im ages exh ibit m arked sen sit ivit y to h em osiderin deposit ion , risk of recu rren t sym ptom at ic h em orrh age (u p to 25% p er year).
an d w ill frequen tly dem on st rate m ult iple, sm all, in ciden tal cav- Th e risk of sym ptom at ic h em orrh age in t yp e IB lesion s is related
ern ou s m alform at ion s th at are n ot visible on oth er sequ en ces. In to th e clin ical h istor y an d locat ion , being as h igh as 5 to 10% per
a series of 132 pat ien ts w ith fam ilial cavern ous m alform at ion s, year for brain stem lesion s, an d 0.5 to 1% for asym ptom at ic su -
Den ier an d cow orkers 14 rep or ted an average of five lesion s per p raten torial lesion s. Type II lesion s h ave th e classic “popcorn ” or
pat ien t on T2-w eigh ted im ages an d 20 per p at ien t on gradien t- “salt -an d -p ep p er” ap p earan ce p rod u ced by locu lated areas of
ech o sequ en ces. Alth ough T2-w eigh ted an d gradien t -ech o im - h em orrh age an d th rom bosis of var ying age, an d m ay be associ-
ages are u sefu l for diagn osis, th ey ten d to overest im ate th e size ated w ith focal calcificat ion s. As w ith t ype I lesion s, th e risk of
of th e lesion an d sh ould n ot be u sed for surgical plan n ing. Vari- sym ptom at ic h em orrh age in t ype II lesion s is related to th e clin i-
ous T1-w eigh ted sequences provide th e m ost accu rate an atom ic cal h istor y an d locat ion of th e lesion , w ith sym ptom at ic lesion s
detail, and are th e best choice w hen considering surgical inter ven- h aving a r isk of 4 to 5% p er year, an d asym ptom at ic lesion s 0.5
t ion . Gadolin iu m -en h an ced T1-w eigh ted sequ en ces are u sefu l in to 1% per year. Type III lesion s are com posed of sm all foci of re-
iden t ifying associated developm en tal ven ou s an om alies (DVAs), solved h em orrh age associated w ith h em osiderin st ain ing of th e
w ell described by Rigam on t i an d Spet zler 15 an d n ow th ough t to su rrou n ding brain . Th ey are rarely sym ptom at ic an d h ave a risk

Table 34.1 Zabramski Classification for Cavernous Malformations

Magnetic Resonance Natural History and Risk


Lesion Type Signal Characteristic Pathological Characteristics of Hemorrhage

Type IA T1: hyperintense focus of hemorrhage “Overt” extralesional focus of Almost all lesions are symptomatic; high
T2: hyper- or hypointense focus of hem orrhage extending outside the risk of recurrent symptomatic
hem orrhage extending through at lesion capsule hem orrhage of up to 60%/year for
least one wall of the hypointense rim brainstem lesions (mean, 25 to 30% per
that surrounds the lesion; focal edem a year)
may be present
Type IB T1: hyperintense focus of hemorrhage Subacute focus of intralesional Risk of symptomatic hemorrhage related
T2: hyper- or hypointense focus of hem orrhage to presentation and location; higher for
hem orrhage surrounded by a symptomatic lesions in the brainstem
hypointense rim and basal ganglia (5–10% per year);
lower in asymptom atic lesions (0.5–1%
per year)
Type II T1: reticulated mixed signal core Loculated areas of hemorrhage and Risk of symptomatic hemorrhage related
T2: reticulated mixed signal core thrombosis of varying age surrounded to presentation; in symptomatic
surrounded by a hypointense rim by gliotic, hemosiderin-stained brain; patients risk of recurrent hemorrhage
in large lesions, areas of calcification 4–5% per year; low risk for
may be seen asymptomatic lesions (0.5–1% per year)
Type III T1: iso- or hypointense Chronic resolved hemorrhage with Rarely symptom atic; lesions have a low
T2: hypointense, with hypointense rim hem osiderin staining within and risk of hem orrhage (< 0.5% per year)
that m agnifies the size of lesion around the lesion
GRE: hypointense with greater
magnification than T2
Type IV T1: poorly seen or not visualized at all Two lesions in the category have been Never symptomatic; very low risk of
T2: poorly seen or not visualized at all pathologically documented to be hem orrhage
GRE: punctate hypointense lesions telangiectasias
Abbreviations: GRE; gradient echo.

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34 Cavernous Malformations 415

of sym ptom at ic h em orrh age of less th an 0.5% per year. Type IV


lesion s are m in u te foci of h em osiderin stain ing iden t ified p ri-
m arily in pat ien ts w ith th e fam ilial form s of cavern ous m alfor-
m at ion , an d are visible on ly on gradien t-ech o im aging.

■ Clinical Presentation
Recu rren t ep isodes of h em orrh age are a clin ical feat u re of cav-
ern ou s m alform at ion s. Hem orrh ages can eith er be asym ptom -
at ic or m an ifest w ith a w ell-defin ed set of n eu rologic sym ptom s,
dep en ding on both th e size an d locat ion of th e lesion . Pat ien ts
w ith su praten torial lesion s m ost com m on ly presen t w ith sei-
zures, accoun t ing for 40 to 80% of n ew ly sym ptom at ic pat ien ts
(Fig. 34.1).3,4,6 Th e on set or exacerbat ion of seizu re act ivit y is
often correlated w ith n ew h em orrh age on im aging st u dies, an d
is th ough t to be a d irect resu lt of h em osiderin d eposit ion in to
surroun ding brain tissue. The breakdow n of h em osiderin releases
elem en t al iron , w h ich h as been sh ow n to be ep ileptogen ic in
variou s an im al m od els.20
Pat ien t s w ith brain stem lesion s t ypically presen t w ith t h e
su dden on set of focal n eu rologic deficits secon dar y to h em or-
rh age (Fig. 34.2). Th e sym ptom s are t ypically m axim al at on set ,
an d ten d to gradually resolve as blood is resorbed. Sym ptom s
m ay resolve com pletely after an in it ial h em orrh age; h ow ever, re-
curren t episodes are likely to result in progressively m ore severe Fig. 34.1 A 3-year-old girl presenting with new-onset seizures. Axial T2-
deficits an d to perm anent im pairm en t and death if left unt reated. weighted m agnetic resonance im aging (MRI) revealed the presence of t wo
Death is rare in th ese pat ien t s w ith ou t a h istor y of recu rren t ep i- frontal, deep white m at ter cavernous m alformations with classic m ulberry
appearance and surrounding hem osiderin deposition. (Courtesy of Bar-
sodes of sym ptom at ic h em orrh age.
row Neurological Institute.)
Pat ien ts w ith sp in al cord lesion s com m on ly presen t w ith on e
of t w o dist in ct clin ical h istories: (1) th e sudden on set of m otor/
sen sor y deficits, or even com p lete loss of spin al cord fu n ct ion , as an d h em orrh age risk of cavern ous m alform at ion s.22–24 Th is n o-
a result of a m ajor h em orrh age; or (2) slow ly progressive m y- t ion h as persu ad ed m any obstet rician s to offer early cesarean
elop athy, or radicu lop athy, secon dar y to rep eated m in or bleed- bir t h s to red u ce th e p oten t ial risk to exp ect an t m ot h ers w it h
ing ep isodes (Fig. 34.3). Pain is a dom in an t sym ptom in m any cerebral cavern ous m alform at ion s; som et im es th e cesarean is
patients w ith spinal cord cavernous m alform ations, and although perform ed w eeks before fu ll gestat ion . Recen t rep or ts, h ow ever,
a m alform at ion t ypically respon ds w ell to surgical in ter ven t ion ,
it carries a h igh risk of recu rren ce (u p to 48% in som e series).10

Incidental Cavernous Malformations


An in creasing n um ber of pat ien ts presen t to th e n eurosurgeon
w it h in cid en t al caver n ou s m alfor m at ion s, d iscovered d u r ing
w orku p for un related com plain ts. Th e m ost com m on com plain ts
for w h ich MRI is perform ed in th is popu lat ion are h eadach es an d
dizzin ess. Closed h ead inju ries are also com m on , w ith abn orm al
fin dings on CT leading to fur th er w orkup w ith MRI an d su bse-
qu en t diagn osis. Th e qu est ion of h ow frequ en tly in ciden t al cav-
ern ou s m alform at ion s can be exp ected in th e gen eral p op u lat ion
w as addressed by Vern ooij et al21 in 2007. Th ey repor ted th e re-
su lts of a screen ing MRI st u dy perform ed on a grou p of 2,000
asym ptom at ic adult s: 0.4%of th is popu lat ion (1 in ever y 250 pa-
t ien ts) h ad in ciden tal cavern ou s m alform at ion s, am ong a variet y
of oth er lesion s.

Cavernous Malformations and Pregnancy


Fig. 34.2 A 21-year-old m an with m ultiple brainstem cavernous m alfor-
In terspersed case repor t s h ave fueled th e n ot ion th at h orm on al m ations present s with acute neurologic deterioration after evidence of
changes during pregn ancy m ay potentially exacerbate the grow th rebleeding on MRI. (Courtesy of Barrow Neurological Institute.)

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416 IV Cerebral and Spinal Cavernous Malformations

Fig. 34.3a,b Sagit tal T2-weighted (a) and axial T1-weighted (b) images demonstrat-
ing a thoracic cavernous m alform ation with evidence of subacute hem orrhage (bright
a on T1/T2). (Courtesy of Barrow Neurological Institute.)

in dicate th at sym ptom at ic rates of h em orrh age du ring th e preg- sulting in the form at ion of cavern ous m alform ations is still poorly
nan cy and subsequen t puerperium are not differen t from reported u n derstood.
rates of h em orrh age in epidem iological st u dies.25,26 Kalan i et al25 Prosp ect ive st u dies h ave n oted th at silen t h em orrh ages are
recen tly rep or ted th at of 168 p regn an cies, on ly five h ad sym p - com m on in fam ilial cases, w ith Zabram ski et al6 repor t ing an
tom at ic h em orrh age w ith an overall sym ptom at ic h em orrh age overall h em orrh age rate of 2%per year, bu t on ly 1.1%per year for
rate of 3%, w ell w it h in t h e ran ge rep or ted for t h e n at u ral h is- sym ptom at ic h em orrh age am ong 59 m em bers of six fam ilies.
tor y of th e disease.27 Taken togeth er, th ese repor t s suggest th at Nearly 29%of p at ien t s develop ed n ew lesion s w ith in th is coh or t .
pregn an cy sh ou ld n ot in flu en ce th e gen eral n eu rosu rgical m an - Bru n ereau et al34 repor ted a sim ilar rate of d e n ovo form at ion
agem en t of cerebral cavern ou s m alform at ion s as p reviou sly dis- (27.5%) w ith an overall rate of 0.2 new lesions/patient-year. As pre-
cussed, an d th e m ethod of deliver y in expectan t m oth ers sh ould viously em ph asized, fam ilial form s of th e disease are especially
be based pu rely on obstet rical con siderat ion s. in flu x, an d requ ire close clin ical an d radiological follow -u p.

Familial Cavernous Malformations


Fam ilial form s of cavern ou s m alform at ion s are in h erited in an ■ Treatment
autosom al dom in an t fash ion w ith in com plete clin ical an d radio-
In 1928, Walter Dan dy 35 n oted th at th ere w ere on ly 44 kn ow n
logical p en et ran ce. Th ree sep arate gen es h ave been id en t ified :
rep orts of cavern ou s angiom as in th e literat ure at th e t im e, an d
KRIT1 (CCM1), MGC4607 (CCM2), an d PDCD10 (CCM3). At least
recom m en ded th at “th e on ly sat isfactor y t reat m en t w as ext irp a-
on e gen e is m ut ated in pat ien t s w ith m ost fam ilial cavern ou s
tion” for th ese extrem ely rare lesions. Although surgical resection
m alform at ion s.16,28 KRIT1 (CCM1) is th e m ost com m on gen e to
is cu rat ive for t h ese lesion s, t h e n eu rosu rgeon m u st carefu lly
be m ut ated in fam ilial form s (56%), an d is th ough t to be a scaf-
w eigh t h e r isks of any su rgical p roced u re again st t h e n at u ral
fold an d effector protein .29 MGC4607 (CCM2) is involved in 33%of
h istor y of th e lesion .
fam ilial form s, an d m ay ser ve to sequester KRIT1 in th e n ucleus
to m ediate sign aling path w ays. PDCD10 (CCM3) is iden t ified in
on ly 6% of fam ilial cases, an d h as been sh ow n to be involved Asymptomatic Incidental
in ap optosis du ring ar terial m orp h ogen esis. All th ree of th ese
gen es are n ow kn ow n to interact to form a single com plex, w h ich
Cavernous Malformations
su bsequ en t ly affect s d ow n st ream p rotein s.30–33 Alt h ough m u ch Eviden ce-based guidelin es for th e m an agem en t of in ciden t al
is kn ow n abou t th ese gen es, th e u n derlying path ophysiology re- cavern ou s m alform at ion s h ave n ot been est ablish ed. Th e deci-

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34 Cavernous Malformations 417

sion of w h eth er to recom m en d su rger y dep en ds on a m u lt it u de assu m ing con fir m at ion of t h e cavern ou s m alfor m at ion as t h e
of factors, in clu ding th e size an d locat ion of th e lesion , w h eth er seizu re focu s.
the disease is fam ilial or sporadic, patien t lifest yle an d preference, Patients w ith cavernous m alform ations w ho present w ith focal
an d su rgeon exp er ien ce; h ow ever, on e of t h e m ost im p or t an t n eu rologic deficits as a result of h em orrh age adjacen t to elo-
factors th e surgeon m u st con sider is th e n at ural h istor y of th e qu en t territor y can be poten t ially difficu lt to t reat surgically, an d
lesion . Mu lt ip le au th ors h ave n oted th at th e risk of h em orrh age carr y a h igh er risk of su rgical com p licat ion s if located in deep
is h eavily in flu en ced by MRI ch aracter ist ics of t h e lesion an d locat ion s.36 Som e au th ors advocate obser vat ion for all lesion s
w h eth er th ere is a h istor y of p reviou s sym ptom at ic h em or- w ith over t h em orrh age an d focal n eu rologic sym ptom s un less
rh age.6 At ou r in st it u t ion , in cid en t ally d iscovered asym ptom - th e h em orrh age is su bst an t ial.16 At our in st it ut ion , our ph iloso-
at ic in tracran ial cavern ous m alform at ion s of t ypes IB, II, an d III phy is to balan ce th e risk of su rger y again st th e n at u ral h istor y of
(Table 34.1) are gen erally m an aged con ser vat ively. Th e risk of th e disease. For pat ien t s w ith sym ptom at ic ext ralesion al h em or-
sym ptom at ic h em orrh age in th ese pat ien ts ap pears n o h igh er rh ages (t yp e IA, Table 34.1) t h e r isk of recu r ren t h em or rh age
th an 0.5 to 1%per year. Th ese risks an d th e n eed of follow -u p are is as h igh as 25% p er year, an d surgical resect ion sh ou ld be con -
discu ssed w ith th e p at ien t .18 Pat ien t s w ith lesion s of t yp es IB sidered for all su rgically accessible lesion s. On ly in cases w h ere
an d II are follow ed w it h ser ial MRI st u d ies, in it ially at yearly sym ptom s are m ild an d th e lesion is deep do w e con sider obser-
in ter vals to assess lesion grow th ; recurren t h em orrh age w ould vat ion , an d recon sider surger y on ce fut ure h em orrh age results
argue for surgical in ter ven t ion . For t ypes IB an d II lesions that in th e lesion reach ing a pial surface. As ou r skill h as im proved
rem ain stable and for t ype III lesions, clinical follow -up an d repeat w ith experien ce, w e h ave begu n to con sider offering surger y for
im aging st u dies are p erform ed at 3- to 5-year in ter vals, u n less lesion s p reviously con sidered for con ser vat ive m an agem en t . In a
w arran ted by n ew on set of sym ptom s. recen t review of 300 brain stem cavern ous m alform at ion s at our
Su rgical m an agem en t in th is grou p of asym ptom at ic pat ien t s in st it u t ion , Abla et al40 repor ted th at even in t rin sic lesion s of th e
is ver y con t roversial, an d on ly un der rare circu m stan ces is resec- brain stem th at h ave n ot yet reach ed th e pial surface (par t icularly
t ion con sidered at ou r in st it ut ion . For exam ple, asym ptom at ic t h ose in t h e p on s) can be safely ap p roach ed . We recom m en d
brain stem lesion s th at dem on st rate evid en ce of exp an sion or th at each sym ptom at ic lesion be evalu ated for su rgical in ter ven -
m or p h ological ch an ge (conversion from t yp e II to t yp e I) on t ion dep en ding on th e locat ion of th e lesion an d th e skill an d
follow -u p im aging car r y a low er t h resh old for su rgical in ter- com for t of th e su rgeon.
ven t ion . Sim ilarly, becau se spin al cord lesion s ap pear to carr y a
h igh er risk of sym ptom at ic h em orrh age an d n eurologic deterio-
rat ion ,36 su rgical in ter ven t ion is con sidered for asym ptom at ic Treatment of Multiple Familial
lesion s of t yp es IB an d II th at reach th e pial su rface an d are lo- Cavernous Malformations
cated in th e d orsal spin al t racts. Ven t rally located lesion s, w h ich
Pat ien ts w ith sym ptom at ic fam ilial cavern om as can presen t a
carr y a m u ch h igh er risk of n eu rologic deteriorat ion w ith su rgi-
p oten t ial d ilem m a to t h e su rgeon . Th e goal rem ain s t h e sam e
cal in ter ven t ion , m ay be bet ter ser ved by con ser vat ive m an age-
as in pat ien ts w ith sporadic cavern om as: reduce th e in ciden ce
m en t in th e asym ptom at ic pat ien t .37
of seizu res an d reduce th e risk of sym ptom s from over t h em or-
rh age. Pat ien t s w ith sym ptom at ic h em orrh ages an d m edically
Symptomatic Patients refractory seizures are candidates for surgical resection. The pres-
en ce of m u lt iple lesion s in th is pop u lat ion m akes accu rate local-
Pat ien t s w ith caver n ou s m alfor m at ion s w h o presen t in it ially
izat ion of th e sym ptom at ic lesion crit ical. Alth ough acu te focal
w ith seizu res are t yp ically m an aged w ith an t iep ilept ic d r ugs,
n eu rologic deficit s are readily localized, for pat ien ts w ith poorly
w ith som e sm all case series rep or t ing u p to 60% seizu re con t rol
con t rolled seizu res inp at ien t m on itoring w ith video elect roen -
u sing th is m eth od alon e.38 How ever, prospect ive rep ort s in di-
cep h alograp hy m ay be n ecessar y for id en t ifying t h e sym ptom -
cate th at recu rren ce is com m on (5.5% p er p at ien t p er year),27
at ic respon sible lesion . W it h carefu l p reop erat ive w orku p an d
w ith Kon d ziolka et al9 rep or t ing as m any as 20% of p at ien t s
seizu re focu s localizat ion , Rocam ora et al41 repor ted seizure con -
even t u ally d evelop in g dr ug-resist an t ep ilep sy. On ce d r ug resis-
t rol in m ore th an 80% of p at ien ts w ith on ly on e epileptogen ic
t an ce d evelop s, th e p oten t ial for a seizu re-free ou tcom e after
focu s am ong m u lt iple lesion s. Surgical resect ion of asym ptom -
su rgical in ter ven t ion is d ram at ically red u ced . Am ong pat ien t s
at ic lesion s in th is p opu lat ion is gen erally con t rain dicated, as th e
w it h a cavern ou s m alform at ion an d a h istor y of a single seizu re,
de n ovo form at ion of n ew lesion s con t in u es at a rate of 0.2 to 0.4
or sp orad ic seizu res, Ferroli et al39 rep or ted n early 98%w ere sei-
n ew lesion s p er pat ien t per year.6,19
zu re free after su rgical resect ion ; th is w as in st ark con t rast to
pat ien t s w it h a long h istor y of seizu res, w h ere less th an 69%h ad
seizu re-free ou tcom es. Ch ron ic h em osid er in d ep osit ion in t h e
brain t issu e su r rou n d ing t h e lesion can be a sou rce of con t in -
u ed seizu res, desp ite com p lete resect ion of th e caver n ou s m al-
■ Conclusion
for m at ion . Alter n at ively, su bopt im al seizu re con t rol can resu lt Cerebral cavern ous m alform at ion s represen t a p oten t ially su rgi-
from a secon dar y ep ileptogen ic focu s, w h ich can arise far from cally cu rable disease p rocess. To m ake a w ell-in form ed decision
th e caver n ou s m alfor m at ion it self, w h ich m ay requ ire a secon d on th e m an agem en t of th ese lesion s, it is im perat ive th at th e
op erat ion for resect ion of t h e secon dar y seizu re focu s.36 As a re- n eu rosurgeon h ave a com preh en sive un derstan ding of th eir epi-
su lt , w e h ave becom e m ore aggressive at offer ing su rgical resec- d em iology an d n at u ral h istor y, an d be aw are of t h e m orbid it y
t ion to pat ien t s w ith ep ilepsy refractor y to single drug th erapy, an d m or talit y of any plan n ed surgical in ter ven t ion .

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48:610–614 29. Bacigaluppi S, Ret t a SF, Pileggi S, et al. Gen et ic an d cellular basis of cere-
8. Leh n h ardt FG, von Sm ekal U, Rü ckriem B, et al. Value of gradient-ech o bral cavern ou s m alform at ion s: im p licat ion s for clin ical m an agem en t . Clin
m agn et ic resonan ce im aging in th e diagn osis of fam ilial cerebral cavern - Gen et 2013;83:7–14
ous m alform at ion . Arch Neurol 2005;62:653–658 30. Hild er TL, Malon e MH, Ben ch arit S, et al. Proteom ic iden t ificat ion of th e
9. Kon dziolka D, Lun sford LD, Kestle JR. Th e n at u ral h istor y of cerebral cav- cerebral cavernous m alform at ion signaling com plex. J Proteom e Res 2007;
ern ous m alform at ion s. J Neurosurg 1995;83:820–824 6:4343–4355
10. Kim LJ, Klopfen stein JD, Zabram ski JM, Son n t ag VK, Spet zler RF. An alysis 31. Ma X, Zh ao H, Sh an J, et al. PDCD10 in teract s w ith Ste20-related kin ase
of pain resolut ion after su rgical resect ion of in t ram edullar y spinal cord MST4 to p rom ote cell grow th an d t ran sform at ion via m odu lat ion of th e
caver n ou s m alfor m at ion s. Neu rosu rger y 2006;58:106–111, d iscu ssion ERK path w ay. Mol Biol Cell 2007;18:1965–1978
106–111 32. Voss K, St ah l S, Sch leider E, et al. CCM3 in teract s w ith CCM2 in dicat ing
11. Aiba T, Tan aka R, Koike T, Kam eyam a S, Takeda N, Kom at a T. Nat ural his- com m on path ogen esis for cerebral cavern ous m alform at ion s. Neuro-
tor y of intracranial cavernous m alform ations. J Neurosurg 1995;83:56–59 gen et ics 2007;8:249–256
12. Por ter PJ, Willin sky RA, Harper W, Wallace MC. Cerebral cavern ous m al- 33. Zhang J, Clat terbuck RE, Rigam ont i D, Chang DD, Dietz HC. Interaction be-
form ations: natural history and prognosis after clinical deterioration w ith t ween krit1 an d icap1alpha infers pert urbation of integrin beta1-m ediated
or w ith out h em orrh age. J Neurosurg 1997;87:190–197 angiogenesis in th e path ogen esis of cerebral cavern ous m alform at ion .
13. Barker FG II, Am in -Hanjan i S, Butler W E, et al. Tem poral clustering of Hum Mol Gen et 2001;10:2953–2960
hem orrhages from untreated cavernous m alform ations of the central n er- 34. Brun ereau L, Levy C, Laberge S, Hout teville J, Labauge P. De n ovo lesions in
vous system . Neurosurger y 2001;49:15–24, discu ssion 24–25 fam ilial form of cerebral cavern ous m alform at ions: clin ical an d MR fea-
14. Den ier C, Labauge P, Brun ereau L, et al; Sociéte Fran çaise de Neuroch ir- t u res in 29 n on -Hisp an ic fam ilies. Su rg Neu rol 2000;53:475–482, d iscu s-
gurgie; Sociéte de Neurochirurgie de Langue Fran çaise. Clin ical feat ures sion 482–483
of cerebral cavern ous m alform at ion s pat ien t s w ith KRIT1 m ut at ion s. An n 35. Dan dy W. Ven ous abn orm alit ies an d angiom as of th e brain . Arch Su rg
Neurol 2004;55:213–220 1928;17:715–793
15. Rigam on t i D, Spet zler RF. Th e associat ion of ven ou s an d cavern ou s m al- 36. Kivelev J, Niem elä M, Hern esn iem i J. Treat m en t st rategies in cavernom as
form at ion s. Repor t of four cases and discussion of th e path ophysiological, of th e brain an d spin e. J Clin Neurosci 2012;19:491–497
diagn ost ic, an d th erap eu t ic im p licat ion s. Act a Neu roch ir (Wien ) 1988;92: 37. Labauge P, Bou ly S, Parker F, et al; Fren ch St u dy Grou p of Sp in al Cord
100–105 Cavern om as. Outcom e in 53 pat ien t s w ith spin al cord cavern om as. Su rg
16. Bat ra S, Lin D, Recin os PF, Zh ang J, Rigam on t i D. Cavern ous m alform a- Neu rol 2008;70:176–181, discussion 181
t ion s: n at ural h istor y, diagn osis an d t reat m en t . Nat Rev Neurol 2009;5: 38. Ch urchyard A, Kh angure M, Grainger K. Cerebral cavern ous angiom a: a
659–670 poten t ially ben ign con dit ion ? Successfu l t reat m en t in 16 cases. J Neurol
17. Abdulrauf SI, Kayn ar MY, Aw ad IA. A com parison of th e clin ical profile of Neurosurg Psych iat r y 1992;55:1040–1045
cavern ous m alform at ion s w ith an d w ith out associated ven ous m alform a- 39. Ferroli P, Casazza M, Marras C, Men dola C, Fran zin i A, Broggi G. Cerebral
t ion s. Neurosurger y 1999;44:41–46, discussion 46–47 cavern om as an d seizures: a ret rospect ive st u dy on 163 pat ien t s w h o un -
18. Dalyai RT, Gh obrial G, Aw ad I, et al. Man agem ent of in ciden t al cavern ous der w en t pu re lesion ectom y. Neurol Sci 2006;26:390–394
m alform at ion s: a review. Neu rosu rg Focu s 2011;31:E5 40. Abla AA, Lekovic GP, Tu rn er JD, de Oliveira JG, Porter R, Sp et zler RF. Ad-
19. Labauge P, Brun ereau L, Laberge S, Hou t teville JP. Prospect ive follow -up van ces in th e t reat m en t an d outcom e of brain stem cavern ous m alform a-
of 33 asym ptom at ic pat ien t s w ith fam ilial cerebral cavern ou s m alform a- t ion surger y: a single-cen ter case series of 300 surgically t reated pat ient s.
t ion s. Neurology 2001;57:1825–1828 Neurosurger y 2011;68:403–414, discu ssion 414–415
20. Ch usid JG, Kopeloff LM. Epileptogen ic effect s of pure m et als im plan ted in 41. Rocam ora R, Mader I, Zen t n er J, Sch u lze-Bon h age A. Ep ilepsy su rger y in
m otor cor tex of m on keys. J Appl Physiol 1962;17:697–700 pat ien t s w ith m u lt ip le cerebral cavern ou s m alform at ion s. Seizu re 2009;
21. Vernooij MW, Ikram MA, Tanghe HL, et al. Incidental findings on brain MRI 18:241–245
in the gen eral pop ulat ion . N Engl J Med 2007;357:1821–1828
22. Kat ayam a Y, Tsubokaw a T, Maeda T, Yam am oto T. Surgical m an agem ent
of cavernou s m alform at ion s of the th ird ven t ricle. J Neurosurg 1994;80:
64–72

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35 Surgical Management of
Supratentorial Cavernous
Malformations
Helm ut Bertalanffy, Venelin Gerganov, and Vincenzo Paterno

Alth ough supraten torial cavern ous m alform at ion s (CMs) do n ot to 20% of pat ien t s.1,7 According to recen t radiological an d im m u-
con st it u te a dist in ct grou p, th e division of CMs in to su p ra- an d n oh istoch em ical st udies, CMs are act ive dyn am ic lesion s dem -
in fraten tor ial lesion s h as clin ical, p ract ical, an d edu cat ion al on st rat ing en doth elial proliferat ion an d n eoangiogen esis.
reason s. Th ese vascular m alform at ion s can occur in any supra- Bot h sp orad ic an d fam ilial CMs h ave been d escr ibed . Th e
ten torial locat ion eith er on th e brain su rface or in deep -seated fam ilial CMs com pose u p to 30% of all cases; th ey are in h erited
region s. Th ey can be solit ar y or m u lt ip le, of var iou s sizes, an d in an autosom al dom in an t pat tern w ith in com plete pen et ran ce
in m any in st an ces t h ey can be d etected in cid en t ally. Th e clin i- an d a variable expression pat tern .8,9 Fam ilial cases are su p posed
cal im pact of CMs in th e su p raten torial region largely depen ds to h ave m ore aggressive biological beh avior, w ith in creased
on w h eth er eloquen t or n on -eloquen t region s are affected, an d bleeding an d grow th ten den cy. Molecu lar gen et ic st udies h ave
w h eth er th e lesion h as bled or n ot . Ap p aren tly, deep -seated cav- sh ow n t h at su ch CMs are associated w it h m u t at ion s in t h ree
ern om as ten d to bleed m ore frequ en tly th an th e su perficial on es, gen et ic loci on ch rom osom al arm s 7q (CCM1), 7p (CCM2), an d 3q
an d t h ey are m ore likely to p rod u ce m orbid it y t h an are su p er- (CCM3).4,10 Th eir gen e products are involved in th e organ izat ion
ficial lesion s. of cytoskeletal an d in teren doth elial jun ct ion protein s of vascular
en d oth elium .2,11 Loss of gen e fu n ct ion u lt im ately im p airs en do-
thelial cell–cell junctions and vasculogen esis.11 Fam ilial CMs tend
to be m ult iple, w h ereas sporadic cavern om as occur u sually as
solitar y lesion s.
■ Pathology and Epidemiology of
Cavernous Malformations
Multiplicity
Cavern ou s m alform at ion s are vascu lar m alform at ion s th at con -
sist of a clu ster of th in -w alled capillar y-like sin u soidal ch an n els Up to on e-fifth of pat ien ts w h o h arbor an in t racran ial CM m ay be
th at are lin ed w ith a single layer of leaky en doth eliu m .1,2 Th e affected by m ult iple lesion s. Th e h igh est percen t age of m u lt iple
endothelial layer contains abnorm al tight junctions w ith im paired lesion carriers can be fou n d in h ereditar y cavern om atosis, w h ere
barr ier fu n ct ion .3 Sign ifican t overexp ression an d altered local- u p to 90% of p at ien t s suffer from m ult iple lesion s.1 In m any in -
izat ion of som e cr u cial t ran sm em bran e cell-con t act p rotein s st an ces, th e lesion s m ay be of variou s sizes an d m ay bleed at dif-
an d vascu lar adh esion m olecules in CM t issue h ave been dem on - feren t t im es (Fig. 35.1), ren dering th e th erap eu t ic decision m ore
st rated, w h ich m igh t explain th e CM-associated bleed ing or ooz- difficu lt th an in solitar y lesion s. Alth ough som e of th e m u lt ip le
ing of er yth rocytes.4 As a con sequen ce, th e t ypical h em osiderin - lesion s m ay affect n on -eloqu en t brain areas, ot h ers m ay be lo-
lad en r im arou n d th e lesion is for m ed . Macroscop ically, CMs cated in d eep -seated region s in clu d in g t h e brain stem . Th ere is
appear as berr y-like, reddish-purple lesions w ith variable size and n o gen eral r u le on h ow to m an age p at ien t s p resen t ing w it h
sh ap e an d con tain h em orrh ages in variou s stages of resorpt ion . m u lt ip le in t racran ial cavern om as, especially w h en th e n u m ber
Ch aracterist ically, th ere is n o in ter ven ing brain paren chym a. of lesion s is h igh . Som e sym ptom at ic lesion s m ay require surgi-
Cavern ou s m alform at ion s m ake u p 8 to 15% of all vascu lar le- cal rem oval, w h ereas oth er lesion s m ay be left in p lace bu t n eed
sion s in th e brain .1,5,6 Th ey occu r in 0.1 to 4% of th e pop ulat ion , to be m on itored w ith follow -u p MRI.
based on m agn et ic reson an ce im aging (MRI) an d au topsy st ud-
ies. Th e clin ical prevalen ce, h ow ever, is m uch low er: it h as been
Lesion Grow th
est im ated t h at on ly 25% of t h e affected in d ivid u als becom e
sym ptom at ic.4,5 CMs var y con siderably in size, from a few m illi- Frequ en tly, on e can obser ve an obvious volum e augm en tat ion of
m eters to several cen t im eters. Mu lt ip le lesion s are presen t in 10 an in t racran ial CM on MRI. Th is m ay n ot n ecessarily con st it ute a

419

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420 IV Cerebral and Spinal Cavernous Malformations

a b c d e

f g h

Fig. 35.1a–h Magnetic resonance im aging (MRI) of a 30-year-old man (d,e) Six months later, a huge intralesional hematoma developed within the
suffering from m ultiple intracranial cavernous m alform ations (CMs) since diencephalic cavernom a extending into the left striatum and posterior tha-
early childhood. At the age of 5 he underwent a first surgical procedure for lam ic region. At that tim e the patient suffered from progressive headache,
evacuation of a right-sided parietal cavernom atous hem atom a. His clinical loss of concentration, and right-sided hem ihypesthesia and hem iparesis.
condition rem ained uneventful during the following years, and MRI fol- The rem aining CMs did not change in size. (f) The patient underwent em er-
low-ups were perform ed on a regular basis. (a,b) T2-weighted axial MRIs gency surgery with the aid of neuronavigation and intraoperative MRI. He
perform ed 2 years prior to present ation dem onstrate three distinct le- was placed in the supine position with the head rotated to the right side
sions: one cortical in the left inferior frontal gyrus adjacent to Broca’s area, and firm ly fixed within the special head holder on the intraoperative MRI
another subcortical in the left superior temporal gyrus, and a third sm all operating table. (g) Superimposed diffusion-tensor imaging (DTI) with fiber
lesion bet ween the thalamus and striatum involving the posterior lim b of tracking (green area) revealed that the left corticospinal tract was displaced
the internal capsule (arrow). The patient was sym ptom -free at that tim e. m edial to the lesion. (h) Intraoperative MRI demonstrates total rem oval of
(c) Fifteen m onths later the lesion within the internal capsule clearly in- the hem atom a and the vascular lesion via a left-sided distal transsylvian
creased in size (arrow), but all lesions continued to rem ain clinically silent. approach.

t ru e lesion grow th . An in crease in cavern om a size can be cau sed De Novo Formation
n ot on ly by an in t ralesion al expan ding h em atom a (Fig. 35.2) but
also by t rue proliferat ion of cavern om a t issu e in th e absen ce of a With th e in creasing use of h igh -qualit y MRI, n ew lesion s th at
local h em orrh age. It is kn ow n th at th e size of th e CM m ay in flu - w ere n ot apparen t on previous MRI exam in at ion s m ay n ow be
en ce n ot on ly th e clin ical p ict u re bu t also th e ou tcom e in cases of detected, p ar t icu larly in p at ien ts h arboring m u lt iple in t racran ial
su rgical th erapy. Th erefore, on ce a t ru e lesion grow th by caver- CMs.1,5 The pathom echanism for such a de novo appearance is not
n om a t issue proliferat ion h as been docum en ted on MRI, th e in - precisely kn ow n .11 Never th eless, th e possibilit y of a d e n ovo for-
dicat ion s for su rgical rem oval sh ou ld be carefu lly recon sidered . m ation has clinical significance; patients w ith CMs should be regu-
Cer tain ly, su ch a decision m u st be u n der t aken on a case-by-case larly follow ed w ith an n u al or bian n u al MRI exam in at ion s, even
basis. after successful rem oval of one or several intracranial cavernom as.

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35 Surgical Management of Supratentorial Cavernous Malformations 421

a b c d

e f g h

Fig. 35.2a–h Magnetic resonance im aging (MRI) scan of a 44-year-old he was now willing to undergo surgery. The hem atom a and the underlying
m an. (a,b) T2-weighted axial and sagit tal MRI performed 3 months before CM were completely rem oved m icrosurgically via a distal transsylvian ap-
presentation dem onstrate a hem orrhagic lesion in the left posterior corona proach. (e,f) MRI perform ed 3 days postoperatively dem onstrates tot al
radiata that extends inferiorly into the extraputam inal subinsular area. The removal of the vascular lesion and a decrease of the still persisting perile-
patient’s only complaints consisted of interm it tent sensory disturbances sional edema. (g,h) Computed tom ography (CT) scans taken 6 weeks later
within the left side of his body. Surgery was offered to the patient, but he showed no further abnormalit y. The edem a completely resolved, and the
decided to wait. (c,d) MRI perform ed 6 weeks later shows a dram atic in- patient had an uneventful postoperative course without additional neuro-
crease in size of the intralesional hem atom a surrounded by significant per- logic disturbance.
ilesional edema. Although the patient’s symptoms only slightly deteriorated,

■ Relevant Anatomy ■ Clinical Presentation


Sixt y to 80% of all in t racran ial CMs are located su p raten tor ially Cavernous m alform ations constitute a heterogeneous group w ith
in cor t ical, su bcor t ical, or deep -seated areas.1,12 Pract ically all regard to th eir size, locat ion , biological ch aracterist ics, clin ical
region s of t h e brain m ay be involved by th ese vascular m alfor- presen tat ion , an d n at u ral h istor y. Th ey are dyn am ic lesion s th at
m at ion s. Most are located in th e fron t al lobes, follow ed by th e ten d to ch ange over t im e, w ith periods of sym ptom at ic exacer-
parietal an d th e tem p oral lobes. Th ey m ay reach th e cor t ical su r- bation and alternating periods of rem ission. Clinical disturbances
face of th e brain in various region s such as th e convexit y or basal are cau sed by in t ralesion al or p er ilesion al h em or rh ages or by
area of th e h em isph eres, th e in terh em isph eric an d sylvian fis- t h e m ass effect of th e lesion , an d m ay con sist of seizu res, focal
su res, an d th e gyral su rface w ith in a su lcu s, or th ey m ay involve n eu rologic d eficit s, h em or rh age, h eadach e, in t racran ial hyp er-
th e epen dym al su rface of th e lateral or th ird ven t ricle. In m any ten sion , or hyd rocep h alu s.1,5,10 Sym ptom s var y from m ild (e.g.,
in st an ces, h ow ever, th e lesion m ay be located w ith in th e w h ite t ran sien t h eadach e) to severe (e.g., in t ract able seizu res, severe
m at ter su bcor t ically, or d eep w it h in t h e su bin su lar area, t h e focal n eu rological d eficit s, an d occasion ally even d eat h ).1 Th e
st riat u m or th e t h alam u s. Most ch allenging are CMs located in m ost frequ en t clin ical p resen t ing sym ptom are ep ilept ic seizu res
eloqu en t cor t ical an d su bcor t ical region s becau se of th e experi- (38–70%), follow ed by over t h em or rh age (8–37%) an d focal
en ce n eed ed for ch oosing th e opt im al su rgical approach an d th e n eu rologic deficit s (10–25%).1,5,13 With regard to th eir evolu t ion ,
clin ical an d n eurologic im plicat ion s of su rger y in such areas. n eurologic deficits m ay be tem porar y, progressive, in term it ten t

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422 IV Cerebral and Spinal Cavernous Malformations

a b

Fig. 35.3a,b (a) Preoperative axial T2-weighted magnetic resonance im - Several m onths later, although the lesion had rem ained unchanged on MRI,
aging (MRI) scan of a 31-year-old m an dem onstrates a sm all left-sided an- the patient insisted on being treated because his clinical at tacks had in-
terior temporom esial cavernous m alformation (CM). The subcortical lesion creased in frequency. His vague neurologic findings were interpreted as
m easures only 5 m m in diameter and is surrounded by a sm all rim of hem o- subclinical seizures. (b) Intraoperative MRI dem onstrates total rem oval of
siderin (arrow). The patient had never experienced a hem orrhagic clinical the vascular m alform ation and the adjacent parenchym al tissue (arrows).
episode and there were no neurologic deficit s. His complaints consisted of The intraoperative findings were convincing; the lesion had an appearance
frequent at tacks of nausea, vertigo, and left-sided facial pain that signifi- of a t ypical CM, and the surrounding brain showed pathological changes
cantly affected his qualit y of life. Initially, it was unclear whether the tempo- with hem osiderin deposits and increased gliotic-like consistency. Im m edi-
ral CM had caused these symptoms, and a wait-and-see course was adopted, ately after surgery the epilepsy was eliminated, and the patient rem ained
particularly as no abnormalit y was detected on electroencephalograph (EEG). seizure-free during the 4-m onth postoperative follow-up period.

or fixed. Alm ost 20%of patients are asym ptom atic, the CMs being Estimating the Risk of Hemorrhage and
fou n d in ciden tally on MRI exam in at ion s. Rehemorrhage in a Specific Case
Bet w een 35% an d 70% of sym ptom at ic su p raten tor ial CMs
m ay cau se recu r ren t ep ilept ic seizu res. Seizu res are refractor y Un for t un ately, th ere are n o object ive clin ical or n euroradiologi-
to m edicat ion in 40% of th e cases. Th e risk of epilept ic seizure cal cr iter ia t h at can be u sed to p recisely est im ate t h e r isk of
occurrence h as been est im ated at 1.51%per person /year or 2.48% h em orrh age in a specific pat ien t , or th e risk of reh em orrh age in
per lesion /year.1,14,15 CMs are n ot con sidered in t rin sically ep ilep - a lesion th at h as previously bled. As a gen eral rule, it can be ob -
togen ic; th e abn orm al epilept ic act ivit y is in duced th rough th eir ser ved th at lesion s th at bleed at least t w o t im es h ave a h igh er
effect on th e surrou nding brain t issu e d u e to gliosis, deposit s of propen sit y for fu r th er bleeding th an lesion s th at h ave bled on ly
blood breakdow n products, isch em ia, ven ous hyper ten sion , an d on ce. In m any in stan ces, an in it ial single h em orrh age m ay be fol-
in flam m ator y react ion s.14 Th e focus of epileptogen ic act ivit y is low ed by a long silen t p eriod. We h ave obser ved even large in tra-
usu ally th e gliot ic h em osiderin -stain ed p erilesion al brain t issue lesion al cavern om atou s h em atom as th at gradu ally disap p eared
(Figs. 35.3 an d 35.4). On th e oth er h an d, CMs m ay in du ce sec- th ereafter w ith ou t recu rren t bleeding. Th u s, w e ten d to adopt a
on dar y epileptogen ic foci in rem ote brain t issu e, for exam ple in w ait-an d-see policy an d obser ve th e fu r th er beh avior of th e vas-
th e lim bic system , via th eir ch ron ic effect on brain n et w orks. Th e cu lar m alfor m at ion w h en ever t h e p at ien t ’s clin ical con d it ion
du al ep ileptogen ic act ivit y h as to be con sidered w h en p lan n ing allow s it , provided th at th ere is n o sign ifican t m ass effect caused
th e operat ive st rategy. by th e in t raparen chym al cavern om a.
Th e an n u al h em or rh age rate in su p raten tor ial CMs is 0.25
to 5%.1,10,12,16,17 CMs ten d to bleed m ore frequ en tly after a p rior
h em orrh age.18 A deep locat ion of th e CM is a con t roversial risk
factor for h em orrh age. It h as been est im ated th at 5 to 17% of in -
■ Neuroimaging
t racran ial CMs occu r in th e basal ganglia or th alam u s.16,19 Th ey Neu roim aging sh ou ld provide th e diagn osis an d det ailed in for-
t yp ically cau se con t ralateral sen sorim otor deficits, an d m ore m at ion on size, m u lt iplicit y, locat ion , an d exten t of th e lesion ;
rarely h eadach e, seizu res, h em or rh age, hyd rocep h alu s, h em i- sign s of p reviou s in t ra- or ext ralesion al bleed ing; relat ion to
an op sia, t h alam ic p ain syn d rom es, ext rapyram idal sym ptom s, essen t ial cor t ical an d su bcor t ical st r u ct u res; an d t h e p resen ce
an d dou ble vision . of an associated developm en tal ven ou s an om aly (DVA). CMs are

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35 Surgical Management of Supratentorial Cavernous Malformations 423

a b c

d e f

Fig. 35.4a–f For m ore than 5 years this 21-year-old wom an suffered from The vascular m alform ation was exposed via a right-sided pterional craniot-
recurrent temporal epilepsy with drop at tacks and paresthesia in her fin- omy through the proxim al sylvian fissure with the aid of neuronavigation.
gers of gradually increased frequency. Antiepileptic m edication did not The lesion had the appearance of a t ypical CM em bedded within the sur-
completely elim inate the seizures, and surgery was offered to the patient. rounding brain tissue. The lesion and the adjacent gliotic tissue were com -
(a–c) Preoperative m agnetic resonance imaging (MRI) scan dem onstrates pletely removed microsurgically. (d–f) Postoperative MRI demonstrates the
an 8-m m cavernous m alform ation (CM) located in the right anterior sub- total rem oval of the CM (arrow). The patient had an uneventful postopera-
insular area within the inferior claustrum and in contact with the anterior tive course without additional m orbidit y, and the epileptic seizures were
and inferior putam en, lateral to the anterior perforating substance (arrow). elim inated.

angiograph ically occult . On com puted tom ography (CT) th ey can by Zabram ski et al18 as a t ype I lesion ; oth ers h ave m ixed sign al
frequ en tly be invisible or hyperden se in cases w h ere calcifica- in ten sit y on T1- an d T2-w eigh ted im aging w ith a surroun ding
t ion or blood p rodu cts are p resen t . h em osiderin ring (t ype II); yet oth ers are hypo- to isoin ten se on
Th e d iagn osis of CM is based on MRI, w h ich is t h e m ost sen - T1- and T2-w eighted (t ype III). Type IV CMs are ver y sm all lesions,
sit ive an d sp ecific im aging m ode. Th e st an dard p reoperat ive t ypically visu alized as pu n ct ate hypoin ten se foci on gradien t -
exam in at ion in cludes n at ive an d con t rast-en h an ced T1- an d T2- ech o (GRE) sequ en ces. It rem ain s con t roversial if th is lat ter t ype
w eigh ted MRI. Con t rast-en h an ced MRI is useful in dem on st rat ing correspon ds to cap illar y telangiectasias or to early-st age CMs.
th e in tern al ch aracterist ics of th e lesion an d th e p resen ce of an T2-w eigh ted GRE im aging is t h e m ost sen sit ive im aging
associated DVA, an d for excluding oth er path ological con dit ion s. tech n ique to evaluate CMs.21 On th ese sequen ces th e h em osid-
Typically, a m ixed sign al on T1- an d T2-w eigh ted sequ en ces, su r- erin -laden t issu e h as a hyp oin ten se sign al. Sm all or occu lt CMs
roun ded by a ring of T2 hypoin ten sit y from h em osiderin leakage, can be diagn osed on ly on GRE MRI. A draw back of th is im aging
is seen .20 How ever, th e MRI feat u res of CMs m ay be qu ite h etero- m ode is th e so-called h em osiderin blossom ing effect . Due to th is
gen eous due to th e variable m agn et ic suscept ibilit y of in t ra- or effect th e apparen t size of th e lesion is in creased an d n orm al or
ext ralesion al blood p rodu ct s at differen t st ages. Th erefore, th e h em osiderin -stain ed brain t issu e m ay be m isin terpreted as a
radiological differential diagnosis of hem orrhagic neoplasm s, such CM—a fact th at is ver y im p ortan t in th e surgical decision m ak-
as brain m etastases or gliom as, m eningiom as, lipom as, or inflam - ing. Suscept ibilit y-w eigh ted MRI is a n ew im aging m ode th at is
m ator y disorders, m ay som et im es be difficult .1 Som e CMs are cap able of reliably detect ing n on h em orrh agic cavern om as an d
hyperin ten se on T1- an d T2-w eigh ted im ages and w ere defin ed telangiectasias.22

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424 IV Cerebral and Spinal Cavernous Malformations

Diffu sion -ten sor im agin g (DTI)-based fiber t rackin g an d in creasingly reliable. DTI an d t ractography do n ot require act ive
fu n ct ional m agn et ic reson an ce im aging (fMRI) are t w o m odern pat ien t p ar t icip at ion an d coop erat ion for dat a acqu isit ion , w h ich
im aging m odalit ies th at are cu rren tly in disp en sable in defin ing broad en s th eir ap plicabilit y.
th e opt im al op erat ive st rategy in CMs located in or close to elo-
quent brain areas. fMRI is a techn ique that enables visualizing the
brain areas that becom e active during various activities. Neuron al
act ivat ion leads to a local in crease in en ergy requirem en t s an d to
Associated Venous Malformation
alteration of the deoxyhem oglobin-to-oxyhem oglobin ratio. This On rout in e MRI exam in at ion s, an associated ven ous m alform a-
gen erates th e so-called blood oxygen level-depen den t (BOLD) t ion m ay be detected in on ly 25 to 30% of su p raten torial CMs.1
respon se u sed for gen erat ing th e MR sign al. Th e u t ilizat ion of How ever, recen t h igh -field MRI st u d ies h ave dem on st rated th e
various paradigm s en ables dem on st rat ing n ot on ly th e m otor, presen ce of an associated ven ou s m alform at ion in close vicin it y
som atosen sor y, and visual cortex, but also th e st ruct ures relevant to th e CM m ore frequ en tly th an previously believed.23 Th e clin i-
to th e h igh er brain fu n ct ion s of langu age, m em or y, em ot ion s, cal sign ifican ce of an associated ven ou s m alform at ion seem s to
an d person alit y. fMRI is n on invasive an d can be safely repeated dep en d on it s size. Alth ough sm all ven ou s m alform at ion s th at
m u ltip le t im es (Fig. 35.5). m igh t be coagulated during th e surgical rem oval of a cavern om a
Diffusion-tensor im aging generates fractional anisotropy m aps, do n ot produ ce any addit ion al m orbidit y, larger ven ous m alfor-
w h ich can be used to recon st ruct w h ite m at ter t racts an d dem - m at ion s m ay drain a sign ifican t am ou n t of brain paren chym a
onstrate their spatial relations to the CMs. Furtherm ore, they pro- an d th erefore sh ould be left in tact . Du ring su rger y, it is sufficien t
vide in form at ion on th e organ izat ion of w h ite-m at ter bun dles to coagulate on ly th e bran ch es th at directly drain th e CM. Oc-
an d th eir in tegrit y. Besides th e cor t icosp in al t ract an d th e opt ic clu ding a sign ifican t part of th e ven ou s m alform at ion m ay lead
radiat ion , th e recon st ru ct ion of sm aller t ract s, such as th e arcu- to local edem a an d m ay cause severe n eu rologic deficit s, as w e
ate fascicle, forn ix, or even in dividu al cran ial n er ves, becom es obser ved in on e of our pat ien ts (Fig. 35.6).

a b c d

e f g h

Fig. 35.5a–h (a) Two-and-a-half years before surgery at our institute, this tional MRI (fMRI) shows the lesion located below the hand area of the pre-
32-year-old wom an experienced an initial hemorrhage from a sm all sub- central gyrus. The lesion was rem oved m icrosurgically via a transcentral-
cortical cavernous m alform ation (CM) with headache, right-sided hem ipa- sulcus approach. (e,f) Intraoperative MRI dem onstrates total rem oval of
resis, sensory deficits, gait ataxia, and aphasic disturbances. The patient was the vascular m alform ation; only a sm all resection cavit y is visible (arrow).
initially treated conservatively, and her symptom s gradually resolved. Four (g) Photograph showing the brain surface exposed during surgery with the
weeks preoperatively, a second clinical episode of cavernom atous hem or- entry point through the central sulcus (arrow) and the Ojem ann cortical
rhage occurred; this tim e the symptom s consisted of headache, fatigue, stimulation probe placed on the cortical hand area of the left precentral
left-sided facial pain, and m otor weakness of the right hand. (b,c) Preop- gyrus. (h) Photograph taken during the surgical procedure that was per-
erative m agnetic resonance im aging (MRI) scan dem onstrating the sm all formed in the brain suite operating room; the anesthetized patient is placed
lesion within the precentral white m at ter adjacent to the corticospinal tract on the MRI table for intraoperative im aging.
with a small associated venous malformation (arrow). (d) Preoperative func-

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35 Surgical Management of Supratentorial Cavernous Malformations 425
Fig. 35.6a–f Magnetic resonance im aging (MRI) scans of a
51-year-old wom an. Five years before surgery the patient
underwent MRI exam ination because of visual disturbances
unrelated to her vascular m alform ations. (a,b) At that tim e, a
sm all deep-seated lesion suspect for cavernous m alform ation
(CM) was incidentally found in the left precentral periven-
tricular white m at ter. This lesion was associated with a ve-
nous malform ation (arrow). The patient rem ained symptom
free for 5 years. Then, 2 m onths before surgery, progressive
m otor weakness of the right hand and beginning right facial
weakness developed. (c,d) MRI at that tim e showed a hem or-
rhagic area from a suspected CM with significant perilesional
edem a in the left precentral white m at ter, t wo sm all satellite
lesions, and an increase in size of the adjacent venous m alfor-
a b m ation (arrows). The patient underwent surgery and the le-
sion was exposed m icrosurgically through the left precentral
sulcus with the aid of neuronavigation. As several tributaries
of the venous m alform ation surrounded the external surface
of the lesion, som e of them had to be coagulated and tran-
sected to be able to com pletely rem ove the CM. This led to
an increase of the local edem a within the white m at ter docu-
mented on CT scans (not shown in this figure), which explained
the initial postoperative severe aphasia and deteriorated motor
function of the right hand. These neurologic deficits gradu-
ally improved in the following days. (e,f) Three m onths after
surgery, a small resection cavit y and the rem aining part of
the venous m alformation are visible on MRI (arrow). By that
tim e the patient had fully recovered neurologically.

c d

e f

m alform at ion is of cru cial im portan ce for furth er decision m ak-


■ Clinical Management of ing. In addit ion to th e pat ien t ’s age an d sex, th e follow ing in for-
Supratentorial Cavernous m at ion sh ould be obtain ed: th e exact date of sym ptom on set , a
Malformations descript ion of th e sym ptom s an d th eir evolu t ion over th e days
follow ing on set to estim ate the velocit y of sym ptom developm ent,
General Aspects th e occu rren ce an d t im e st age of a secon d clin ical exacerbat ion
suggest ing a secon d or recu rren t bleeding even t , th e p at ien t’s
Sym ptom at ic p at ien t s h arbor ing a CM are often in it ially seen
m edicat ion at th e t im e of sym ptom on set an d at th e t im e of th e
by m edical specialists oth er th an n eurosurgeon s. Th ese special-
in ter view , t h e p ossibilit y of p regn an cy in fem ale p at ien t s, an d
ist s m ay recom m en d on ly con ser vat ive t reat m en t s. By th e t im e
any com orbidit y.1 Th e MRI sh ould fu rn ish eviden ce of several
t h ese p at ien t s p resen t to n eu rosu rgeon s, t h ey m ay be in t h e
im por t an t feat ures th at h ave been m en t ion ed above.
acute or subacu te st age, w ith fresh cavern om atous h em atom as,
or th ey m ay be experien cing a h em orrh age-free in ter val several
w eeks or m on th s after a h em orrh agic ep isod e. Occasion ally,
p at ien t s m ay presen t w ith a CM detected in ciden tally on MRI
Assessing the Surgical Resectability
perform ed for oth er clin ical in dicat ion s. Obtain ing detailed in - Alth ough tech n ically any in t racran ial cavern om a m ay be resect-
form at ion on clin ical an d m orph ological aspects of th e vascular able in experien ced h an ds, a sm all lesion located deeply w ith in

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426 IV Cerebral and Spinal Cavernous Malformations

dien cep h alic st r u ct u res m ay pose a real ch allenge becau se its Goals of Surgery
rem oval m ay be associated w ith su bstan t ial n eu rologic deterio-
On ce th e in dicat ion s for surger y h ave been establish ed, surger y
rat ion , eit h er tem p orar y or p er m an en t . Many sp ecialist s m ay
sh ould fulfill th e follow ing goals:
classify such a lesion as a su rgically in accessible cavern om a.
Th e m ore exp erien ce th at n eu rosu rgeon s h ave gain ed w ith • Rem ovin g t h e CM com p letely to elim in ate t h e r isk of re-
su rgical rem oval of lesion s sim ilar to th at of a p resen t ing p at ien t , bleeding
th e bet ter th ey can est im ate th e su rgical risks an d provide t h e • Im proving th e clin ical sym ptom s (epilepsy, n eurologic disor-
pat ien t n ot on ly w ith dat a from th e literat u re, bu t also w ith st a- ders), ideally cu ring th e pat ien t of th e disease
t ist ical data from th eir ow n p at ien t series. In form ing th e pat ien t • Avoid in g any sign ifican t m an ip u lat ion of adjacen t brain p a-
about th eir ow n resu lt s an d clearly describing best- an d w orst- ren chym a an d su p er ficial or deep blood vessels u n related to
case scen arios w ill en h an ce th e p at ien t’s con fiden ce, st rength en t h e CM
th e doctor–p at ien t relat ion sh ip , an d en able th e pat ien t to m ake • Ch oosing th e opt im al su rgical ap proach an d u sing an app ro-
a m ore inform ed d ecision . priate m icrosurgical tech n ique (Fig. 35.7)
• Avoid in g com p lete obliterat ion of an associated ven ou s m al-
for m at ion th at m ay sign ifican tly drain adjacen t brain paren -
Indication for Surgery chym a, except for sm all bran ch es directly related to th e CM
In con t rast to superficial lesion s in n on -eloquen t brain region s,
th e vast m ajorit y of d eep -seated lesion s con st it u te a p oten t ial
th reat to th e pat ien t’s h ealth . Never th eless, all sym ptom at ic le-
sion s regardless of th eir locat ion m ay affect th e p at ien t’s daily
■ Alternative Management Options
life an d m ay at least be can didates for su rgical th erapy. Gamma Knife Radiosurgery
Most com m on ly, su rger y of su praten torial CMs is defin itely
in dicated in th e follow ing lesion s: Gam m a kn ife radiosu rger y h as been p rom oted as an altern at ive
opt ion for all CMs, regardless of th eir locat ion , or on ly for th e
• Sym ptom at ic h em or rh agic lesion s cau sin g p ersisten t n eu ro - deep ly located an d su rgically m ore ch allenging lesion s.24–26 Th e
logic disorders or recu rren t ep ilept ic seizu res effect of rad iosu rger y is p ar t ial obliterat ion of, or a d ecrease
• Sym ptom at ic lesion s w ith t w o or m ore bleeding episodes in th e size of, CMs, w h ich sh ou ld low er th e reh em orrh age risk
• On e or m ore sym ptom at ic an d h em orrh agic lesion s of m u lt ip le w ith in 2 years. According to som e recen t st udies, radiosurger y
in t racran ial CMs seem s effect ive in p at ien ts w ith m u lt iple p ret reat m en t h em or-
Hem orrh agic lesion s w ith lit tle or m oderate space-occu pying rh ages. Nagy et al26 evalu ated t w o grou p s of p at ien t s w ith deep -
effect an d th at h ave cau sed on ly m ild sym ptom s (Fig. 35.2), or seated CMs: on e grou p w ith a single sym ptom at ic h em orrh age,
n on h em orrh agic lesion s th at h ave caused on ly a single epilept ic an d th e oth er group w ith m ult iple sym ptom at ic bleeds. Th ey
seizu re, can in it ially be m an aged w ith obser vat ion becau se th e foun d th at gam m a kn ife t reat m en t led to m arked reduct ion of
in it ial even t can be follow ed by a long silen t p eriod. CMs de- rebleeding risk in pat ien t s w ith repeated pret reat m en t h em or-
tected in ciden tally sh ould n ot con st it ute an in dicat ion for sur- rh ages, w h ereas th e ben efit in th ose w ith a single bleed w as less
ger y becau se th ey can be easily m on itored as w ell, w ith clin ical clear. In th e first grou p, th e h em orrh age rate w as 30% p er year
follow -u p exam in at ion s an d repeat MRIs. before t reat m en t , decreased to 15%per year over a 2-year period
an d 2.4%th ereafter. Pat ien ts from th e secon d group h ad 2.2%an -
n ual h em orrh age rate before t reat m en t , 5.1% in th e first 2 years
Timing of Surgery an d 1.3%th ereafter. On ly m in or perm an en t adverse radiat ion ef-
fect s w ere obser ved (7.3% of th e pat ien t s). Oth er auth ors claim
Th e t im ing of su rger y depen ds p rim arily on w h eth er th e p at ien t
th at gam m a kn ife su rger y can effect ively redu ce th e rebleeding
presen ts in th e acu te, su bacu te, or ch ron ic stage of cavern om ato-
rate even in p at ien ts w ith a single sym ptom at ic h em orrh age.27
sis. Sign ifican t in t ra- or perilesion al bleeding m ay requ ire rap id
Desp ite all th ese p u blicat ion s, th ere is n o evid en ce th at radio-
t reat m en t . As m en t ion ed above, sym ptom evolu t ion over t im e
su rger y p rotects p at ien t s w ith CMs again st fu t u re h em orrh age
plays an im portan t role in defining the optim al t im ing of surger y.
risk. Meth od ological difficu lt ies, su ch as select ion bias, variable
We h ave en coun tered th e follow ing sit u at ion s:
d efin it ion of h em or rh agic even t s, an d var iable m et h od s to cal-
• Im m ediate em ergen cy su rger y in cases of a large cavern om a- cu late t h e an n u al h em orrh age rate lim it t h e valu e of t h ese
tous h em atom a an d rap id clin ical deteriorat ion (Fig. 35.1) st u d ies.28 Th e p resu m ed p rotect ive effect of ir rad iat ion m ay
• Early su rger y, but n ot as an em ergen cy p rocedure, in cases of sim ply reflect th e n at u ral biological evolut ion of CMs. St udies on
less dram at ic clin ical evolu t ion ; th e p at ien t m ay th u s h ave su f- th e n at u ral h istor y of CMs h ave sh ow n th at CMs h ave dyn am ic
ficien t t im e to con sider th e n eu rosu rgeon’s recom m en dat ion beh avior: som e rem ain st able, som e in crease in volum e, an d
for surgery and perh aps discuss the m at ter w ith fam ily or other som e d ecrease in volu m e.29 Moreover, t h e an n u al bleed in g r isk
doctors (Fig. 35.6) is n ot con st an t becau se t h ese lesion s are n ot st at ic. An ot h er
• Su rger y at a later stage, th e in dicat ion being based on follow - p oin t w or t h con sid er ing is t h at t h e existen ce of a d irect cor rela-
u p MRI in cases follow ing a st able cou rse after an in it ial h em - t ion bet w een cavern om a size an d risk of h em orrh age h as n ot
orrh age (Fig. 35.2) been proven .10,12 It is also n otew orthy th at radiat ion th erapy is
• No su rgical t reat m en t at presen t , bu t regu lar MRIs ever y 2 to 4 n ot absolutely safe, especially if applied to lesion s in eloquen t
m on th s brain areas.

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35 Surgical Management of Supratentorial Cavernous Malformations 427

a b c

d e f

Fig. 35.7a–f (a–c) Preoperative m agnetic resonance im aging (MRI) scans the surgical exposure of the lesion was planned via the distal sylvian fis-
of a 45-year-old wom an suffering from slight left-sided hemiparesis and sure. (e) Screenshot from neuronavigation showing the trajectory obtained
hem idysesthesia dem onstrate a cavernous m alform ation (CM) with fresh with the navigation pointer and tooltip extension before the skin incision.
intralesional hem atom a located within the posterolateral and superior part (f) The lesion was completely rem oved as seen on the postoperative MRI.
of the right thalam us, superiorly reaching the deep periventricular white The patient had an uneventful postoperative course without any clinical
m at ter. (d) The patient underwent surgery with the aid of neuronavigation. deterioration.
She was placed in the supine position with the head rotated to the left;

Radiosu rger y h as also been recom m en ded for t reat m en t of ■ Microsurgical Resection of
patien ts w ith CM-related ep ilepsy. Based on th e fin dings of a
m u lt icen ter st u dy, Régis et al 30 p rop osed gam m a kn ife rad io - Cavernous Malformations
su rger y for pat ien ts w ith epilepsy an d CMs located in eloquen t Preoperative Planning and Selection of the
areas. Th e ou tcom e an alysis sh ow ed t h at 53% of t h e p at ien t s
Surgical Access Route
becam e seizure-free, an d in 20% a h igh ly sign ifican t decrease in
th e n u m ber of seizu res w as ach ieved. Microsu rgical excision , ac- On ce th e in dicat ion s for surger y h ave been est ablish ed, th e sur-
cording to th e au th ors, sh ou ld be lim ited to cort ical-su bcor t ical gical procedure m u st be m et icu lou sly plan n ed. Preoperat ive t ri-
ep ileptogen ic CMs th at are n ot located in fu n ct ion al cor tex. Con - plan ar MRI w ith fiber t racking an d fMRI p rovide su fficien t dat a
sid er ing t h at t h e r isk of h em or rh age after gam m a kn ife t reat - to en able th e surgeon to ch oose a safe surgical corridor to th e
m en t is n ot elim in ated an d t h at t h e rate of rad iat ion -related CM. Sup erficial lesion s are readily accessible. Deeper lesion s n ot
com plicat ion s is as h igh as 13% in som e st u dies,31 th e ben efit of abut t ing a pial surface m ay be reach ed via a t ran ssu lcal approach
th is t reat m en t m od e is m ore th an qu est ion able. (Figs. 35.5 an d 35.8). Deep -seated cavern om as can distor t an d

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428 IV Cerebral and Spinal Cavernous Malformations

a b

c d

Fig. 35.8a–d This 11-year-old girl suffers from hereditary cavernomatosis shows a huge hem orrhagic lesion at the site of the previously treated left-
and harbored m ultiple intracranial cavernous malform ations (CMs). At the sided frontolateral cavernom a with significant perilesional edem a; the le-
age of 4 years she underwent surgery with complete rem oval of a large sion is located superior to Broca’s area. Despite assum ed complete rem oval
hem orrhagic pontine cavernoma. At that tim e, a left-sided subcortical cav- at previous surgery, it is probable that hidden portions of the left-sided
ernom a within the m iddle frontal gyrus was already present. This lesion frontal CM were the source of this clinically relevant rebleed. The third sur-
was treated m icrosurgically 1 year later with the intention of complete re- gery was perform ed with the intention of complete rem oval of the vascular
m oval. Except for a slight right-sided hem ispastic syndrom e, the patient m alform ation. (c,d) Post operative computed tomography (CT) scan taken
rem ained neurologically stable. Several weeks before surgery at the pres- 1 day after surgery dem onstrates no local abnorm alities. The young patient
ent institute, she developed progressive headache. (a,b) Preoperative MRI had an uneventful postoperative course without any speech problems.

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35 Surgical Management of Supratentorial Cavernous Malformations 429

a b c

d e f

Fig. 35.9a–f This 19-year-old m an suffered from right-sided hem iparesis slightly rotated to the right side; the neuronavigation pointer with tooltip
at tributed to an intralesional bleed from a left-sided striatal cavernous mal- extension shows the trajectory to the lesion. (e) Photograph of the fronto-
form ation (CM). (a,b) Preoperative m agnetic resonance im aging (MRI) temporal orbitozygom atic bone flap obtained in one piece; the lesion was
dem onstrates the t ypical appearance of a CM located within the left glo- exposed via a left-sided combined pterional orbitozygom atic craniotomy
bus pallidus in close vicinit y to the posterior lim b of the internal capsule. and a com bined transsylvian subfrontal approach. (f) Im m ediate postop-
(c) Screenshot from intraoperative neuronavigation shows the planned view- erative CT scan dem onstrates rem oval of the lesion without local side ef-
ing trajectory. (d) The patient is placed in the supine position with the head fects. The patient did well after surgery without additional m orbidit y.

displace adjacent brain struct ures by th eir space-occupying effect Preop erat ive an atom ic an d fu n ct ion al im aging dat a set s, in -
an d th e surroun ding perilesion al edem a. Th ese lesion s require clu d in g fMRI an d DTI-based fiber t rackin g, can be fu sed an d
precise an alysis of all available n eu roradiological im ages before p rocessed to display th e th ree-dim en sion al (3D) relat ion sh ips of
d ecid in g on a su rgical ap p roach . In rare in st an ces, sku ll base th e CM to th e su rrou n ding n eu rovascu lar st ru ct u res (Fig. 35.13).
ap proach es such as th e orbitozygom at ic approach m ay im prove Th is in form at ion form s th e basis for p reoperat ive su rgical p lan -
access to cer tain dien ceph alic lesion s (Fig. 35.9). n ing an d can be ut ilized in th e surgical field for in t raoperat ive
In m ost cases, a t ran ssylvian rou te (Figs. 35.1, 35.2, 35.3, 35.4, n euron avigat ion al guidan ce. In t raoperat ive n euron avigat ion en -
35.7), th e su pracerebellar in fraten torial rou te (Fig. 35.10), th e ables select ing t h e opt im al op erat ive ap p roach an d t rajector y
fron tobasal in terh em isp h eric t ran slam in a-term in alis ap p roach to th e lesion , w h ile sp ar ing cr it ical n eu rovascu lar st r u ct u res.33
(Fig. 35.11), an d th e fron top recen t ral in terh em isp h eric t ran scal- During su rger y, fun ct ion al n euron avigat ion guides th e posit ion -
losal approach (Figs. 35.12 an d 35.13) su fficien t ly p rovide access ing of th e cran iotom y an d th e select ion of th e brain en t r y zon e,
to m ost CMs. Each of th ese surgical access rou tes h as st rength s an d in dicates th e sh or test an d safest corridor to th e lesion (Figs.
an d associated com plicat ion s. 35.1, 35.4, 35.5, 35.6, 35.7, 35.9, 35.13). Sm all deep -seated CMs
can be m ore easily localized an d reach ed by perform ing a t ar-
Intraoperative Visualization and geted t issue dissect ion . For exam ple, if a t ran scallosal approach
is selected, th e targeted in cision of th e corpu s callosu m , w ith th e
Lesion Exposure callostom y p reform ed p arallel to th e path of fibers, m ay decrease
Due to recen t tech n ological developm en ts an d th eir applicat ion th e risk of n europ sych ological m orbidit y. Th e ut ilizat ion of fu n c-
to n eu rosu rger y, safe su rgical rem oval of CMs (even t h ose in t ion al n eu ron avigat ion is esp ecially advan t ageou s in CMs lying
areas con sidered to be too dangerous w h en u sing conven t ion al w ith in or close to crit ical brain areas; it h elp s preven t injur y n ot
tech n iqu es) h as been p erform ed.1,32 on ly to eloquen t cor tex but also to th e subcor t ical con n ect ion s. A

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430 IV Cerebral and Spinal Cavernous Malformations

a b c

d e f

g h i

Fig . 35.10a–i This 32-year-old wom an presented with sym ptom s of cal approach. A m edian suboccipital craniotomy extending superiorly be-
raised intracranial pressure caused by obstructive hydrocephalus due to yond the level of the transverse sinus exposed the posterior aspect of the
a posterior thalam ic cavernom a that compressed the aqueductal region. cerebellum . The dura was sutured to the superior bony rim , enabling ele-
(a,b) Preoperative axial and sagit tal m agnetic resonance im aging (MRI) vating the transverse sinus to enlarge the surgical field. The lesion was ex-
scans dem onstrate the lesion originating from the posterior part of the posed via a left-sided supracerebellar-infratentorial route and completely
right thalam us, with its m edial surface extending into the posterior third rem oved. Both m edial cerebellar bridging veins were preserved. (g –i) Post-
ventricle and touching the left thalam us. (c) The patient was placed in the operative MRI dem onstrates total rem oval of the cavernom a; no additional
sem isit ting position. (d–f) Intraoperative photographs showing the surgi- neurologic deficits were noted postoperatively.

safe distan ce of 5 to 10 m m bet w een eloqu en t cor tex an d t racts, as in t raoperat ive ult rasoun d, CT, or MRI (Figs. 35.1, 35.3, 35.5,
as delin eated by fMRI an d fiber t racking, h as been gen erally rec- 35.11, 35.12, 35.13). In t raoperat ive im age update is n ot required
om m en ded to avoid fu n ct ion al deficits. for m ost CMs (e.g., in large cor t ical or su bcort ical lesion s). Th ey
Du ring su rger y, h ow ever, th e accuracy of th e n euron avigat ion can be safely accessed an d rem oved u sin g t h e in it ial n eu ron avi-
decreases du e to brain distor t ion or sh ift . Th is sh ift is cau sed by gat ion al dat a. Moreover, th e brain sh ift can be redu ced w it h
loss of cerebrosp in al flu id, app licat ion of brain ret ractors, grav- ad equate posit ion ing of th e pat ien t’s h ead, use of sm aller cran i-
it y, an d m ass rem oval. Th u s, th e preoperat ively acquired im aging otom ies, an d ju d iciou s brain ret ract ion . Th u s, in p at ien t s w it h
dat a set s do n ot m atch th e act u al in t raoperat ive relat ion s. Th is in sular cavern om as, th e h ead sh ould be rot ated 90 degrees.32
can be com pen sated for by th e u se of biom ech an ical sim u lat ion Th e gravit y-in du ced brain sh ift occu rs th en on ly in th e ver t ical
algorith m s or various m ath em at ical m odels. Th e m ost efficien t plan e, w h ich ren ders it s effect m ore predictable by th e su rgeon .
m eth od, h ow ever, is th e use of in t raoperat ive im aging tools such In a p reviou sly p resen ted series of pat ien t s w ith in su lar CMs, th e

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35 Surgical Management of Supratentorial Cavernous Malformations 431

a b c

d e f

g h i

Fig. 35.11a–i Im ages of a 33-year-old m an harboring an anterior tha- sure with a sm all parenchym al incision lateral to the superior lam ina termi-
lam ic/hypothalam ic cavernous m alform ation (CM). Although this patient nalis (arrow). The corticospinal tract is located lateral to the lesion (violet),
never experienced a sudden hem orrhagic episode, he suffered from pro- whereas the intact fornices are anterom edial to the CM (green). (f) Intra-
gressive left-sided hem ispastic syndrom e. (a–c) Preoperative triplanar MRI operative photograph showing the resection cavit y while obtaining hem o-
shows the lesion within the anterior portion of the thalam us that also in- stasis with bipolar coagulation. (g–i) Postoperative T1-weighted MRI with
volves the hypothalam us and reaches the superior part of the m idbrain. superimposed contour of corticospinal tracts (violet) and fornices (green)
(d,e) Intraoperative MRI docum ents complete rem oval of the cavernom a. obtained from diffusion-tensor imaging (DTI) and fiber tracking.
The m alform ation was reached through an anterior interhem ispheric expo-

sen ior au th or dem on st rated th e h igh reliabilit y of n avigat ion al provide im ages of h igh qu alit y, in par t icu lar at th e begin n ing of
gu idan ce based on p reop erat ive im aging; th e t arget ing accuracy surger y. Ult rasoun d clearly depicts superficial lesion s, th eir an a-
of th e system w as in sufficien t in on ly on e of eigh t pat ien ts.32 tom ic lan dm arks, an d th e large vessels. Ult rasoun d is less expen -
Th e u lt rasou n d is u sed in eith er a 2D or 3D m od e for in t ra- sive an d less logist ically dem an ding th an in t raop erat ive MRI. A
operat ive im aging. It can also be in tegrated in to an exist ing n eu- further advantage is th at the im age acquisition requires lit tle tim e
ron avigat ion platform or u sed as a separate 3D u lt rasoun d-based an d does n ot in terru pt th e surgical w orkflow ; th e im aging feed-
n avigat ion tool.34 In th e on e-platform con cept , th e ult rasoun d back is alm ost real t im e. Som e draw backs of th e tool in clu de th e
hardw are com ponen ts are in tegrated in to th e n euronavigation. By less clear dep ict ion of deep -seated CMs, th e loss of im age qu alit y
utilizing a sem itransparent color overlay, the visualization of the du ring su rger y, an d th e difficult in terp ret at ion of th e fin dings.
hyperech ogen ic areas is opt im ized. Th e ult rasoun d can also be In t raoperat ive MRI, in par t icular h igh -field MRI, en ables up -
used in divid ually as a st an d-alon e system .35 Modern u lt rasou n ds dat ing both th e an atom ic an d fu n ct ion al n eu ron avigat ion dat a

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432 IV Cerebral and Spinal Cavernous Malformations

a b c d

h
e f g

Fig. 35.12a–h Preoperative m agnetic resonance im aging (MRI) scans of a and painful sensation within the right arm . (a–d) Triplanar MRI t aken 6
34-year-old m an harboring a large diencephalic cavernom a that extends m onths before surgery at our institute; a few sm all areas with intralesional
inferiorly into the m idbrain. The patient becam e symptom atic 3 years be- hem atom a are visible. (e –h) An MRI obtained 2 m onths before surgery
fore surgery with a slight left-sided facial palsy. Two years later, another dem onstrates an increase in the lesion’s volum e due to several fresh intra-
symptomatic episode occurred with dysarthria, dysgraphia, left-sided ptosis, lesional encapsulated hem atom as.

sets. Th e sp ect r u m of available MR sequ en ces an d th e im age th e con ten t (fresh or old h em atom a) un der con t in uou s salin e ir-
qu alit y are com p arable to th at of diagn ost ic MRI. Th ese data can rigat ion . Th is is im p or t an t , esp ecially in deep -seated lesion s, to
be processed, t ran sferred to th e n avigat ion system , an d used fur- redu ce th e lesion volum e an d en able fur th er exposure. How ever,
th er by th e su rgeon . MRI en ables con t rol of th e exten t of rem oval th ere m ay be cases w ith out su ch in t ralesion al h em atom a.
an d dem on st rates th e w h ole brain , in cluding th e perilesion al Th e n ext step involves est ablish ing a clear dissect ion p lan e
areas of in terest . In ou r exp er ien ce, t h is in for m at ion an d t h e bet w een th e outer surface of th e lesion an d th e surroun ding
u p dated fiber t racking dat a th at are t ran sferred to th e n avigat ion brain paren chym a. Th is w ill guaran tee th at th e en t ire lesion w ill
system are ver y h elp fu l in gu iding fu r th er resect ion of com p lex, be successfully evacu ated. A firm scar m ay require sh arp dissec-
deep ly located CMs. Major lim itat ion s to th e w idesp read u se of t ion an d division w ith m icroscissors. Th e p lan e of dissect ion is
th is tech n iqu e are it s h igh cost an d h igh w orkflow dem an ds. first establish ed in all direct ion s, ideally 360 degrees aroun d th e
lesion . Th en t h e lesion is grad u ally sep arated from t h e brain
t issu e an d con com itan tly sh ru n k w ith bip olar cau ter y at a low
Microsurgical Dissection Technique set t ing. Sm all feeding ar teries or drain ing vein s, som e of th em
Cavern ou s m alform at ion s m ay con t ain h em orrh age in variou s perh ap s part of an associated ven ou s m alform at ion , are coagu -
st ages of resolu t ion . Th e m ore frequ en tly th e m alform at ion h as lated an d divided w ith m icroscissors. Tearing th e lesion sh ou ld
bled, th e m ore severe th e scar form at ion w ith in an d aroun d th e be avoided as it m ay h arm th e brain paren chym a, par t icularly in
lesion m ay be. Cavern om as are com posed n ot on ly of soft t issu e, eloqu en t brain areas. In deep -seated lesion s, on ly a sm all su rgi-
su ch as path ological vessels an d con n ect ive t issu e, bu t also of a cal corridor is u su ally available, m ost of th e t im e sm aller th an
ver y firm m at rix of fibers an d m em bran es. Th ese form th e w all th e ou ter diam eter of th e vascu lar m alform at ion . In su ch cases,
of th e cavern s an d den se capsular t issue th at m ay keep th e le- th e p or t ion s of th e cavern om a th at h ave already been sep arated
sion s con n ected to th e su r rou n d in g brain t issu e. On ce a caver- from t h e brain are cu t off t h e m ain lesion an d rem oved . Th is
n om a is ap p roach ed su rgically, great care sh ou ld be t aken to m aneuver offers additional space for further dissection and can be
com p letely rem ove t h e lesion w it h ou t leavin g h id d en p ar t s of repeated several t im es. Th e p resen ce of a h em osiderin -st ain ed
th e m alform at ion beh in d. To ach ieve th is goal an d to m in im ize gliot ic rim aroun d th e cavern om a m ay greatly facilit ate th e dis-
th e su rgical m an ip u lat ion of th e su rrou n ding brain p aren chym a, sect ion . How ever, in som e in stan ces th is gliot ic t issu e m ay be
th e in t ralesion al h em atom a capsu le m ay be op en ed to asp irate absen t an d th e lesion al cavern s m ay be fou n d directly em bedded

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35 Surgical Management of Supratentorial Cavernous Malformations 433

a b c d e

f g h i j

Fig. 35.13a–j Intraoperative m agnetic resonance im aging (MRI) of the evidence of the small satellite lesion within the corpus callosum (arrow) that
sam e patient as shown in Fig. 35.12. (a–c) Screenshots from intraoperative was separated from the m ain lesion by a sm all parenchym al layer. Without
neuronavigation with tool tip extension pointing to the center of the lesion; this intraoperative evidence, the residual would have been m issed and left
the lesion is in close contact with the corticospinal tract located lateral to in place. It was subsequently removed completely. (g–j) Intraoperative pho-
the cavernous m alform ation (CM). Note also further enlargem ent of the tographs showing the lesion exposed transcallosally and the adjacent large
intralesional hem atom a in the posterior part of the cavernom a. (d–f) Tri- venous m alform ation together with the enlarged thalam ostriate vein that
planar intraoperative MRI dem onstrating rem oval of the large thalam ic have been left intact. The patient had a completely uneventful postopera-
cavernom a. The surgeon’s impression at that tim e was that the lesion had tive course without additional neurologic or cognitive deficits.
been completely rem oved. Fortunately, the intraoperative MRI furnished

in to t h e brain p aren chym a, a d elicate sit u at ion esp ecially in a por ted on a series of 79 p at ien ts w ith CMs located in fu n ct ion -
deep -seated locat ion . In su ch cases, th e d issect ion is p erform ed ally eloqu en t supraten torial areas. At 6 m on th s, 81% w ere im -
carefu lly u sing sm all cot ton oids th at h elp separate th e caver- proved relat ive to th eir p reop erat ive con dit ion an d 18% w ere
n om a from t h e brain t issu e u sing m ild bip olar cau ter y. At t h e u n ch anged. Good ou tcom es w ere ach ieved in 97%. Gross et al19
en d of t h e d issect ion , t h e su rgeon m u st carefu lly in sp ect t h e perform ed a m eta-an alysis of th e literat u re on su rger y of basal
resect ion cavit y in all direct ion s to en sure th at n o h idden le- ganglia an d th alam ic CMs an d foun d a 89% resect ion rate, a 10%
sion al rem n an ts are left . We p refer to perform a m et icu lou s low - risk of long-term surgical m orbidit y, an d a 1.9% risk of surgical
in ten sit y cauter y of th e cavern om a bed at th e com plet ion of th e m or talit y.
resect ion . Th is facilitates opt im al h em ost asis an d en ables u s to Alth ough surger y is n ot con sidered th e first-lin e t reat m en t of
address possible rem n an ts of path ological vessels in th e resec- CM-related epilepsy, it s efficacy h as been repeatedly n oted.38 Ex-
t ion cavit y. cision of th e lesion an d of th e surroun ding h em osiderin -st ain ed
gliot ic rim im proves seizu re con t rol in th e m ajorit y of pat ients.1
As sh ow n by Van Gom pel et al,39 a decrease in seizu re frequ en cy
is obser ved in 90% of p at ien t s, an d in 60 to 90% seizure freedom
is ach ieved. According to a m u lt icen ter st u dy of 168 con secut ive
■ Outcome pat ien ts w ith a single su praten torial CM an d sym ptom at ic ep i-
Th e criteria for assessing su rgical ou tcom e are com pleten ess of lepsy,15 70% of th e p at ien t s w ere seizu re free in th e first 3 years
rem oval, presen ce of t ran sien t or perm an en t n eu rologic deterio- p ostop erat ive, an d in 25% on ly rare seizu res or a w or t h w h ile
rat ion , an d con t rol of seizu res. Th e low m orbidit y rate an d th e im provem en t (Engel grades II–III) occurred. No m or talit y w as
favorable neurologic outcom es follow ing m icrosurgical resection obser ved, an d on ly 7% of th e pat ien ts h ad m ild postoperat ive
of CMs ju st ify th eir su rgical m an agem en t . Gen erally, th e surgical n eu rologic deficits. Oth er auth ors h ave presen ted sim ilar surgi-
risks an d resu lt s are dep en den t on t h e CM’s locat ion . In m ajor cal outcom es.14,40
rep or ted series th e op erat ive m ortalit y ranged bet w een 0% an d The epileptic activit y in patients w ith longer history is m ore
1.9%.1,19,36,37 Th e r isk of t ran sien t n eu rologic m orbid it y w as 7.6 d ifficu lt to con t rol.41 In selected cases of ch ron ic or m ore com -
to 21%, an d of perm an en t disabilit y 1.3 to 3.2%. Ch ang et al37 re- p lex seizures, presu rgical invasive or n on invasive elect roen ceph -

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434 IV Cerebral and Spinal Cavernous Malformations

alograph recording, m agn etoen cep h alography, or in t raop erat ive their an atom ic locations and the difficulties associated w ith their
elect rocor t icograp hy m ay be u t ilized as a gu ide to th e exten t of su rgical exp osu re. Modern n eu roradiological im aging p rovides
resect ion .41,42 In pat ien ts w ith m esial tem poral lobe epilepsy, t h e n ot on ly precise m orph ological data con cern ing th e com posi-
elect rocor t icograp h ic fin d ings p r ior to t h e select ive am ygdalo- t ion , size, locat ion , exten t , an d relat ion sh ips of th e lesion , bu t
h ippocam pectom y w ere foun d to correlate w ith outcom e; m ore also dat a related to per t in en t brain fun ct ion . Th e m ost com m on
pat ien ts w ere seizu re free w h en th e spikes w ere rest ricted to th e in dicat ion s for surgical t reat m en t of cavern om as are bleeding
m esiobasal tem poral lobe.43 w ith or w ith out n eurologic con sequen ces an d epilept ic seizures.
In som e cases, t h e severit y of th e h em orrh age m ay even requ ire
em ergen cy su rger y. Radiosu rgical t reat m en t is used in several
cen ters; h ow ever, available dat a do n ot u n equivocally prove th at
■ Conclusion th is t reat m en t m odalit y elim in ates th e risk of recu rren t h em or-
Su praten torial CMs do n ot differ from in fraten torial cavern om as rh age. Th e m ain goal of surger y is com plete rem oval of th e m al-
w ith regard to th eir path om orph ological proper t ies an d th eir form at ion to avoid rebleeding. Associated ven ous m alform at ion s
bleeding prop en sit y. Th e division in to su pra- an d in fraten torial sh ou ld be h an d led cau t iou sly, p ar t icu larly t h ose of large cali-
lesion s h as clin ical, p ract ical, an d ed u cat ion al reason s. Th ese ber, to avoid local ven ous congest ion or in farct ion . Microsurgical
vascu lar m alform at ion s occu r in any supraten torial area of th e ext irp at ion of CMs is cu rren tly th e t reat m en t of ch oice. In expe-
brain in cluding eloquen t region s. Deep -seated lesion s, par t icu- rien ced h an ds, even large an d deep -seated cavern om as can be
larly th ose w ith in th e dien cep h alon , are m ost ch allenging du e to successfully rem oved w ith an acceptably low m orbidit y.

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34. Tirakot ai W, Miller D, Hein ze S, Ben es L, Ber t alan ffy H, Su re U. A n ovel lep sy du e to cavern ou s m alform at ion s. Neu rosu rg Focu s 2006;21:e8
platform for im age-gu ided u lt rasou n d . Neu rosu rger y 2006;58:710–718, 42. Stefan H, Sch eler G, Hu m m el C, et al. Magn etoen ceph alography (MEG)
discu ssion 710–718 pred ict s focal ep ileptogen icit y in cavern om as. J Neu rol Neu rosu rg Psy-
35. Unsgård G, Solh eim O, Lindseth F, Selbekk T. In t ra-operat ive im aging w ith ch iat r y 2004;75:1309–1313
3D ult rasoun d in n eurosurger y. Act a Neuroch ir Suppl (Wien ) 2011;109: 43. Ch en X, Su re U, Haag A, et al. Pred ict ive valu e of elect rocor t icograp hy
181–186 in ep ilep sy p at ien t s w it h u n ilateral h ip p ocam p al sclerosis u n d ergoing
36. Am in -Hanjan i S, Ogilvy CS, Ojem an n RG, Crow ell RM. Risks of surgical select ive am ygdaloh ippocam pectom y. Neurosurg Rev 2006;29:108–113
m an agem en t for cavern ou s m alform at ion s of th e n er vou s system . Neu ro-
su rger y 1998;42:1220–1227, discussion 1227–1228

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36 Surgery for Brainstem
Cavernous Malformations
Adib A. Abla, M. Yashar S. Kalani, and Robert F. Spetzler

Cavernous m alform ation s, or cavernom as, are vascular neoplasm s Factors p redisp osing in dividu als to cavern ou s m alform at ion
th at are ben ign an d can occu r anyw h ere in t h e cen t ral n er vou s rupt ure in clude lesion locat ion in th e posterior fossa,9,11 lesion
system . Brain stem cavern ou s m alform at ion s (in clu d ing th ose in size, a h istor y of previou s ru pt u re, an d th e presen ce of an associ-
th e m idbrain , p on tom esen cep h alic ju n ct ion , pon s, p on tom edu l- ated developm en t al ven ous an om aly.12–14 A h istor y of previous
lar y ju n ct ion , an d m edu lla) accou n t for n early 20%of all in t racra- rupt u re of a cavern ou s m alform at ion is associated w ith as m uch
n ial cavern ou s m alform at ion s.1–4 Th e m ost com m on site w ith in as a 7-fold in crease in th e risk of a fu t ure ru pt u re.2,15,16
th e brain stem for th ese lesion s is th e p on s.5 Com p ared w ith cor- Pat ien t s w it h brain stem caver n ou s m alfor m at ion s h ave a
t ical cavern ou s m alform at ion s, lesion s in th e brain stem are less d ocu m en ted h igh er rate of sym ptom at ic h em or rh age an d re-
likely to rem ain su bclin ical an d are m u ch less likely, if ever, to h em orrh age w h en com pared w ith pat ien t s w ith cavern ous m al-
cau se seizu res. Brain stem cavern ou s m alform at ion s often cau se form at ion s in oth er locat ion s.2 In our cum u lat ive series th at w as
a m yriad of fin dings, in cluding cran ial n er ve deficits an d m otor recen tly rep orted, th e h em orrh age rate for all adult p at ien t s be-
or sen sor y sym ptom s, an d th ey can cause headach es as w ell as fore su rgical p rocedures for brain stem cavern om as w as 4.6% per
diplop ia, ver t igo, an d ata xia. year of life p er pat ien t 8 ; in ch ildren p resen t ing w ith ru pt u red
Not all p at ien t s w it h brain stem caver n ou s m alfor m at ion s brain stem cavern ous m alform at ion s, th e rate is expected to be
requ ire su rger y, so th e n at u ral h istor y of th ese lesion s m ust be sign ifican tly h igh er th an in adu lts, given th eir sh or ter life sp an .
w eigh ed again st th e risks of surger y an d the experien ce of th e Our rate, calcu lated ret rosp ect ively, also n at urally carries a selec-
su rgeon p rior to in it iat in g t h erapy. Th is ch apter ou t lin es t h e in - t ion bias from referral to a cen ter th at sees th ose w ith aggressive
dicat ion s for an d t im ing of su rger y as w ell as th e su rgical ap - lesion s requiring su rger y.
proach es th at p rovid e t h e best access to th ese lesion s w it h ou t Patients w ho have hem orrhage from cavernous m alform ations
jeop ardizing pat ien t ou tcom es. can also u n dergo tem poral clu stering of bleeds.17 In ou r recen t
series describing adu lt an d pediat ric pat ien ts w h o h ad rep eat
h em orrh ages, th e bleed rate per p at ien t per year in th e obser va-
t ion p eriod bet w een th eir first bleed an d th e t im e of su rger y w as
■ Patients’ Clinical Presentation and 35% in adults 8 an d 44% in ch ildren .18 Oth ers h ave fou n d reh em -
Natural History of Brainstem orrh age rates of bet w een 21% an d 60% for brain stem cavern ous
m alform at ion s during th e obser vat ion p eriod.7
Cavernous Malformations
Pat ien t s w h o presen t w ith cavern ou s m alform at ion s can h ave
a h ost of sym ptom s ranging from m ild to devastat ing effects re-
lated to h em orrh age, w h ich m ay in clu de com a an d even death .
Mor t alit y for p at ien t s w ith brain stem cavern ou s m alform at ion s
■ Rationale for and Timing of Operation
ranges from 0 to 17% for th ose w ith recu rren t h em orrh ages.5–7 Brain stem cavern ous m alform at ion s often cause repet it ive h em -
Sym ptom s from brain stem cavern ous m alform at ion s, am ong a orrh age. A rupt ure gen erally displaces rath er th an invades sur-
recen t series of surgically t reated p at ien t s at ou r in st it ut ion ,8 in - rou n ding st ru ct u res, in cluding cran ial n er ve n uclei/t ract s or de-
clu ded cran ial n eu ropathy (63%), sen sor y deficit s (53%), m otor scen ding m otor an d ascen ding sen sor y t ract s. Hem orrh age from
com plain t s (37%), h eadach e (39%), dou ble vision (33%), at axia a cavern ous m alform at ion causes tem porar y n eu rologic deficit s,
(29%), vertigo (25%), n ausea or em esis (17%), dysarthria (12%), and w h ich often im prove over t im e w ith resorpt ion of blood prod-
dysph agia (11%). Morbidit y from th e cavern ou s m alform at ion u ct s. As such , th e in dicat ion s for t im ing of su rger y are n ot clear
ict us or rep eat h em orrh ages cou ld be localized to w h ite m at ter or w ell establish ed. In th e set t ing of im provem en t of sym ptom s,
t ract s or cran ial n er ve n u clei in th e vicin it y of th e lesion . som e su rgeon s argu e th at a su rgical ap p roach sh ou ld be delayed.
Hem orrh age rates at t ribu t able to brain stem cavern ou s m al- In deed, su rgical en t r y in to th e cavern om a cavit y frequ en tly cre-
for m at ion s can be calcu lated from bir th , alt h ough t h is m et h od ates sym ptom s th at m im ic a prior bleed, resu lt ing in tem p orar y
is n ot rigorou sly validated or en t irely accu rate. Th e ret rosp ect ive w orsen ing of th e p at ien t’s d eficit s. Oth er su rgeon s argu e th at
h em or rh age rate sin ce bir t h can var y. Som e au t h ors h ave re- im m ediate su rgical in ter ven t ion after a bleed en ables rem oval of
por ted rates as low as 0.25%,9 w h ereas oth ers h ave repor ted rates blood an d breakdow n produ ct s th at m ay be h arm ful to cran ial
as h igh as 6.5% per pat ien t per year in cases of fam ilial disease n er ve n u clei w h ile m in im izin g com p ression of cr it ical t ract s. It
(1.1% per lesion per year).10 is un likely th at th ese t w o paradigm s w ill ever be tested in a ran -

436

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36 Surgery for Brainstem Cavernous Malform ations 437

dom ized fash ion , an d p at ien t-sp ecific factors m u st be taken in to Table 36.1 Recommended Cranial Approaches Based on Brainstem
con siderat ion p rior to offering su rgical in ter ven t ion . Ou r prefer- Cavernous Malformation Location
en ce is to operate w ith in 4 to 8 w eeks of th e last h em orrh agic
Malformation Location Recommended Approach
ep isode. Ow ing to referral pat tern s, h ow ever, som e p at ien t s are
operated on long after th eir h em orrh agic episodes. In oth er cases Medulla Suboccipital
w h ere th e pat ien t exh ibits rapid declin e, a m ore urgen t in ter- Far lateral
ven t ion m ay be in dicated. At Barrow Neurological In st it u te, w e Pontom edullary Suboccipital
favor aggressive su rgical resect ion of lesion s in p at ien t s w h o are Retrosigmoid
Pons Retrosigmoid (if accessible in CP angle or
sym ptom at ic or of lesion s th at abu t a p ial su rface. In th ose p a-
via MCP)
t ien ts w ith m in im al sym ptom s or for th ose lesion s th at do n ot
Retrosigmoid or supracerebellar
arise to a pial surface, w e favor con ser vat ive m an agem en t .
infratentorial (for lateral/superior MCP
cavernous malform ation)
Suboccipital telovelar (for medial inferior
MCP cavernous malform ation)
■ Surgical Approaches and Adjunct Pontom esencephalic Retrosigmoid
Treatments for Brainstem Lateral supracerebellar infratentorial
Orbitozygomatic (if not obscured by clivus/
Cavernous Malformations petrous apex)
Su rgical ap proach es to th e brain stem are u n dergoing con st an t Mesencephalic Orbitozygomatic
evolut ion .4,8,18 W h ereas h istorically, large sku ll base app roach es Lateral supracerebellar infratentorial
w ere n eeded to approach deep -seated lesion s, m ore recen t ad- (including those extending into
van ces in surgical equipm en t an d tech n iqu e n ow obviate th e thalamus)
n eed for extensive approach es. At ou r cen ter, w e n ow rout in ely Abbreviations: CP, cerebellopontine angle; MCP, m iddle cerebellar peduncle.
use several standard approaches to reach lesions in the brainstem
(Table 36.1). Th ese ap p roach es are adequ ate for th e rem oval of
all brain stem cavern ous m alform at ion s w h en used in conjun c-
t ion w ith app rop riate tech n ological advan ces th at m ay n ot h ave We m on itor both som atosen sor y evoked poten t ials an d m otor
been available during earlier t reat m en t eras. Su ch advan ces in - evoked poten t ials during all brain stem operat ion s. Ideally, th e
clu de th e u se of th e CO2 laser, ligh ted bipolar or m icrosuct ion brain stem is en tered u sing a lateral en t r y p oin t . Th e op en ing
(Fig. 36.1), t ractography/diffuser ten sor im aging, en doscopic an - in to t h e brain stem is gen erally sm all an d ver t ical, r u n n ing p ar-
terior skull base approaches to look at th e ven t ral su rface of th e allel to th e t raversing fibers from th e cor tex. Met icu lou s tech -
brain stem , an d n euron avigat ion . n iqu e facilit ates en t r y d eep in to t h e brain stem for lesion s t h at
Th e su rgical ap proach es do n ot requ ire brain t ran sgression d o n ot abu t t h e p ial m argin . Im age gu idan ce is cr it ical for brain -
before m aking an en t r y in to t h e brain stem , w ith t h e except ion stem cavernous m alform ation surger y, especially for deep -seated
of access via th e m iddle cerebellar p ed u n cle to reach th e p on s. lesion s.

a b

Fig. 36.1a,b (a) Spet zler lighted bayonet-st yle bipolars. (b) Malleable m i- vascular and skull base lesions. J Neurosurg 2012:116:291–300. Reprinted
crosuction instruments. Lighted instrum ents allow for bet ter visualization with perm ission from the Am erican Association of Neurological Surgeons
in deep corridors com m only encountered during brainstem surgery. (From and Journal of Neurosurgery.)
Spet zler RF, Sanai N. The quiet revolution: retractorless surgery for complex

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438 IV Cerebral and Spinal Cavernous Malformations

Fig. 36.2 The t wo-point m ethod is used to deter-


m ine the ideal craniotomy placem ent, which is delin-
eated by the projection onto the cranial surface of
the line connecting the center of the lesion and the
point where it reaches the pial surface. (Courtesy of
Barrow Neurological Institute.)

Select ion of th e app rop riate cran iotom y can be gu ided by th e tors w ith th is approach an d to stay m edial to th e cort icospin al
t w o-poin t m eth od (Fig. 36.2).19 Th is m eth od en t ails placing on e t ract s. In rare in stan ces, th is ap proach h as been u sed to rem ove
poin t in th e cen ter of th e lesion or at w h at is th ough t to be th e lesion s by m an euvering lateral to th e m otor t ract s as w ell. Visu-
lim it of th e resect ion an d th e secon d poin t w h ere th e p ia of th e alizat ion of t h e m id brain can be accom p lish ed by u sing t h e op -
brain stem w ill be en tered m ost favorably. Project ing t h e lin e t icocarot id w in d ow , t h e carot id -ocu lom otor w in d ow , or bot h ,
bet w een t h ese t w o p oin t s on to t h e su r face suggest s w h ich cra- en abling rem oval of th e cavern ous m alform at ion .
n iotom y site w ou ld be best su ited for t h e lesion . In ad d it ion ,
several gen eral tech n ical pearls m ust be closely adh ered to w h en
operat ing on pat ien ts w ith brainstem cavern ous m alform at ion s. Suboccipital Approach
First , it is essen t ial to preser ve th e d evelop m en t al ven ou s an om - Th e su boccip it al ap proach is a w orkh orse for rem oval of brain -
aly associated w ith th e cavern ous m alform at ion . It s sacrifice can stem cavern ou s m alform at ion s as w ell as m ost lesion s in th e cer-
cau se ven ou s hyper ten sion w ith in th e brain stem an d even death . ebellum . It is useful for reach ing posteriorly sit uated lesion s from
Secon d, th e gliot ic rim of t issu e su rroun ding th e cavern ou s m al- th e cer vicom edu llar y ju n ct ion u p to th e floor of th e fou r th ven -
form at ion sh ould also be preser ved. Th ird, th e floor of th e four th t ricle. Using a telovelar varian t of th is app roach w ith d issect ion
ven t ricle sh ou ld be resp ected w ith th ese ap p roach es at all cost s. of th e in ferior m edullar y velum an d tela ch oroidea of th e four th
ven t ricle provides access to lesion s in th e m iddle cerebellar pe-
du n cle (ideally th ose m ore m edially an d in feriorly sit u ated in th e
Orbitozygomatic Approach m iddle cerebellar peduncle). How ever, the floor of the fourth ven-
The orbitozygom atic approach (Fig. 36.3) is best suited for access- tricle near th e facial colliculus is an im portan t landm ark that m ust
in g lesion s bet w een t h e cerebral p ed u n cles, esp ecially ven t ral be recognized and protected; any cavernous m alform ation resec-
lesion s of th e m idbrain . We h ave previou sly p u blish ed tech n ical t ion in th is vicin it y m u st be m et icu lou s. Exop hyt ic lesion s in th is
descript ion s of variat ion s of th e orbitozygom at ic cran iotom y.20 region of th e facial collicu lus are ideally suited to t h is approach
More recen tly, it h as n ot been n ecessar y to rem ove th e en t ire becau se th ey presen t th em selves in to th e fou r th ven t ricle. How -
zygom at ic process, as in a fu ll orbitozygom at ic cran iotom y. In - ever, th ose th at are st ill covered by brain an d do n ot com e to th e
stead, w e perform on ly an aggressive m odified orbitozygom at ic su rface are ver y likely to cau se sixth or seven th n er ve p alsies; for
cran iotom y w ith en ough exposure of th e m iddle tem poral fossa these lesions, w e prefer to w ait for addit ion al h em orrhage to bring
an d w ide sylvian fissure split , an d m obilizat ion of th e tem poral th em to th e su rface. To preven t hydroceph alu s after th e p roce-
lobe as n ecessar y, to p rovide adequ ate visu alizat ion of th e m id- dure, it is im portant to place a piece of Gelfoam in the fourth ven-
brain . Great care m ust be taken to protect basilar ar ter y perfora- t ricle to absorb any in traoperat ive blood th at m ay be presen t .

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36 Surgery for Brainstem Cavernous Malform ations 439
Fig . 36.3a– c (a) The orbitozygom atic approach is depicted, as
is the surgical trajectory (arrow) to anteriorly situated brainstem
lesions. (b) Two separate cavernous malformations in the midbrain
are shown on preoperative axial T1-weighted postcontrast m agnetic
resonance im aging (MRI). (c) Postoperative axial T2-weighted MRI
shows a sm all am ount of postoperative blood after the lesions were
resected via a left orbitozygom atic approach with entry via the in-
terpeduncular fossa. (Courtesy of Barrow Neurological Institute.)

b c

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440 IV Cerebral and Spinal Cavernous Malformations

Retrosigmoid Approach th e m iddle cerebellar pedu n cle. We h ave m oved aw ay from a


su btem p oral ap p roach w ith a m ed ial p et rosectom y to access
The retrosigm oid approach (Fig. 36.4) is a versat ile approach used lesion s of th e pon s, an d n ow w e m ore often use an orbitozygo-
to rem ove lesion s in th e p on s, w h ere lesion s can grow to an in - m at ic approach , if th e cavern ous m alform at ion is m ore an terior
credibly large size. Pon t in e lesion s m ay n ot arise to a pial surface. an d is at th e pon tom esen ceph alic ju n ct ion , or w e use a ret rosig-
In th ese cases, access in to th e pon s is often provided by en tering m oid approach for m ore posteriorly sit uated lesion s. We prefer

a b

c d

Fig. 36.4a–d (a) The retrosigm oid approach is depicted, as is the surgical sagit tal contrast-enhanced (c) m agnetic resonance im aging (MRI). (d) The
trajectory (arrow), to m ore laterally situated brainstem lesions. This ap - postoperative axial T2-weighted MRI shows the resection bed (arrow). (Cour-
proach was used to treat an 11-year-old girl with a brainstem cavernous tesy of Barrow Neurological Institute.)
m alform ation shown preoperatively (arrow) on axial T2-weighted (b) and

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36 Surgery for Brainstem Cavernous Malform ations 441

Fig. 36.5 Depiction of a lateral approach (arrow) to a


pontine cavernous malformation that avoids transgression
of anteriorly situated m otor fibers. (Courtesy of Barrow
Neurological Institute.)

to en ter th e m iddle cerebellar pedu n cle beh in d th e fifth cran ial w ard u sing a ret rosigm oid ap p roach for su ch lesion s, w h ich is
n er ve. In th e case of m ore an teriorly sit uated lesion s, w h ich can m ore m in im ally invasive an d bet ter tolerated . In t radu ral dissec-
be accessed by a ret rosigm oid approach , w e stay lateral to th e t ion involves or visu alizes th e t w elfth n er ve rootlets, as w ell as
m otor fibers (Fig. 36.5). th e ver tebral ar ter y an d posterior in ferior cerebellar ar ter y t ake-
off w h en approach ing th e m edu lla. At th e cran ial aspect of th e
app roach , on e can often visu alize th e sixth cran ial n er ve.
Far-Lateral Approach
Th e far-lateral ap p roach is a u sefu l cran iotom y for accessing le- Lateral Supracerebellar
sion s an teriorly or laterally sit u ated in th e m edu lla or cer vico-
m edullar y jun ct ion . Th e approach can be com bin ed w ith a ret ro-
Infratentorial Approach
sigm oid app roach for addit ion al access. Th e far-lateral app roach Th e lateral su p racerebellar ap p roach is cu rren tly th e m ost com -
involves placing th e p at ien t in a park-ben ch posit ion . We u se a m on varian t of th e supracerebellar in fraten torial approach es
lin ear off-m idlin e in cision to p erform th is app roach , alth ough (Fig. 36.6) for resect ion of brain stem cavern ous m alform at ion s.
oth ers h ave u sed a h ockey-st ick or “lazy S” in cision s to accom - We u se t h is ap p roach w h en accessing lesion s at t h e p oster ior
plish th e sam e.21 We t ypically drill som e of th e occipital con dyle aspect of th e m idbrain , w h en th e en t r y poin t m ay lie n ear th e
to allow for in creased ret ract ion of th e dura laterally an d to fur- takeoff of th e four th cran ial n er ve, or w h en approach ing lesion s
th er ou r abilit y to look m ore m edially. Th e far-lateral approach th rough th e p osterior asp ect of th e am bien t cistern on th e w ay
em p loys a sim ilar cran iotom y an d C1 lam in ectom y to th e su b - to rem oving lesion s th at exten d in to th e th alam us. Altern at ively,
occip it al ap p roach , alt h ough w it h t h e far-lateral ap p roach t h e th ose lesion s th at sit except ion ally h igh in th e m iddle cerebellar
C1 lam in ectom y can be a h em ilam in ectom y an d th e cran iotom y pedu n cle, n ear th e su p erior cerebellar p edu n cle, can be accessed
is m ore eccen t r ic to t h e sid e of t h e op erat ion . Mobilizat ion of from above. Th e lateral su p racerebellar app roach can be com -
t h e ver tebral ar ter y is rarely if ever d on e or in d icated in t h is bin ed w ith a ret rosigm oid approach because th e in cision an d th e
ap p roach , bu t t h e ver tebral ar ter y is t h e biggest liabilit y w ith cran iotom ies for t h e t w o sh are m any sim ilar it ies. Th e su p racer-
regard to injur y w ith th e far-lateral approach . It is im por t an t to ebellar ap p roach requ ires less exp osu re of t h e sigm oid sin u s
con t in u ou sly p alpate th e C1 t ran sverse process to keep on e’s ori- an d involves crossing th e t ran sverse sin us w ith th e cran iotom y
en t at ion w ith resp ect to th e ver tebral ar ter y. In previou s years, so th at th e dura can be reflected su periorly. How ever, w h en
w e had used the far-lateral approach for m ore superiorly sit uated com bin ing th e t w o app roach es, it becom es p ossible to m obilize
lesion s, w h ere en t r y in to th e brain stem n ear th e low er cran ial th e cerebellu m d ow nw ard an d m edially aw ay from th e pet rou s
n er ves w as n ecessar y.4,18,19 More recen tly, w e h ave m oved to- bon e.22
(text cont inues on page 446)

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442 IV Cerebral and Spinal Cavernous Malformations

a b

c d

Fig . 36.6a–o (a) Com parison of variations of the supracerebellar infra- infratentorial approach was used to access a m idbrain-thalamic brainstem
tentorial cranial approach to brainstem cavernous m alform ations in the cavernous m alform ation in a 15-year-old girl, shown by the arrow on pre-
m idbrain and upper pons. Three variants of this approach and the trajec- operative axial T2-weighted m agnetic resonance im aging (MRI) through
tory (arrows) afforded by each are illustrated. A left lateral supracerebellar the m idbrain (b) and thalam us (c) and on sagit tal T1-weighted MRI (d).

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36 Surgery for Brainstem Cavernous Malform ations 443

e f g

h i
Fig. 36.6a–o (continued ) A residual lesion was discovered on a postop- m idline (h) and left (i) thalam us. The trajectory of the initial resection is
erative T2-weighted MRI axial view through the m idbrain (e) and lower (f) shown (e,h, arrow), whereas the lim it of the resection (g) and the initial
and upper (g) thalam us; it was also visible on sagit tal views through the resection cavit y (f,i) are indicated by arrows. (continued on page 444)

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444 IV Cerebral and Spinal Cavernous Malformations

j k

Fig. 36.6a–o (continued ) A second-stage procedure was performed on


postoperative day 4 using the same craniotomy and approach. (j) The tra-
jectory of the second resection is shown by the arrow. (k–o) The extended
cavit y is noted by arrows on postoperative axial T2-weighted MRI (j–l) at
progressively higher levels and sagit tal (m) T2-weighted MRI im ages
through the m idline and progressively m ore lateral images on the left side
l (n,o). (Courtesy of Barrow Neurological Institute.)

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36 Surgery for Brainstem Cavernous Malform ations 445

m n

o Fig. 36.6a–o (continued )

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446 IV Cerebral and Spinal Cavernous Malformations

for m at ion s w ere in t h e brain stem . Th e m ost com m on clin ical


■ Outcomes of Surgical Resection of presen tat ion s of th ese p at ien t s in clu ded cran ial n er ve deficits
Brainstem Cavernous Malformations (51.1%), h em iparesis (40.9%), n um bn ess (34.7%), an d cerebellar
sym ptom s (38.6%). Th e st u dy au th ors n oted n ew p ostoperat ive
Several recen t rep or t s h igh ligh t t h e feasibilit y an d safet y of
d eficit s in 31.2% of cases. At follow -u p , 105 p at ien t s (61.8%)
rese ct in g cave r n ou s m alfor m at ion s in t h e brain ste m an d
im proved, 44 (25.9%) w ere u n ch anged, an d 19 (11.2%) w orsen ed
t h alam u s.4,8,18,23–26
n eu rologically, alt h ough t h ese n u m bers in clu de t h ose w it h
Tw o recen t repor ts from ou r in st it ut ion describe our result s
t h alam ic lesion s. Th e au th ors con clu ded th at good preop erat ive
in ad u lt an d p ed iat r ic p op u lat ion s. In ou r ad u lt ser ies of 260
m odified Ran kin Scale scores (98.2% vs 54.5%, p = 0.001) an d
p atien t s,8 w e n oted a sign ifican t rate of n ew or w orsen ing defi-
single h em orrh age (89% vs 77.3%, p < 0.05) w ere predict ive of
cit s p ostop erat ively (n ew deficit s in 137 p at ien t s [53% of t h e
good long-term outcom e.
coh or t ]). Of t h ese, t h e m ajor it y w ere tem p orar y d eficit s t h at
Li et al25 review ed a series of 242 pat ien t s w h o h ad been
im p roved at follow -u p. Perm an en t n ew deficit s w ere n oted in
t reated w ith m icrosu rgical resect ion . In th is series, com p lete
93 pat ien ts (36%). Perioperat ive com plicat ion s w ere n oted in 74
su rgical resect ion w as ach ieved in 95% of cases, an d p ostopera-
pat ien ts (28%) an d in clu ded th e n eed for t rach eostom y, feed ing
t ive deficit s w ere n oted in 46.3% of p at ien t s. Alth ough 35.1% of
t ube placem en t , an d repair of cerebrospin al fluid leakage. Eigh -
pat ien ts in th is series exh ibited w orsen ing p ostop erat ive defi-
teen pat ien t s experien ced reh em orrh age during th e follow -up
cits, th e m ajorit y im proved to baselin e w ith in 3 to 6 m on th s of
period and 12 required reoperation for residual or recurrent m al-
th e op erat ion . At a m ean follow -u p of 89.4 m on th s, p at ien t con -
form at ion. In th is adult experien ce, th e rate of postoperat ive re-
dit ion h ad im p roved in 60.7%, w as u n ch anged in 28.9%, an d h ad
h em orrh age w as 2%. Ou r adult series in cluded an average follow -
w orsen ed in 10.3%. Th e p ostop erat ive an n u al h em orrh age rate
u p t im e of 51 m on t h s, an d t h e average scores on t h e Glasgow
w as 0.4%. Th e m ean m odified Ran kin Scale scores w ere 2.2 on
Outcom e Scale (GOS) w ere 4.6 at last follow -up com pared w ith
adm ission , 2.6 at disch arge, 2.3 at 3 an d 6 m on th s after su rger y,
4.2 at disch arge an d 4.4 preop erat ively.
an d 1.8 at the m ost recen t evalu at ion .
In ou r p ed iat r ic ser ies of 40 p at ien t s,18 w e n oted a sim ilarly
Gross et al27 recen tly su m m arized ou tcom es of 1,390 pat ien t s
h igh rate of t ran sien t p ostop erat ive d eficit s t h at im p roved in
w h o h ad u n d ergon e brain stem caver n ou s m alfor m at ion su r-
40% of pat ien ts. Cavern ous m alform at ion s in ch ildren ten ded to
ger y. In cases w ith part ially resected cavern ous m alform at ion s,
be larger t h an t h ose in ad u lt s (2.3 cm vs 1.8 cm , resp ect ively).
n early t w o-th irds (62%) rebled. Th e rate of early n eurologic m or-
In ch ildren , th e m ean presen t ing or preoperat ive GOS w as 4.2,
bidit y associated w ith surger y w as 45%. Of th ese pat ien ts, th e
w h ich declin ed to 4.05 at disch arge, but im proved to 4.5 at last
m ajorit y required tracheostom y or gastrotom y procedures. W here
follow -up. Pat ien t sym ptom s im proved com pared w ith baselin e
long-term follow -u p w as available, th e dat a suggest t h at m ost
for 16 pat ien ts. On ly five pat ien ts w ere suspected to h ave reh em -
pat ien ts im p rove after resect ion of th eir m alform at ion . Th e over-
orrh age, w ith t w o requiring surger y over an average 31.9 m on th s
all surgical or cavern om a-related m or talit y rate w as 1.5%.
of clin ical follow -u p. A quar ter of th e pat ien t s in our pediat ric
series w ere left w ith a n ew p erm an en t deficit . We n oted a h igh er
rate of reh em or rh age (5.25% an n u al rebleed r isk after su rger y)
in th e pediat ric popu lat ion com pared w ith th e adu lt populat ion
described above.
■ Conclusion
In ou r exp er ien ce, m ost p at ien t s w it h brain stem caver n ou s Operat ing on brain stem cavern ous m alform at ion s is n ot w ith out
m alfor m at ion s h ad favorable ou tcom es p ost su rger y an d t h e in h eren t risk an d th e decision to t reat sh ould be based on th e
vast m ajor it y d id n ot rebleed in eit h er series; 87.5% of p ed iat - n at ural h istor y of th e lesion , surgeon experien ce, an d expected
r ic p at ien t s an d 92.3% of ad u lt p at ien t s did n ot exp erien ce a rates of m orbidit y. Recent advances have allowed for less destruc-
reh em or rh age after su rger y. Th is com p ares favorably to th e p re- t ive ap proach es to deep -seated lesion s. Adju n ct s, su ch as n eu ro-
op erat ive h em or rh age rates of 97.5% of ch ild ren an d 96.9% of n avigat ion , physiological m on itoring, an d bet ter surgical tools,
ad u lt s. h ave m in im ized m orbidit y an d im proved pat ien t outcom es. De-
Stein berg’s grou p 26 recen t ly su m m ar ized th e St an ford Un i- spite th ese advan ces, brain stem surger y is associated w ith a h igh
versit y exp er ien ce w it h resect ion of d eep -seated caver n ou s rate of tem p orar y n eu rologic d eficit s, an d p at ien t s sh ou ld be
m alform at ion s of th e brain stem an d th alam u s. Of 176 pat ien ts cou n seled on t h e p ossibilit y of tem p orar y d isabilit y p r ior to
h arbor in g 179 caver n ou s m alfor m at ion s, 136 caver n ou s m al- u n dergoing su rger y.

References
1. Fer roli P, Sin isi M, Fran zin i A, Giom bin i S, Solero CL, Broggi G. 5. Frit sch i JA, Reulen HJ, Spet zler RF, Zabram ski JM. Cavern ou s m alform a-
Brain stem caver n om as: lon g-ter m resu lt s of m icrosu rgical resect ion in t ions of th e brain stem . A review of 139 cases. Act a Neurochir (Wien )
52 p at ien t s. Neu rosu rger y 2005;56:1203–1212, d iscu ssion 1212–1214 1994;130:35–46
2. Sam ii M, Egh bal R, Car valho GA, Mat th ies C. Surgical m anagem en t of 6. Por ter PJ, Willin sky RA, Harper W, Wallace MC. Cerebral cavern ou s m al-
brain stem cavern om as. J Neu rosu rg 2001;95:825–832 form at ion s: n at ural h istor y an d progn osis after clin ical deteriorat ion
3. Wang CC, Liu A, Zh ang JT, Su n B, Zh ao YL. Su rgical m an agem en t of brain - w ith or w ith out h em orrh age. J Neurosurg 1997;87:190–197
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59:444–454, discu ssion 454 Vascu lar Malform at ions (SAIVMs) collaborators. Un t reated clinical course
4. Porter RW, Det w iler PW, Spet zler RF, et al. Cavernous m alform ations of the of cerebral cavernou s m alform at ions: a prospect ive, populat ion -based
brainstem : experience w ith 100 patients. J Neurosurg 1999;90:50–58 coh or t st u dy. Lan cet Neurol 2012;11:217–224

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8. Abla AA, Lekovic GP, Turn er JD, de Oliveira JG, Por ter R, Spet zler RF. Ad- 19. Brow n A, Th om pson B, Spet zler RF. Th e t w o poin t m eth od: Evaluat ing
van ces in th e t reat m en t an d outcom e of brainstem cavern ous m alform a- brain stem lesion s. Bar row Neu rological In st it u te Qu ar terly 1996;12:
t ion surger y: a single-cen ter case series of 300 surgically t reated pat ien t s. 20–24
Neurosurger y 2011;68:403–414, discussion 414–415 20. Lem ole GM Jr, Hen n JS, Zabram ski JM, Spet zler RF. Modificat ion s to th e
9. Del Curling O Jr, Kelly DL Jr, Elster AD, Craven TE. An an alysis of the n at ural orbitozygom at ic approach . Techn ical n ote. J Neurosurg 2003;99:924–
h istor y of cavern ous angiom as. J Neurosurg 1991;75:702–708 930
10. Zabram ski JM, Wasch er TM, Spet zler RF, et al. Th e n at ural h istor y of fa- 21. Velat GJ, Spet zler RF. Th e far-lateral approach an d it s variat ion s. World
m ilial cavern ous m alform at ion s: result s of an ongoing st u dy. J Neurosurg Neurosurg 2012;77:619–620
1994;80:422–432 22. de Oliveira JG, Lekovic GP, Safavi-Abbasi S, et al. Su p racerebellar in fraten -
11. Moriarit y JL, Clat terbuck RE, Rigam ont i D. Th e n at ural h istor y of cavern - torial approach to cavern ous m alform at ion s of th e brain stem : surgical
ous m alform at ion s. Neurosurg Clin N Am 1999;10:411–417 varian t s an d clin ical experien ce w ith 45 pat ient s. Neurosurger y 2010;
12. Kupersm ith MJ, Kalish H, Epstein F, et al. Nat ural h istor y of brain stem cav- 66:389–399
ern ous m alform at ion s. Neu rosurger y 2001;48:47–53, discussion 53–54 23. Gross BA, Batjer HH, Aw ad IA, Ben dok BR, Du R. Brain stem cavern ous m al-
13. Hasegaw a T, McInern ey J, Kon dziolka D, Lee JY, Flickinger JC, Lun sford LD. form at ion s: 1390 surgical cases from th e literat ure. World Neurosurg
Long-term result s after stereot act ic radiosurger y for pat ien t s w ith cav- 2013;80:89–93
ern ou s m alform at ion s. Neu rosu rger y 2002;50:1190–1197, d iscu ssion 24. Ch en LH, Zh an g HT, Ch en L, Liu LX, Xu RX. Min im ally invasive resect ion
1197–1198 of brain stem cavern ous m alform at ion s: su rgical approach es an d clin ical
14. Abdulrauf SI, Kayn ar MY, Aw ad IA. A com parison of th e clin ical profile of exp erien ces w ith 38 p at ien t s. Clin Neu rol Neu rosu rg 2014;116:72–79
cavern ous m alform at ion s w ith an d w ith out associated ven ous m alform a- 25. Li D, Yang Y, Hao SY, et al. Hem orrh age risk, surgical m an agem en t , an d
t ion s. Neurosurger y 1999;44:41–46, discu ssion 46–47 fun ct ion al outcom e of brain stem cavern ous m alform at ion s. J Neu rosurg
15. Math iesen T, Edner G, Kih lst röm L. Deep an d brainstem cavern om as: a 2013;119:996–1008
con secut ive 8-year series. J Neurosurg 2003;99:31–37 26. Pan dey P, Westbroek EM, Gooderh am PA, Stein berg GK. Cavern ous m al-
16. Kon dziolka D, Lun sford LD, Kestle JR. The n at ural h istor y of cerebral cav- form at ion of brainstem , th alam us, and basal ganglia: a series of 176 pa-
ernou s m alform at ion s. J Neurosu rg 1995;83:820–824 t ien t s. Neurosurger y 2013;72:573–589, discussion 588–589
17. Barker FG II, Am in -Hanjan i S, Butler W E, et al. Tem poral clustering of 27. Gross BA, Batjer HH, Aw ad IA, Ben d ok BR, Du R. Brain stem cavern ou s m al-
hem orrh ages from u nt reated cavernou s m alform at ion s of the cen t ral form at ions: 1390 surgical cases from th e literat ure. World Neurosurg
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18. Abla AA, Lekovic GP, Garret t M, et al. Cavern ous m alform at ion s of th e
brainstem presen t ing in ch ildh ood: su rgical experien ce in 40 pat ien t s.
Neurosurger y 2010;67:1589–1598, discu ssion 1598–1599

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37 Microsurgery of Intramedullary
Spinal Cavernous Malformations
M. Yashar S. Kalani, Maziyar A. Kalani, and Robert F. Spetzler

Cavern ou s m alform at ion s are com m on ben ign vascular lesion s.1 h igh er am ong pregn an t w om en .11,18 Th e risk of CM h em orrh age
Alt h ough p reviou sly t h ough t of as rare lesion s, t h e w id er ap - d u r ing p regn an cy h as recen t ly been ch allenged ; in review in g
p licat ion of m agn et ic reson an ce im agin g (MRI) h as led to m ore t h eir n at u ral h istor y dat a, Kalan i an d Zabram ski 1 d id n ot n ote
frequen t iden t ificat ion of th ese lesion s as culprits for n eu rologic an in crease in th e risk of h em orrh age in w om en w ith isolated or
declin e in p at ien t s.2 Cavern ous m alform at ion s (CMs) con sist of fam ilial CMs du ring p regn an cy, deliver y, or p uerperium .
endothelium -lined vascular channels w ithout intervening norm al Mu lt iple CMs m ay be p resen t in u p to 50% of p at ien t s.19,20 In
paren chym a. Cavern ou s m alform at ion s of th e sp in e are u n com - our recen t experien ce, 8%of pat ien ts h ad fam ilial CMs, an d th ese
m on , bu t lesion s t h at are in t rad u ral,3–5 in t rad u ral ext ram ed u l- pat ien ts w ere m ore likely to h ave brain an d sp in al lesion s.4 In
lar y,6,7 ext rad u ral in t rasp in al,8,9 osseou s lesion s exten d in g in to pat ien ts w ith a sp in al CM w h o u n der w en t brain im aging, 34%
th e ext radu ral sp in al can al,10 an d m ore recen tly a m alform at ion h ad on e or m ore brain lesion s.
th at w as in t ra n eu ron al, perin eu ral, in t radu ral/ext ram edullar y,
ep idural, an d in t raosseou s 11 h ave been rep or ted .
Sch u lt ze 12 is credited w ith th e first successful su rgical re-
m oval of an int ram edullar y CM of th e spin al cord. More recen tly
im provem en t s in im aging an d su rgical tech n iqu e h ave en abled
■ Clinical Presentation
th e iden t ificat ion an d defin it ive t reat m en t of th ese lesion s. Th e Most CMs rem ain asym ptom at ic an d are discovered on ly in ci-
curren t m an tra in th e t reat m en t of spin al CMs is th at com plete den tally or if th ey cau se n eu rologic dysfu n ct ion . It is sp ecu lated
su rgical resect ion sh ou ld be th e goal of th erapy. Mu lt iple series th at sp in al in t ram edu llar y CMs are m ore aggressive th an th eir
h igh ligh t th e safet y an d efficacy of surgical resect ion .3–5,8,9 Su rgi- in t racran ial cou n terpart s.4,21 In th e sp in al cord , CMs are m ore
cal resect ion is associated w ith low m orbidit y an d t h e p oten t ial likely to be fou n d in th e th oracic sp in e 3–5,16,17 (Table 37.1), an d
for fu n ct ion al recover y an d im p rovem en t of dysest h et ic p ain t h e clin ical sym ptom s resu lt in g in t h eir id en t ificat ion are as-
sym ptom s. Th is ch apter review s t h e in cid en ce, p resen t at ion , sociated w ith th eir an atom ic locat ion . Th e t w o m ost frequ en t
an d in dicat ion s of, an d tech n iques for, m icrosurgical resect ion of presen tat ion s of sp in al CMs are secon dar y to su bacu te or ch ron ic
in t ram edu llar y sp in al CMs. m yelop athy or acu te h em orrh age,22,23 w ith m ixed repor t s cit ing
one as the m ore dom inant cause of presentation over the other.3–5
In cases of ch ron ic m yelopathy, th e slow n at u re of disease pro-
gression m ay m im ic a dem yelin at ing process such as m ult iple
sclerosis or Foix-Alajou an in e syn drom e.15 A recen t st u dy cited
■ Epidemiology th e m edian du rat ion of sym ptom s at n early 20 m on th s,5 w ith
Cavern ou s m alform at ion s can be iden t ified in 0.5%of th e gen eral m ost pat ien ts n eu rologically im proving after th eir in it ial episode
p op u lat ion .13 Th ese lesion s are m ore frequ en t ly seen in som e of deteriorat ion .3
racial grou p s, likely cau sed by gen et ic bot tlen ecks an d effect s of Regardless of presen tat ion , th e m ech an ist ic basis of n eu ro-
im m igrat ion of fou n d er p op u lat ion s. Cavern ou s m alform at ion s logic declin e app ears to be repeated cycles of h em orrh age. Acu te
are eith er isolated (a single lesion w ith ou t a fam ily h istor y) or deficits are due to significant hem orrhage. Given the sm all size of
fam ilial (w ith th e pat ien t h arboring m u lt iple lesion s an d w ith a th e sp in al cord an d spin al can al, a large h em orrh age m ay cau se a
fam ily h istor y of CMs). With th e in t roduct ion of MRI, an in creas- rapid expan sion in th e volu m e w ith in th e sp in al can al an d cause
ing n u m ber of cases of CMs bot h in t h e brain an d in th e spin e a rapid declin e seen on exam in at ion . In cases of acu te declin e,
h ave been iden t ified. Spin al CMs accoun t for rough ly 5% of all patien ts frequ en tly p resen t w ith p ain correspon ding to th e level
cen t ral n er vous system (CNS) CMs an d 5 to 12% of spin al vascu- of the lesion. After a hem orrhage, neurologic function can decline
lar m alform ation s.14,15 Th e m ajorit y of cases of sp in al CM are re- for days w it h a gen eral t ren d tow ard im p rovem en t over w eeks
por ted bet w een th e th ird an d fifth decades of life bu t th ey are to m on th s.3–5 Ch ron ic progressive m yelopathy is likely caused by
presen t in all age grou ps.3–5,7,15,16 sm all rep eated ep isodes of h em orrh age cau sing a h em osiderin -
Despite initial reports of a fem ale preponderan ce, several large st ain ed gliot ic cap su le to for m adjacen t to t h e sp in al cord . Th e
clin ical series suggest a 1:1 gen der dist ribu t ion .4,17 Th e role of com bin at ion of h em orrh age, clot form at ion , an d clot resorpt ion
fem ale h orm on es in th e biology of CMs is an area of con t roversy leads to th e release of toxic m et abolites of h em oglobin , leading
an d based on isolated case repor ts; it h as been suggested th at to gliosis, scarring, an d dest r uct ion of n eural t issues. Th e toxic/
th e in ciden ce of h em orrh age (an d h en ce presen t at ion ) m ay be m et abolic alterat ion s an d local pressu re effect s of th e CM on th e

448

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37 Microsurgery of Intram edullary Spinal Cavernous Malform ations 449

Table 37.1 The Distribution of Spinal Cavernous Malformations


Based on Segment of the Spine

Spinal Segment %of Cases

Cervical 20–30
Thoracic 54–77
Lum bar 3–10
Sacral <1

su rrou n ding sp in al cord lead to m yelopath ic sym ptom s. Un like


oth er spin al vascular m alform at ion s such as arterioven ous m al-
form ation s that exh ibit their m axim al sym ptom s at onset, spin al
CMs exh ibit a progression of deficits.24

■ Imaging
Caver n ou s m alfor m at ion s w ere p reviou sly labeled as an gio -
grap h ically occult lesion s, an at t ribu te likely cau sed by th e lack
of direct ar terial input an d th e ven ous n at u re of th ese lesion s.25
As a resu lt , angiograp hy an d m yelograp hy rarely dem on st rate
th ese lesion s, an d given th e availabilit y of n on invasive im aging
m odalit ies, th ese invest igat ion s are rarely in dicated for th e diag-
n osis an d t reat m en t of spin al CMs. Com puted tom ography (CT)
is in sen sit ive, but it is in exp en sive an d easy to obt ain in m ost
cen ters. CT m ay sh ow eviden ce of an in t ram edullar y lesion an d
recen t h em orrh age.15,23
Magn et ic reson an ce im aging is th e im aging m odalit y of ch oice
for th e diagn osis of an d su rgical plan n ing for brain an d spin al
CMs (Figs. 37.1 an d 37.2).2,26 Cavern ou s m alform at ion s are dy-
n am ic lesion s th at exh ibit eviden ce of repeated cycles of h em or- Fig. 37.1 Magnetic resonance im aging (MRI) appearance of spinal cav-
ernous malform ations (CMs). Sagit tal T1-weighted MRIs reveal an iso- to
rhage and resolution of clot. As such, the MRI appearance of these
hypointense lesion, whereas T2-weighted im ages show a hyperintense
lesion s depen ds on th e t im ing of h em orrh age.27 Gen erally, CMs “popcorn-like” lesion with a hypointense rim . Because both the lesion(s)
appear as iso- to hypoin ten se lesion on T1-w eigh ted im ages (Fig. and hem orrhages evolve during the course of the acute bleed and chronic
37.2a) an d a hyperin ten se “popcorn -like” lesion w ith a hypoin - rem odeling of the tissue, the MRI appearance of CMs can vary depend-
ten se rim on T2-w eigh ted im ages (Fig. 37.2b). Th e hypoin ten se ing on the tim ing of this process. (Courtesy of Barrow Neurological
rim visible on T2-w eigh ted im ages is m ost likely at t ribu t able to Institute.)
th e leakage of h em osid erin from rep eated m icroh em orrh ages.26
En h an cem en t w ith gadolin iu m – diet hylen et riam in e pen t aacet ic
acid can also var y across patien ts, resulting in features oth er than
th ose deem ed path ogn om on ic for sp in al CMs. Given th e rar it y of th ese lesion s, th ere are few dat a on t h e
opt im u m t im in g of su rger y for sym ptom at ic cases. Som e au -
th ors h ave specu lated th at a delay of 4 to 6 w eeks after h em or-
rh age allow s for th e form at ion of a d efin able gliot ic p lan e an d
■ Timing of Surgery and Indication ease of resect ion .16 On e can also ch allenge th is opin ion w ith th e
obser vat ion t h at t h e sm all size of t h e sp in al cord an d can al can -
for Intervention n ot tolerate t h e rapid exp an sion in volu m e cau sed by th e bleed,
At Barrow Neurological In st it ute, w e offer surgical in ter ven t ion an d t h at t h e earlier rem oval of t h e m ass an d blood clot m ay h elp
for pat ien ts w ith sym ptom at ic spin al cord CMs an d seldom t reat w ith im p rovem en t by relievin g p ressu re from t h e sp in al cord .
asym ptom at ic pat ien t s w ith in ciden tal lesion s, preferring to A factor correlated w it h p ostop erat ive im p rovem en t h as been
m on itor th em w ith clin ical exam in at ion an d serial MRI. Pat ien t s th e degree of in it ial disabilit y an d sh or t delay u n t il su rgical in -
w ith m ild sym ptom s m ay be follow ed w ith serial exam in at ion s ter ven t ion .29 Pat ien t s t reated soon after th e on set of sym ptom s
to determ in e th e n eed for in ter ven t ion . Th e risk of h em orrh age exh ibit m ore robu st fu n ct ion al im p rovem en t w ith in 3 years of
(est im ated bet w een 1.4%an d 4.5%per year) 16,28 m ust be w eigh ed t reat m en t com p ared w ith p at ien t s w h ose t reat m en t is delayed
again st th e risk of in ter ven t ion in in dividu al cases. (76% vs 52%).

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450 IV Cerebral and Spinal Cavernous Malformations

a b

Fig. 37.2a–d Imaging of a representative patient with an intramedullary spinal


cord cavernous malformation (CM). (a) Sagit tal T1-weighted magnetic resonance
imaging (MRI) demonstrating a mixed intensit y lesion behind the C7 vertebral
body consistent with an intramedullary spinal cord CM. (b) Sagit tal T2-weighted
MRI of the sam e lesion. (c) Axial T2-weighted MRI showing the lesion located
laterally within the spinal cord. This lesion was resected through a myelotomy
at the dorsal root entry zone (DREZ), and the lesion was extirpated with the use
of a carbon dioxide laser. (d) Postoperative sagit tal T1-weighted MRI shows no
residual lesion. (From Mitha AP, Turner JD, Abla AA, Vishteh AG, Spet zler RF.
Outcom es following resection of intram edullary spinal cord cavernous m alfor-
mations: a 25-year experience. J Neurosurg Spine 2011;14:605–611. Reprinted
with permission from the Am erican Association of Neurological Surgeons and
the Journal of Neurosurgery: Spine.) d

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37 Microsurgery of Intram edullary Spinal Cavernous Malform ations 451

n ot arise to a pial surface, a m yelotom y in on e of th ree surgical


■ Operative Procedure corridors can be perform ed ; th ese su rgical corridors in clu de a
Preoperative Considerations m id lin e m yelotom y, a p osterolateral m yelotom y t h rough t h e
dorsal root en t r y zon e (DREZ) an d su bst an t ia gelat in osa, or a lat-
Th e goals of su rger y for spin al CMs are to resolve th e m yelop a- eral m yelotom y ven t ral to th e den t ate ligam en t s (Fig. 37.4).4,16
thy, rem ove th e clot bu rden , h alt th e progression of n eu rologic Posterior-colum n dysfun ct ion h as been reported in m any p a-
d eter iorat ion , an d p reven t fu r t h er h em or rh age resu lt ing in t ien ts u n d ergoing a p osterior app roach .3 After th e m yelotom y is
n eu rologic deteriorat ion . Prior to th e operat ion , th e pat ien t an d perform ed, th e pia is gen tly tacked u p to opt im ize th e exposure.
fam ily sh ould be w arn ed th at postoperat ively th e pat ien t m ay be During th e m yelotom y, th e system ic blood pressu re m ust be kept
t ran sien tly w orse an d th at m ost pat ien ts gen erally im prove bu t elevated to avoid spin al cord isch em ia. We p refer a m ean ar terial
m ay requ ire a m oderate cou rse of postoperat ive reh abilitat ion . pressure of 85 m m Hg du ring th is procedu re.
Pat ien t edu cat ion is crit ical to h elp pat ien t s u n derst an d w h at Caver n ou s m alfor m at ion s are resected u sin g m icrosu rgical
th ey can realist ically exp ect during t reat m en t an d recover y. tech n iqu es u n d er t h e op erat ing m icroscop e. Th e su rgical tech -
n iqu es for rem ovin g sp in al CMs are sim ilar to t h ose u sed to ex-
cise ben ign in t ram edu llar y spin al cord t um ors. Th e except ion is
Intraoperative Monitoring th at sp in al CMs m ay be m ore adh eren t to th e con t igu ou s spin al
cord th an ben ign t u m ors.31 In m ost cases, a gliot ic plan e, cau sed
At Bar row Neu rological In st it u te, sp in al som atosen sor y evoked
by m ult iple episodes of h em orrh age, separates th e lesion from
p oten t ials an d m otor evoked p oten t ials are m on itored in all pa-
t h e n or m al, albeit h em osider in -st ain ed sp in al cord . In p at ien t s
t ien ts u n dergoing su rgical resect ion of sp in al CMs. Baselin es are
w it h lon g-st an d ing an d slow ly p rogressive sym ptom s, likely
obt ain ed before an d after p at ien t s are p osit ion ed to preven t u n -
cau sed by m u lt ip le ep isod es of h em or rh age, t h e sp in al cord
w an ted ou tcom es su ch as vascu lar com p rom ise an d spin al cord
m ay ap p ear at rop h ic.3 Care is t aken to dissect sh arp ly w ith in th e
injur y in pat ien ts w ith sp on dylosis.
gliot ic plan e surroun ding th e lesion to avoid injur y to n orm al
spin al t issue. Th e use of elect rocoagulat ion sh ould be m in im ized,
an d h em osiderin -stain ed t issue sh ould be p reser ved as m uch as
Surgical Technique possible. We p refer to rem ove sm all lesion s en bloc bu t debu lk
Most spin al CMs are dorsally located an d can be app roach via a larger lesion s to p reven t inju r y to th e n orm al sp in al cord.32 Care
p oster ior or p osterolateral ap p roach . We p refer a p oster ior ap - m u st be t aken n ot to rem ove ven ou s m alfor m at ion s frequ en t ly
p roach w ith osteop last ic lam in op last y or lam in ectom y. Bot h associated w it h CMs. Th ese cr ypt ic m alfor m at ion s often ser ve
procedu res can be perform ed by m aking a keyh ole lam in otom y. as th e prim ar y drain age source for region s adjacen t to CMs, an d
A Midas Rex foot plate (Medt ron ic, Elizabeth , NJ) is placed below th eir rem oval can be associated w ith perm an en t sign ifican t defi-
th e lam in a, an d drilling proceeds cep h alad to rem ove th e seg- cits.33 In m ost cases, a sm all am oun t of bleeding is en coun tered
m en t en bloc. Th e du ra m ater is op en ed sh arp ly u sing m icroscis- as th e lesion is dissected free from th e surroun ding spin al cord.
sors an d t acked to th e adjacen t soft t issu es. Carefu l m icroscopic Th is bleeding is u sually ven ous in n at u re an d easily con t rolled.
in spect ion of th e dorsal su rface of th e sp in al cord usually reveals Residu al CMs can reh em orrh age, cau sing fu r th er m yelopathy.
a bluish discolorat ion (Fig. 37.3), w h ich m arks th e locat ion of th e To preven t leaving beh in d a residual, th e bed of th e resect ion
lesion . If th e lesion or discolorat ion is n ot n oted on visu al in sp ec- cavit y m u st be t h orough ly in sp ected , an d h em ost asis obt ain ed
t ion , in t raop erat ive u lt rason ograp hy m ay be u sed to localize th e p r ior to du ral closu re u sing eit h er 4-0 Nu rolon or 6-0 Prolen e
lesion an d to plan th e m yelotom y.30 In cases w h ere th e CM does sut ures. In pat ien ts w h o u n dergo osteoplast ic lam in oplast y, th e

Fig. 37.3 Intraoperative photograph of a spinal cavernous


m alform ation (CM) identified by it s distinct bluish discol-
oration. Although these lesions m ay be readily identified
using m icroscopic m agnification, intraoperative ultraso-
nography m ay be needed to identify lesions without an
exophytic component. (Courtesy of Barrow Neurological
Institute.)

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452 IV Cerebral and Spinal Cavernous Malformations

Fig . 37.4a– c Schem atic represent ation of the surgical safe zones for
placem ent of myelotomy used to resect spinal cavernous m alform ations
(CMs). Arrows depict the trajectories for entry into the spinal cord. The sur-
gical technique used to rem ove these lesions is sim ilar to that used to re-
sect benign intram edullary spinal cord tum ors. Care is taken to dissect
sharply within the gliotic plane surrounding the lesion to avoid injury to
norm al spinal tissue. The use of electrocoagulation should be minimized,
and hemosiderin-stained tissue should be preserved as m uch as possible.
(Courtesy of Barrow Neurological Institute.)

b
c

en bloc lam in ae segm en t s are reaffixed to th e sp in e u sing m icro- cau sed by form at ion of a de n ovo lesion or m ore likely by a sm all
fixat ion titan ium p lates. residu al th at w as n ot detected in t raoperat ively or on follow -up
im aging.

■ Postoperative Considerations
St able p at ien ts u n dergo MRI on postoperat ive day 1 both to ob -
■ Surgical Outcomes
tain a baselin e for com parison of fut ure st udies an d to determ in e Pat ien t s u n d ergoin g su rger y for sp in al CMs often exp er ien ce
t h e p resen ce of resid u al lesion . Th e role of p ostop erat ive MRI t ran sien t n eu rologic w orsen in g d u r in g t h e im m ed iate p ost -
for follow -up of spin al CMs is n ot clear. Th ese st udies are usually op erat ive period, but m ost ret urn to baselin e or im prove over
difficu lt to in terpret becau se h em osiderin -stain ed t issu e is n ot t im e.3–5,21,35 Th e surgical resect ion of dorsally exophyt ic lesions
resected an d th e im aging ch aracterist ics of th is t issue cou ld re- is associated w ith th e low est risk of com plicat ion s, follow ed by
sem ble a residu al CM. dorsal an d ven t ral lesion s. In review ing 117 cases of sp in al CM,
We recom m en d th at follow -u p im aging be obtain ed an n ually Zevgaridis et al16 repor ted im p rovem en t in 66%, n o ch ange in
for at least th e first 2 years after su rger y to m on itor th e p rogres- 28%, an d deteriorat ion of n eu rologic fun ct ion in 6% of pat ien ts.
sion or recu r ren ce of d isease. Sym ptom at ic p at ien t s m ay n eed In an oth er recen t series,5 35.9% w ere im p roved, 54.7% w ere u n -
to be evalu ated m ore frequ en t ly an d closely. In asym ptom at ic ch anged, an d 9%w orsen ed. Jallo et al21 repor ted im m ediate n eu -
p at ien t s w it h a n egat ive MRI, t h e follow -u p in ter vals can be rologic d eclin e in 50% of p at ien t s in t h eir ser ies after su rger y.
in creased. At a m ean follow -u p of 4.5 years, h ow ever, on ly 8% w ere w orse,
Despite p ostop erat ive MRIs con sisten t w ith a radiograp h ic 46% w ere st able, an d 46% h ad im p roved.
cure, recu rren ce rates as h igh as 5% h ave been reported years Th e sen ior au t h or h as su rgically rem oved over 100 sp in al
after resect ion of cerebral CMs.4,34 Th e recu rren ce cou ld be CMs. In repor t ing h is experien ce w ith th e first 80 lesion s, 11% of

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37 Microsurgery of Intram edullary Spinal Cavernous Malform ations 453

Table 37.2 Neurologic Status of Patients Prior to Surgery, at


Immediate Postoperative Assessment and at Long -Term Follow -Up

Immediately Long -Term


Frankel Preoperative, Postoperative, Follow -Up,
Grade n (%) n (%) n (%)

A 1 (1.3) 1 (1.3) 1 (1.6)


B 1 (1.3) 0 (0) 0 (0)
C 9 (11.3) 14 (17.5) 4 (6.4)
D 47 (58.8) 44 (55) 37 (59.7)
E 22 (27.5) 21 (26.3) 20 (32.3)
Total 80 (100) 80 (100) 62 (100)
Source: From Mitha AP, Turner JD, Abla AA, Vishteh AG, Spet zler RF. Outcomes
following resection of intram edullary spinal cord cavernous m alform ations: a
25-year experience. J Neurosurg Spine 2011;14:605–611. Reprinted with
permission from the Am erican Association of Neurological Surgeons and the
Journal of Neurosurgery: Spine.

to exh ibit d eclin es after t h e op erat ion in t h is scen ar io. Alter-


n at ively, if surgical in ter ven t ion is im m ediate, m ore p at ien ts are
Fig. 37.5 Graph showing im m ediate postoperative and long-term out- likely to dem on st rate n o ch ange or to exh ibit im p rovem en t be-
com es of resection of spinal cord cavernous m alform ations (CMs) by the cause they have already suffered a decline due to the hem orrhage.
senior author (R.F.S.). (From Mitha AP, Turner JD, Abla AA, Vishteh AG, Spet- In our experien ce, despite m et iculous surgical resect ion , 5% of
zler RF. Outcom es following resection of intram edullary spinal cord cav-
pat ien ts p resen t again w ith reh em orrh age.4
ernous m alform ations: a 25-year experience. J Neurosurg Spine 2011;14:
605–611. Reprinted with permission from the Am erican Association of In our h an ds th ere w ere few com plicat ion s an d n o m or t alit y
Neurological Surgeons and the Journal of Neurosurgery: Spine.) associated w it h t h e resect ion of in t ram ed u llar y sp in al CMs
(Table 37.3). Im m ediate postoperat ive com plicat ion s w ere n oted
in 6% of p at ien ts an d long-term com plicat ion s in 14%. Sh or t-
term com p licat ion s in clu d ed cerebrosp in al flu id (CSF) leaks
pat ien ts w ere w orse, 83% w ere th e sam e, an d 6% im p roved im -
an d deep ven ous th rom boses. Long-term com plicat ion s in cluded
m ediately p ostoperat ively. At 5-year follow -up , 10% w ere w orse,
spinal cord tethering, kyphotic deform it y, and degenerative spon-
68% un ch anged, an d 23% im proved n eurologically (Fig. 37.5 an d
dylolisth esis of t h e sp in e likely p rom oted by t h e lam in ectom y
Table 37.2).
or lam in op last y. If sym ptom s recu r in t h e absen ce of residu al
In review ing th ese results, it w as n oted th at th e t im ing of sur-
CM after su rger y, local teth ering of th e spin al cord related to scar
ger y can great ly alter ou tcom es im m ed iately after su rger y an d
form at ion sh ould be con sidered.
in th e long term . If su rger y is delayed after a bleed, th e pat ien t
After surgical resect ion , n eurologic deteriorat ion secon dar y
h as t im e to recover from th e bleed, an d m ore pat ien ts are likely
to ch ron ic progressive m yelopathy is less likely to reverse, as
n eu rologic d eficit s are associated w it h a rap id d eclin e.21 Resec-
t ion effect ively t reat s p ain ,36 alt h ough t h is im p rovem en t m ay
Table 37.3 Immediate and Delayed Complications Related to be t ran sien t .37 Th e im m ediate pain relief associated w ith su rgical
Surgical Procedure resect ion m ay be du e to placem en t of m yelotom y an d disru pt ion
Complication N (%) of th e posterior colu m n pain path w ays.
Labauge et al 17 h ave suggested t h at a sp in al locat ion in t h e
Immediate (N = 80) h or izon t al p lan e is associated w it h im p rovem en t p ostop era-
DVT 2 (2.5) t ively. We h ave n oted a sign ifican t cor relat ion bet w een lon g-
CSF leak 2 (2.5)
ter m ou tcom e an d t h e lengt h of t h e lesion in t h e an terop oste-
Serous fluid collection 1 (1.3)
r ior d im en sion .4
Delayed (N = 71)
Kyphosis 4 (5.6)
Tethered cord 3 (4.2)
Stenosis 2 (2.8)
■ Conclusion
Abbreviations: DVT, deep venous throm bosis; CSF, cerebrospinal fluid.
Source: From Mitha AP, Turner JD, Abla AA, Vishteh AG, Spet zler RF. Outcomes Sp in al CMs are vascu lar lesion s am en able to aggressive su rgical
following resection of intram edullary spinal cord cavernous m alform ations: resect ion w ith gen erally good ou tcom es an d m in im al m orbidit y.
a 25-year experience. J Neurosurg Spine 2011;14:605–611. Reprinted with In the m ajorit y of cases a posterior approach can be used to safely
permission from the Am erican Association of Neurological Surgeons and the
Journal of Neurosurgery: Spine.
rem ove t h ese lesion s an d p reven t sequ elae of fu r t h er h em or-
Note: Incidence of each complication is expressed in term s of the num ber of rh age. Su rgical resect ion of th ese lesion s sh ou ld be referred to
patients and percent of total patients. cen ters w ith expert ise in th eir t reat m en t.

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454 IV Cerebral and Spinal Cavernous Malformations

References
1. Kalan i MY, Zabram ski JM. Risk of sym ptom at ic h em orrh age during preg- 20. Vish teh AG, Zabram ski JM, Spet zler RF. Pat ient s w ith spin al cord cavern -
n an cy in cerebral caven ou s m alform at ion s. J Neurosurg 2013;118:50–55 ous m alform at ion s are at an in creased risk for m ult iple neuraxis cavern -
2. Rigam on t i D, Hadley MN, Drayer BP, et al. Cerebral cavern ous m alform a- ous m alform at ion s. Neu rosurger y 1999;45:30–32, discussion 33
t ions. In ciden ce an d fam ilial occu rren ce. N Engl J Med 1988;319:343– 21. Jallo GI, Freed D, Zareck M, Epstein F, Koth bauer KF. Clin ical presen t at ion
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3. Tong X, Deng X, Li H, Fu Z, Xu Y. Clin ical presen t at ion an d surgical out- Neurosurg Focus 2006;21:e10
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4. Mith a AP, Turn er JD, Abla AA, Vishteh AG, Spet zler RF. Ou tcom es follow ing m anagem ent. Neurosurgery 1992;31:219–229, discussion 229–230
resect ion of in t ram edullar y spin al cord cavern ous m alform at ion s: a 25- 23. Zen t n er J, Hassler W, Gaw eh n J, Sch roth G. In t ram edu llar y cavern ous an -
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progn osis of sym ptom at ic pat ient s w ith in t ram edullar y spin al cord cav- KD. Sym ptom at ic cavern ou s m alform at ion s affect ing th e spin e an d spin al
ern om a: clin ical ar t icle. J Neurosurg Spin e 2011;15:447–456 cord. Neurosurger y 1995;37:195–204, discussion 204–205
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haem angiom a (intradural-extram edullar y) underlying repeated subarach - an ce of a cavern ous m alform at ion adjacen t to an exist ing developm en tal
noid h aem orrh age. J Neurol 1982;226:289–293 ven ous an om aly. AJNR Am J Neuroradiol 2005;26:156–159
7. Pagn i CA, Can avero S, Forn i M. Report of a cavern om a of th e cauda equin a 26. Rigam on t i D, Drayer BP, Joh n son PC, Hadley MN, Zabram ski J, Spet zler RF.
an d review of th e literat ure. Surg Neurol 1990;33:124–131 The MRI appearan ce of cavern ous m alform at ions (angiom as). J Neurosurg
8. Hillm an J, Bynke O. Solitar y ext radu ral cavern ous h em angiom as in the 1987;67:518–524
sp in al can al. Repor t of five cases. Su rg Neu rol 1991;36:19–24 27. Zabram ski JM, Wasch er TM, Sp et zler RF, et al. Th e n at u ral h istor y of fa-
9. Padovan i R, Togn et t i F, Proiet t i D, Pozzat i E, Ser vadei F. Ext rath ecal cav- m ilial cavern ous m alform at ion s: result s of an ongoing st udy. J Neurosurg
ern ous hem angiom a. Surg Neu rol 1982;18:463–465 1994;80:422–432
10. Guth kelch AN. Haem angiom as involving th e spin al epidural space. J Neu- 28. San dalcioglu IE, Wiedem ayer H, Gasser T, Asgari S, Engelh orn T, Stolke D.
rol Neurosurg Psych iat r y 1948;11:199–210 In t ram edu llar y spin al cord cavern ous m alform at ion s: clin ical feat ures
11. Oppen lan der ME, Kalan i MY, Dickm an CA. Spin al an d paraspinal gian t and risk of hem orrh age. Neurosurg Rev 2003;26:253–256
cer vical cavern ous m alform at ion w ith post par t um present at ion . J Neu ro- 29. Zevgaridis D, Bü t t n er A, Weis S, Ham burger C, Reu len HJ. Spinal epidural
surg Spin e 2012;16:447–451 cavern ous hem angiom as. Repor t of th ree cases an d review of th e litera-
12. Sch ult ze F. Weiterer Beit rag zu r Diagn ose un d operat iven Beh andlung von t ure. J Neurosu rg 1998;88:903–908
Gesch w ulsten der Rucken m arksh aute un d des Rucken m arks. Duet sch 30. Lun ardi P, Acqui M, Ferran te L, For t un a A. Th e role of in t raoperat ive ult ra-
Med Woch en sch r 1912;38:1676–1679 soun d im aging in th e surgical rem oval of in t ram edullar y cavern ous an -
13. Labauge P, Laberge S, Brun ereau L, Levy C, Tourn ier-Lasser ve E. Heredi- giom as. Neurosurger y 1994;34:520–523, discussion 523
t ar y cerebral cavern ous angiom as: clin ical an d gen et ic feat ures in 57 31. Th om p son BG, Old field EH. Sp in al ar ter ioven ou s m alfor m at ion s. In :
Fren ch fam ilies. Société Fran çaise de Neuroch irurgie. Lan cet 1998;352: W in n HR, ed . You m an s Neu rological Su rger y. Ph ilad elp h ia: Sau n d ers;
1892–1897 2004:2375
14. Sam ii M, Klekam p J. Su rgical resu lt s of 100 int ram edu llar y t um ors in rela- 32. Vish teh AG, Sp et zler RF. Rad ical excision of in t ram ed u llar y caver n ou s
t ion to accom panying syringom yelia. Neurosurger y 1994;35:865–873, an giom as. Neu rosu rger y 1999;44:428
discu ssion 873 33. Vishteh AG, San kh la S, An son JA, Zabram ski JM, Spet zler RF. Su rgical re-
15. Cosgrove GR, Ber t ran d G, Fon t ain e S, Robit aille Y, Melanson D. Cavern ous sect ion of in t ram edullar y spin al cord cavern ous m alform at ion s: delayed
angiom as of th e spin al cord. J Neu rosu rg 1988;68:31–36 com plicat ion s, long-term outcom es, an d associat ion w ith cr ypt ic ven ous
16. Zevgaridis D, Medele RJ, Ham burger C, Steiger HJ, Reulen HJ. Cavern ous m alform ations. Neurosurgery 1997;41:1094–1100, discussion 1100–1101
haem angiom as of th e spin al cord. A review of 117 cases. Act a Neuroch ir 34. Por ter RW, Det w iler PW, Sp et zler RF, et al. Caver n ou s m alfor m at ion s
(Wien ) 1999;141:237–245 of t h e brain stem : exp er ien ce w it h 100 p at ien t s. J Neu rosu rg 1999;90:
17. Labauge P, Bou ly S, Parker F, et al; Fren ch St u dy Grou p of Sp in al Cord 50–58
Cavern om as. Outcom e in 53 pat ien t s w ith spin al cord cavern om as. Surg 35. An son JA, Spet zler RF. Surgical resect ion of in t ram edullar y spinal cord
Neurol 2008;70:176–181, discussion 181 cavern ous m alform at ion s. J Neurosurg 1993;78:446–451
18. Safavi-Abbasi S, Feiz-Erfan I, Spet zler RF, et al. Hem orrh age of cavern ou s 36. Kim LJ, Klopfen stein JD, Zabram ski JM, Son nt ag VK, Spet zler RF. An alysis
m alform at ions during pregn an cy an d in th e peripar t um period: causal or of pain resolut ion after su rgical resect ion of in t ram edullar y spin al cord
coin ciden ce? Case repor t an d review of th e literat ure. Neurosurg Focus caver n ou s m alfor m at ion s. Neu rosu rger y 2006;58:106–111, d iscu ssion
2006;21:e12 106–111
19. San toro A, Piccirilli M, Frat i A, et al. In t ram edullar y spin al cord cavern ous 37. Deut sch H. Pain outcom es after su rger y in pat ien t s w ith in t ram edullar y
m alform at ion s: repor t of ten n ew cases. Neurosurg Rev 2004;27:93–98 sp in al cord caver n ou s m alform at ion s. Neu rosu rg Focu s 2010;29:E15

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V Cerebral and Spinal Aneurysms

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38 Intracranial Aneurysms
Mart in Lehecka, Juhana Frösen, Miikka Korja, Hanna Lehto, Rik u Kivisaari,
Rossana Rom ani, Mika Niem elä, and Juha Hernesniem i

In t racran ial an eu r ysm s (IAs) are acqu ired d ilat at ion s of in t ra- so-called dissect ing or blister-t ype an eur ysm s, presen t as focal
cran ial arteries, an d th ey are t ypically discovered at th e arterial ch anges w ith an ext rem ely t h in ar terial w all th at h as n ot yet d is-
bran ch ing sites n ear th e skull base. Form at ion an d possible r up - ten ded to a clear an eu r ysm sh ape.
t u re of an IA is a m u lt ifactorial even t in w h ich on ly som e of th e In addit ion to sh ap e an d size, IAs are also classified based on
in t rin sic an d ext rin sic risk factors h ave been iden t ified so far. th eir et iology. Traum a to th e ar ter y w all m ay cause an eu r ysm al
W hen an IA rupt ures, it causes a subarachn oid h em orrhage (SAH). dilat at ion , called pseu doan eu r ysm (0.5%, Helsin ki database), in
An an eur ysm al SAH is a devastat ing even t associated w ith a cu- w h ich th e ar ter y w all is disr u pted by t rau m a. Blood t h en leaks
m ulat ive m ortalit y of u p to 50% at 6 m on th s.1,2 An an eu r ysm al ou t from t h e vessel lu m en , d isten d in g t h e ou ter layers of t h e
SAH represen ts on ly 5 to 10% of st rokes, bu t because th e disease ar ter y w all or even prot ruding from th e en t ire w all, follow ing
st rikes at a fairly you ng age for st rokes (50–60 years) an d is often w h ich a h em atom a is created, in side of w h ich blood con t in u es
fat al, th e loss of product ive life years is sim ilar to th at for cerebral to circulate.
in farct ion an d in t racerebral h em orrh age. Earlier, th e t reat m en t In flam m ator y resp on se cau sed by focal in fect iou s disorders
of IAs focused alm ost exclusively on pat ien ts w ith ru pt ured an - in th e in t racran ial arter y w all can also cau se an eur ysm form a-
eu r ysm s. Now, w ith th e in creasing n u m ber of u n r u pt u red IAs t ion . Desp ite being referred to as m ycot ic an eu r ysm s, th ese in -
being iden t ified by m odern im aging m eth ods, preven t ive t reat- fect iou s an eu r ysm s are m ostly of bacterial origin (often dist al
m en t of u n rupt u red IAs h as becom e of equal im por tan ce. an d em bolic in n at ure) an d represen t on ly a ver y sm all por t ion
of IAs (< 0.1%, Helsin ki database). Th eir h istology sh ow s m ore
w idespread degen erat ive ch anges in th e ar ter y w all, an d th ey are
u su ally m ore fragile th an oth er an eur ysm s.
■ Pathophysiology
Structure Origin
An an eu r ysm is a dilat at ion of a blood vessel, in w h ich all t h e Un r u pt u red IAs are ver y rare in ch ild ren bu t t h eir p revalen ce
layers of th e vascular w all are affected by degen erat ive ch anges in creases after 30 years of age.4,5 Moreover, IAs can be in duced in
th at lead to disten t ion of th e vessel. Th e IA w all lacks t h e elast ic laborator y an im als by procedu res th at in du ce hyperten sion an d
lam in as of a n orm al in t racran ial ar ter y w all, an d in con t rast to ch ange th e h em odyn am ic con dit ion s of th e cerebral circu lat ion .
n orm al vascular w all an atom y, th ere are n o clear in t im a, m edia, Th ese obser vat ion s dem on st rate th at IAs are acqu ired p ath olo-
an d adven t it ia layers.3 gies. Alt h ough IAs are n ot congen it al, con gen it al factors t h at
affect th e st ru ct u re an d st rength of in t racran ial ar teries an d th e
h em odyn am ic con dit ion s of th e cerebral vasculat u re m ay pre-
Classification d isp ose to IA for m at ion . In an im al m od els, t h e for m at ion of
in d uced IAs is associated w ith in flam m at ion of th e in t racran ial
Th e IAs are classified, based on th eir sh ape, as saccu lar an eu -
ar ter y w all. Desp ite th e an eu r ysm w all in flam m at ion t h at is
r ysm s, w h ich are pouch -like focal disten t ion s of th e vessel w all,
associated w ith degen erat ion an d r u pt ure,6 m ost an eu r ysm s are
an d as fusiform an eur ysm s, w h ich are t ubular disten t ion s along
n ot cau sed by in fect ion s.
a larger d iseased segm en t of a vessel (Fig. 38.1). Most IAs are
saccu lar (96% of IAs, data from th e Helsin ki Cerebral An eu r ysm
Dat abase; see Clin ical Presen tat ion , below ), an d t ypically arise at Pathophysiology of Aneurysm Wall
proxim al bran ch ing sites of m ajor ar teries. Fu siform an eu r ysm s
Degeneration and Rupture
(3% of IAs, Helsin ki dat abase) occur t ypically bet w een bifurca-
t ion s at p roxim al segm en ts of m ajor in t racran ial ar teries. Histo- Alth ough IA form at ion can be in duced in laborator y an im als,
logically th ey m ostly resem ble saccu lar an eu r ysm s. th ere are n o experim en t al m odels in w h ich IAs w ou ld sp on t an e-
Size can affect th e h istological st r u ct u re of an an eu r ysm . Th e ously rupt u re. Th is m ean s th at IA form at ion is a separate process
t w o ext rem es in size are gian t an eu r ysm s at on e en d of th e con - from IA ru pt u re, as suggested also by th e clin ical obser vat ion
t in u u m an d sm all blister-t ype an eu r ysm s at th e oth er en d . Both th at som e IAs n ever ru pt u re.
presen t w ith a h istop ath ological st ru ct u re differen t from th at Th ere are n o experim en tal m odels w ith spon tan eou s ru pt u re
of ot h er an eu r ysm s. Gian t an eu r ysm s (≥ 25 m m in d iam eter) of an IA, so m ost of th e in form at ion on th e path ophysiology of an
are often ch aracter ized by an on ion -skin –like layered st r u ct u re IA w all degen erat ion an d ru pt ure is derived from obser vat ion al
of t h rom bu s of var iou s ages. Th e u n u su ally sm all an eu r ysm s, st udies com paring t issue sam ples from un rupt ured and rupt ured

457

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458 V Cerebral and Spinal Aneurysms

a b

Fig. 38.1a–c (a) Saccular aneurysm at the basi-


lar bifurcation. (b) Fusiform aneurysm of the
basilar trunk. (c) Blister-t ype aneurysm (arrow) at
c the m edial wall of the left internal carotid artery.

h um an IAs. Th ese st u dies sh ow th at loss of en doth elial cells, lu- in th e IA w all resected on ly a few h ou rs after ru pt u re.3 Th ese
m in al th rom bosis, loss of sm ooth m u scle cells from th e IA w alls, obser vat ion s suggest th at in flam m at ion of th e IA w all precedes
an d event ual degen erat ion of th e ext racellular m at rix are fin d- IA rupt ure.
ings th at are associated w ith IA w all ru pt u re.3,5 In addit ion , in fil- Alth ough in flam m at ion is associated w ith IA w all degen era-
t rat ion of th e IA w all by in flam m ator y cells an d act ivat ion of th e t ion an d precedes a r u pt u re, it is n ot clear w h eth er it is th e cau se
h um oral im m un e system (com plem en t) in th e IA w all are associ- of w all degen erat ion or m erely a react ion to th e processes th at
ated w ith IA w all d egen erat ion an d r u pt ure.3,5,6 in du ce th e degen erat ion . Un like th e ru pt u red IA w all, th e w all
In flam m ator y cells an d com plem en t act ivat ion are detected of an un rupt u red IA con sist s t ypically of an en doth elial layer, a
also in som e un ru pt ured IA w alls an d do n ot correlate w ith t im e sm oot h m u scle cell layer, an d an ou ter layer of con n ect ive t is-
from ru pt u re.3,5 Moreover, in flam m ator y cell in filt rat ion is fou n d su e an d fibroblasts (Fig. 38.2).3 Th e h istological st ru ct u re of th e

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38 Intracranial Aneurysms 459

a b

c d

e f

g h

Fig. 38.2a–h Structure of the intracranial aneurysm (IA) wall can vary be- layer (d). (e,f) Ruptured IA walls are characterized by loss of m ural smooth
t ween aneurysm s and even within a single aneurysm . (a) During surgery, m uscle cells, degradation of the wall m atrix, and inflam m ation of the de-
areas with a very thin and translucent wall m ay be seen (arrows), whereas generated wall. (g,h) Inflam m atory cell infiltration (arrows) is higher in de-
other regions of the wall appear thicker and stronger. (b) Sim ilar focal generated IA walls (inflam m atory cells in brown, lipid filled matrix in red),
changes can be seen in the m acroscopic exam ination of som e of IA fundi than in IA walls that resemble norm al cerebral artery or hyperplastic intima
resected for pathological studies, as well as at the m icroscopic level in his- layer. (Panels c to f are m icrophotographs taken from hem atoxylin-eosin
topathology studies (c–h). Wall structure is associated with rupture of the staining, and panels g and h are m icrophotographs from CD45 im m uno-
aneurysm . Unruptured IAs tend to have a wall that resem bles either a nor- histochem istry stainings with oil-O-red and hem atoxylin background.)
m al cerebral artery wall without elastic laminas (c), or a hyperplastic intim a

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460 V Cerebral and Spinal Aneurysms

sm ooth m u scle layer often resem bles th at of a m yoin t im al hy- of au topsy series an d im aging st udies, th e overall prevalen ce of
perplasia th at develop s in th e ar ter y w all in resp on se to m ech an - u n rupt u red IAs w as est im ated to be about 2%in th e gen eral pop -
ical st ress or inju r y to th e en doth elial or sm ooth m uscle cells.5 u lat ion .7 W h en th e m et a-an alysis is adjusted for age an d sex, th e
W h at cau ses t h e d egen erat ion of t h e u n r u pt u red , m yoin t im al prevalen ce of u n ru pt u red IAs is sign ifican tly h igh er: 3.2% (95%
hyperplasia-like IA w all in to a decellularized, degen erated, an d con fid en ce in ter val [CI], 1.9–5.2) in a m iddle-aged (fifth decade)
in flam ed r u pt u re-pron e IA w all is u n clear. pop u lat ion w ith ou t com orbidit ies an d w ith an equ al sex dist ri-
It seem s that aberrant flow conditions induced by IA geom etry but ion .4 Th e in ciden ce of u n ru pt u red IAs does n ot sign ifican tly
con t ribu te sign ifican tly to IA w all degen erat ion via loss of in t act var y by coun t r y or by eth n ic group, despite differen ces in th e
endothelial layer and form ation of throm bosis on the lum inal sur- in ciden ce of an eu r ysm al SAH am ong eth n ic groups.4
face of th e IA w all.5 IA geom et r y cau ses tor t u ou s flow in side th e Th e p revalen ce of u n r u pt u red IAs is h igh er in fem ales as w ell
IA lum en w ith n onphysiological t ran sm ural pressure an d sh ear as in pat ien ts w ith a fam ily h istor y of an eur ysm al SAH or un r up -
st ress on th e vessel w all. Th ese factors alon e are sufficien t to in - t ured IAs.4 Th ere are n o populat ion -based prospect ive follow -up
du ce ch anges in sm ooth m u scle cell h om eostasis an d loss of in - coh ort st u dies describing th e risk factors for th e form at ion of u n -
tact en doth elial layer, w h ich leads to diffu sion of lipids, protein s, rupt ured IAs. In pat ien ts previou sly t reated for an IA, th e risk
an d oth er m acrom olecules from th e circulat ion to th e IA w all.5 factors for the form ation of new IAs (de novo IAs) are sm oking,
Moreover, t h e aberran t flow con dit ion s m ay p redisp ose to lu m i- hypertension, and fem ale sex.8 It is likely th at these sam e risk fac-
nal th rom bosis, w hich is associated w ith IA w all degen eration and tors also predispose to IA form at ion in pat ien ts w ithout prior IAs.
rupture.3,5 Lum inal throm bus m ay im pair diffusion of oxygen and
nutrients to the m yointim a-like hyperplastic IA w all, and is also a
source of oxygen radicals and iron that cause cytotoxic oxidative
st ress. In addit ion , th e in t ralu m in al th rom bu s is a sou rce of pro-
■ Genetics
teases capable of degrading the extracellular m atrix of the IA wall.5 Th e role of gen es in th e p revalen ce or in ciden ce of a m u lt ifacto-
rial disease is m easu red by th e h erit abilit y of th e d isease, w h ich
can be described as h ow m u ch variat ion of a t rait (e.g., a disease)
w ith in a specific popu lat ion is du e to gen es rath er th an to th e
■ Relevant Anatomy environ m en t . Her it abilit y for m u lt ifactor ial d iseases an d d isor-
d ers is gen erally m easu red t h rough t h e cor relat ion s bet w een
Th e IAs are categorized , according to th eir an atom ic locat ion , as
relat ives, m ost effect ively u sing large t w in coh or t s.
an terior an d posterior circulat ion an eur ysm s. An terior circula-
Th ere are n o h erit abilit y st u dies on IAs, an d t h u s t h e con t ri-
t ion an eu r ysm s are located on th e in tern al carot id ar teries (ICAs)
bution of genetic factors to variations of the trait is unknow n. The
or on e of th eir term in al bran ch es, th e m iddle cerebral arteries
curren t belief am ong th e scien t ific an d clin ical com m un it ies is
(MCAs), or th e an terior cerebral ar teries (ACAs). Posterior circu-
that roughly 10%of all SAH cases are associated w ith a fam ily his-
lat ion an eu r ysm s origin ate from ver tebral ar teries, th e basilar
tor y.9 A disease m ay run in a fam ily due to gen etic or environm en -
ar ter y or on e of its term in al bran ch es, th e cerebellar ar teries, or
tal factors, or often both . Th e largest t w in st udy to date clearly
th e posterior cerebral ar teries (PCAs). Dist ribu t ion of IAs along
dem on st rates th at th e con cordan ce for SAH in t w in s is ext rem ely
th e differen t in t racran ial ar teries is u n equ al, so th at cer t ain ar-
low (1.2%).10 St at ist ical m odel fit t ing on th e basis of th ese few
teries an d th eir segm en t s are overrepresen ted, possibly due to
con cordan t pairs sh ow ed th at th e est im ated h erit abilit y is 41%,10
flow -related reason s (see Clin ical Presen t at ion , below ).
but th is est im ate is n ot ver y precise, because on ly six con cordan t
Th e IAs are t ypically located at th e branch ing sites of th e m ajor
t w in pairs for SAH were available for the statistical analysis. How -
in t racran ial ar teries su rrou n d ed by cistern s of th e subarach n oid
ever, th e h eritabilit y est im ate of 41%suggests th at th ere is on ly a
space. Th e cistern al space varies in size an d sh ape depen ding
m oderate role for gen et ic factors in th e et iology of SAH. An oth er
on t h e an atom ic locat ion an d in d ivid u al var iat ion . IAs fou n d in
large st udy also fou n d th at a fam ilial SAH is a ver y rare even t .11
n ar row cistern s ten d to be m ore em bedded in th e surroun ding
Even th ough th ese st u dies address SAH, n ot an eur ysm s, th ere are
brain .
n o epidem iologically valid st udies sh ow ing fam ilial aggregat ion
On e or m ore bran ch es u su ally origin ate from th e an eu r ysm
of an eu r ysm cases du e to gen et ic or environ m en tal factors.
base. Keep in g t h ese bran ch es p aten t is on e of t h e key goals in
Th ere are several p u blish ed rep or t s an d review s on t h e ge-
any an eu r ysm t reat m en t . Size, n u m ber, an d or ien t at ion of t h e
n et ics of fam ilial IAs.12 In terest ingly, a recen t st udy suggested a
bran ch es var y depen ding on th e an atom ic locat ion of th e an eu-
sh ared gen et ic backgroun d at 5q23.2 for IAs an d h igh blood pres-
r ysm as w ell as th e exact angioarch itect ure of th at part icular an -
su re,13 suggest ing th at at least som e of th e iden t ified gen et ic
eu r ysm . Apart from th e m ajor bran ch es, m any IAs are involved
varian ts m ay prim arily be associated w ith risk factors rath er
w ith sm all perforating arteries. Inadvertent occlusion of the sm all
th an w ith IAs. All associat ion an d lin kage st u dies sh ou ld also ad-
perforator(s) can cau se ver y severe n eu rologic deficits. Dep en d-
dress if th e varian t-associated risk varies sign ifican tly w ith es-
ing on the size and location of the IA, there m ay also be direct in -
tablished environ m en tal risk factors, such as hyper ten sion an d
volvem ent w ith the brainstem or other central neural structures.
sm oking.
In brief, genom e-w ide association st udies are designed to iden-
tify associat ion s, n ot causalit y, an d th ey can be con foun ded by
m any factors, such as fam ilial risk factors (un con t rolled in n early
■ Epidemiology all st udy design s). Curren t results on IA gen et ics do n ot provide
Th e IAs are rare in ch ildren an d you ng adu lt s, bu t th e prevalen ce th e n ecessar y an sw ers, an d m ore st rictly con t rolled, larger, an d
in creases sign ifican tly after 30 years of age.4 In a m et a-an alysis defin itive st udies are n eeded in th e fut ure.

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38 Intracranial Aneurysms 461

m un icat ing arter y (ACoA) or pericallosal arter y (see Clin ical Pre-
■ Diseases Associated w ith Aneurysms sen tat ion , below ).
Som e diseases are closely related to IA form at ion , su ch as au toso-
m al polycyst ic kidn ey disease an d fibrom u scular dysplasia.14 Th e Aneurysm Grow th and Risk of Rupture
m ech an ism of associat ion in eith er of th ese diseases is u n clear,
but th ese pat ien ts often h ave severe hyper ten sion . How ever, in Th e large size of an IA is a risk factor for ru pt u re, an d som e long-
patients w ith autosom al polycystic kidney diseases, th e defect ive term follow -up series even dem on st rate an in crease in th e an -
gen e produ ct th at causes th e disease is exp ressed directly in th e n ual risk of ru pt ure w ith an in crease in th e size of th e grow ing
sm ooth m uscle cells of th e cerebral ar teries. an eur ysm .16 IA size, th erefore, w ould seem as a good m arker for
Con n ect ive t issu e disorders th at w eaken th e cerebral arter y a r u pt u re-pron e IA, esp ecially becau se it is relat ively easily
w all h ave been th ough t to predispose to th e form at ion of IAs. m easu red. How ever, alth ough an eu r ysm size in creases th e ru p -
Becau se of th e relat ive rarit y of th ese d isorders an d th e fact th at t ure risk, it is n ot a ver y sen sit ive m arker for rupt u re-pron e IAs.
m ost u n r u pt u red IAs are asym ptom at ic an d requ ire im agin g Many of t h e r u pt u red IAs are sm all (see Clin ical Presen t at ion ,
st u d ies for d iagn osis, st ron g evid en ce for su ch associat ion s is below ). Moreover, th e lack of a clear associat ion bet w een IA size
lacking. Th ere is som e eviden ce th at th e collagen disorder Eh lers- an d w all st ruct ure m ean s th at IAs can h ave a degen erated an d
Dan los t yp e IV m igh t be associated w it h an eu r ysm al SAH.14 fragile r u pt ure-pron e w all irresp ect ive of t h eir size.3 So IA size
How ever, con t rar y to w h at w as p reviou sly th ough t , th e m ore alon e sh ould n ot be used as a m arker to exclu de u n rupt ured IAs
com m on Marfan syn drom e, w h ich cau ses defect ive elast ic fibers from t reat m en t .
in th e ar ter y w all an d p redisp oses to aort ic an eu r ysm s, is n ot
associated w ith IAs. Aneurysmal Subarachnoid Hemorrhage
Alth ough oth er m an ifest at ion s of vascular disease, such as
ath erosclerot ic lesion s or ext racran ial an eu r ysm s, are n ot clearly Th e in ciden ce of an eu r ysm al SAH varies. In m ost popu lat ion s th e
associated w ith IAs, pat ien ts w ith t reated IAs h ave a h igh er risk in ciden ce is reported to be 6 to 10 cases per 100,000 person -
of occlu sive vascular disease later in life. Th is associat ion m igh t years.17 For u n kn ow n reason s, in Fin lan d, Nor th ern Sw eden , an d
be related to risk factors com m on for both IAs an d ath erosclero- Jap an th e in ciden ce is m u ch h igh er, w ith 16 to 20 cases p er
sis, su ch as sm oking an d hyper ten sion . 100,000 person-years.2 These countries have various population-
based n at ion al h ealth care registers th at also in clude fatal SAH
cases. Th is is often n ot th e case for oth er cou n t ries an d m ay ex-
plain som e of th e differen ces. Th e in it ial h em orrh age cau ses th e
greatest m or talit y. Abou t 15% of SAH pat ien ts die before reach -
■ Natural History ing m edical at ten t ion .18 In th e h istoric an d un selected series by
Many IAs do n ot ru pt u re, as dem on st rated by th e p revalen ce of Pakarin en ,18 th e cum ulat ive m ortalit y w as 32% during th e first
u n rupt u red IAs in p rosp ect ive au top sy series (2–3.6%).7 Th ere day, 46% during th e first w eek, 56% du ring th e first m on th , an d
are n o p rosp ect ive follow -u p st u d ies to d eter m in e t h e r isk of 60% during th e first 6 m on th s. If th e an eur ysm is left un t reated,
r u pt u re of u n selected in cid en t al IAs, so all t h e est im ates on about on e-third of pat ien ts w h o recover from th e in it ial h em or-
r u pt ure risk for an IA are based on follow -up of eith er selected rh age die of rebleeding du ring th e first 6 m on th s. Delayed cere-
in ciden t al IAs or asym ptom at ic IAs in pat ien ts t reated for oth er bral vasosp asm is t h e secon d m ajor cau se of d eat h in p at ien t s
rupt ured an eur ysm s. A m et a-an alysis of th ese series foun d an su r vivin g t h e in it ial ict u s. Even w ith m od er n t reat m en t , case-
overall an n ual risk of rupt ure of 1.2% du ring 5-year follow -u p.15 fat alit y rates are st ill close to 50% at 1 m on th after SAH.1
How ever, m u lt iple factors affect th e n at u ral h istor y of an IA, an d
n eed to be con sidered w h en assessing th e risk of r upt u re.

■ Clinical Presentation
Patient-Related Risk Factors for IA Rupture Th e dat a p resen ted in th is an d th e n ext sect ion w ere obt ain ed
Older age, fem ale sex, sm oking, an d hyper ten sion in crease th e from th e Helsin ki Cerebral An eu r ysm Dat abase, w h ich con t ain s
risk of IA ru pt u re.9,15 Un r u pt ured IAs in pat ien ts w ith a previous in form at ion on all 4,257 pat ien t s w ith IAs w h o w ere adm it ted to
h istor y of an eur ysm al SAH h ave an in creased risk of rupt u re for th e Dep ar t m en t of Neu rosu rger y at Helsin ki Un iversit y Cen t ral
un kn ow n reason .15 Hosp it al bet w een 1980 an d 2008. Th is cen ter ser ves, w it h ou t
select ion , th e catch m en t area of south ern Fin lan d, w h ich h as a
pop u lat ion of 2 m illion . Of th e 4,257 pat ien ts, 3,062 (72%) pa-
Aneurysm-Related Risk Factors for t ien ts p resen ted w ith an eu r ysm al SAH an d r u pt u red an eu r ysm ,
an d 1,195 (28%) pat ien ts w ith un rupt u red an eu r ysm s on ly.
Aneurysm Rupture Am ong th e pat ien ts w ith rupt ured an eur ysm s in our series,
In follow -u p st u d ies of u n r u pt u red IAs, larger an eu r ysm size t h ere w as a clear p red om in an ce of w om en over m en (58% vs
in creases th e risk of r upt ure, as does locat ion in th e posterior 42%). Men ten d ed to p resen t w it h SAH at you n ger age t h an
circulat ion . Obser vat ion al st u dies dem on st rate th at th e irregular w om en , m ean age 49 years (range, 5–88 years) versu s 54 years
sh ap e of th e an eu r ysm dom e, as w ell as cer t ain dom e geom e- for w om en (range, 15–92 years).
tries, m ay be associated w ith rupture. Clin ical series, on the other Th e 4,257 p at ien t s h ad a tot al of 6,163 an eu r ysm s—3,062
h an d , suggest t h at th e d ist r ibu t ion of r u pt u red IAs also favors rupt ured an d 3,101 un rupt u red. Mu lt iple an eur ysm s w ere seen
som e locat ion s in th e an terior circu lat ion su ch as an terior com - in 30% of pat ien t s.

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462 V Cerebral and Spinal Aneurysms

Most of t h e an eu r ysm s w ere fou n d in t h e an ter ior circu la- Table 38.1 Size and Location of 6,163 Aneurysms Found in 4,257
t ion (89% of th e ru pt u red an d 90% of th e u n r u pt u red). Th e m ost Patients Admitted to the Department of Neurosurgery in Helsinki
com m on sites for r upt ured IAs w ere th e ACoA, 31%; th e m iddle Betw een 1989 and 2008
cerebral ar ter y bifurcat ion (MCAbif), 26%; an d th e in tern al ca- Ruptured Unruptured
rot id ar ter y at th e origin of th e posterior com m u n icat ing arter y
(ICA-PCoA), 13%. In th e posterior circulat ion , th e m ost frequen t N 3,062 3,101
locat ion w as th e basilar arter y bifu rcat ion (4%). For un rupt u red Location
an eur ysm s th e dist ribut ion w as differen t: ACoA, 10%; MCAbif, ICA 622 (20%) 741 (24%)
ICA-PCoA 396 (13%) 200 (6%)
30%; ICA-PCoA, 6%; an d basilar bifu rcat ion , 4% (Table 38.1).
ACoA 945 (31%) 318 (10%)
Th e m ajorit y of an eu r ysm s w ere sm aller th an 15 m m . For th e
MCA 1,020 (33%) 1,577 (51%)
rupt u red cases th e m edian size w as 8 m m (range, 1–70 m m ); for
MCA-MbifA 810 (26%) 917 (30%)
un r u pt ured cases th e m edian size w as 4 m m (range, 1–60 m m ).
DACA 143 (5%) 168 (5%)
Of th e rupt ured an eur ysm s, 37% w ere sm aller th an 7 m m an d
VBA 332 (11%) 297 (10%)
90% sm aller th an 15 m m . An eur ysm s sizes are represen ted in
VBA-Bas bif 127 (4%) 111 (4%)
Table 38.1) Size, median (range) 8 (1–70) 4 (1–60)
< 7 mm 1,123 (37%) 2,256 (74%)
7–14 mm 1,616 (53%) 609 (20%)
Aneurysm Rupture Patterns
15–24 m m 281 (9%) 103 (3%)
In an eur ysm al SAH, com puted tom ography (CT) can dem on - > 24 m m 42 (1%) 94 (3%)
st rate variou s ru pt u re p at tern s (Fig. 38.3). Differen t an eur ysm Abbreviations: ICA, internal carotid artery; ICA-PCoA, origin of posterior
locat ion s cau se differen t r u pt u re p at tern s dep en ding on th e size comm unicating artery; ACoA, anterior com m unicating artery; MCA, m iddle
of th e an eu r ysm , it s at tach m en t to th e surroun ding brain , an d cerebral artery; MbifA, middle cerebral artery bifurcation; DACA, distal anterior
th e w id th of t h e cistern al space in w h ich it resides. Frequ en cies cerebral artery; VBA, vertebrobasilar area (posterior circulation); Bas bif, basilar
artery bifurcation.
of th e differen t rupt u re pat tern s w ith respect to th e an eur ysm

a b

Fig. 38.3a–f Various findings in acute subarachnoid hem orrhage (SAH) on computed tom ography (CT) images. (a) Thin layer of blood (arrow) in sub-
arachnoid space only (Fisher t ype II). (b) Prom inent blood collection in subarachnoid space (Fisher t ype III).

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38 Intracranial Aneurysms 463

c d

e f

Fig. 38.3a–f (continued ) (c) Intracerebral hem atom a (ICH) related to rup- rysm (Fisher t ype IV). (e) Subdural hem atom a and ICH related to rupture of
ture of a right-sided m iddle cerebral artery (MCA) aneurysm . (d) Intraven- right-sided MCA aneurysm . (f) Acute hydrocephalus in a patient with an
tricular hem orrhage (IVH) related to rupture of a posterior circulation aneu- aneurysm al SAH.

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464 V Cerebral and Spinal Aneurysms

Table 38.2 Computed Tomography Findings in 3,062 Patients w ith Aneurysmal Subarachnoid Hemorrhage Based on the
Aneurysm Location

Aneurysm Location

ACoA ICA MCA DACA VBA

N 945 622 1,020 143 332


Subarachnoid blood only 487 (52%) 310 (50%) 415 (40%) 46 (32%) 120 (36%)
ICH 307 (32%) 126 (20%) 480 (47%) 84 (59%) 10 (3%)
ICH + IVH 204 (22%) 73 (12%) 158 (16%) 39 (27%) 7 (2%)
IVH 141 (15%) 60 (10%) 73 (7%) 27 (19%) 63 (19%)
Subdural hematom a 21 (2%) 20 (3%) 75 (7%) 11 (8%) 3 (1%)
Severe hydrocephalus 116 (12%) 49 (8%) 51 (5%) 21 (15%) 73 (22%)
Abbreviations: ACoA, anterior com m unicating artery; ICA, internal carotid artery; MCA, m iddle cerebral artery; DACA, distal anterior cerebral
artery; VBA, vertebrobasilar area; ICH, intracerebral hem atom a; IVH, intraventricular hemorrhage.

locat ion are sh ow n in Table 38.2. Th e m ost com m on is su barach - parable to th ose of digital su bt ract ion angiograp hy (DSA) in an -
n oid h em orrh age w ith blood in side th e subarach n oid space on ly eu r ysm s larger th an 2 m m 19 ; (4) it dem on st rates calcificat ion s in
(45%). Som e ru pt ured an eur ysm s are associated w ith in t racere- th e w alls of ar teries an d t h e an eu r ysm ; an d (5) it qu ickly recon -
bral h em atom a (ICH; 33%), in t raven t ricular h em orrh age (IVH; st r u ct s th ree-dim en sion al (3D) im ages t h at sh ow, for exam p le,
12%), a com bin at ion of ICH an d IVH (16%), an d subdu ral h em a- th e su rgeon’s view of th e IA. Som e IAs m ay be difficu lt to visu al-
tom a (4%). An ICH is m ost often seen in MCA an eur ysm s (47%) ize by rou t in e 3D CTA, u su ally du e to a ver y sm all size, so th at
an d p er icallosal an eu r ysm s (59%). An IVH is m ost frequ en t ly su bsequ en t rotat ion al 3D DSA is requ ired. In gian t an d fu siform
en cou n tered in p osterior circu lat ion an eu r ysm s an d pericallosal an eur ysm s, m agn et ic resonan ce im aging (MRI) w ith differen t
an eur ysm s. Subdural h em atom as are seen in up to 7% of ru p - sequ en ces, along w ith 3D CTA, h elps to dist inguish th e t r ue w all
t ured MCA an eur ysm s. Th e com bin at ion of ICH an d IVH predict s of th e an eu r ysm an d th e in tralum in al th rom bosis.
th e least favorable ou tcom e. Blood in th e su barach n oid cistern s
can resu lt in hydrocep h alu s. Severe preoperat ive hydroceph alu s
w as seen in 10% of our 3,062 patien ts (Table 38.2).
Th e r u pt u re p at ter n an d hyd rocep h alu s bot h affect t h e p a- ■ Treatment of Ruptured Aneurysms
t ien t s’ in it ial con d it ion . Table 38.3 sh ow s t h e in it ial con d it ion
based on the World Federation of Neurosurgical Societies (W FNS) Treat m en t of r u pt u red IAs h as th ree m ain goals: (1) to p reven t
scale w ith resp ect to th e an eu r ysm locat ion . In an eur ysm s often rebleeding; (2) to preven t delayed vasospasm ; an d (3) to m an age
associated w ith ICH (MCA an d pericallosal ar ter y), poor in it ial all th e addit ion al p roblem s cau sed by th e in it ial im pact of SAH.
grad e (W FNS 4 or 5) w as obser ved in 32% com p ared w it h 22%
of r upt ured ICA an d ACoA an eur ysm s. Posterior circulat ion pre-
sen ted m ost frequ en tly w ith IVH, w h ich also reflected on th e Prevention of Rebleeding
preop erat ive grade. Th e p eak in ciden ce of rebleeding occu rs du ring th e first 24
h ours, w h en th e risk is 4 to 7%.18 After th is t im e period, th e risk
rem ain s at 1 to 2% p er day for th e n ext 2 w eeks, an d for th e first
Imaging m on th th e cum ulat ive risk is 30 to 35%. About 60% of th e pa-
Mu lt islice h elical CT angiograp hy (CTA) h as becom e th e prim ar y t ien ts w h o h ave a rebleeding die.18 Th e best m eth od to preven t
m odalit y for im aging of IAs in m any cen ters. Th ere are several rebleeding is in ter ven t ion w ith eith er a m icron eurosu rgical or
reason s for th e popu larit y of th is im aging m odalit y: (1) it h as en dovascular approach. Early surgery com bin ed w ith nim odipin e
vir t u al in dep en den ce from th e h em odyn am ic sit uat ion ; (2) it is (calcium an t agon ist) t reat m en t h as been sh ow n to reduce both
n on invasive an d fast; (3) its sen sit ivit y an d specificit y are com - th e rebleed ing rate an d th e risk of vasosp asm .19 By preven t ing

Table 38.3 Initial Clinical Condition Based on the World Federation of Neurosurgical Societies (WFNS) Scale
of 3,062 Aneurysmal Subarachnoid Hemorrhage Patients Based on the Aneurysm Location

Aneurysm location

ACoA ICA MCA DACA VBA

N 945 622 1,020 143 332


Initial WFNS
I 561 (59%) 355 (57%) 460 (45%) 64 (45%) 160 (48%)
II 149 (15%) 107 (17%) 143 (14%) 23 (16%) 53 (16%)
III 20 (2%) 24 (4%) 97 (9%) 14 (10%) 7 (2%)
IV 98 (10%) 57 (9%) 138 (14%) 16 (12%) 38 (11%)
V 117 (12%) 79 (13%) 181 (18%) 26 (18%) 74 (22%)
Abbreviations: ACoA, anterior com m unicating artery; ICA, internal carotid artery; MCA, m iddle cerebral artery; DACA, distal anterior
cerebral artery; VBA, vertebrobasilar area.

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38 Intracranial Aneurysms 465

early rebleeds, early surger y both decreases th e m or t alit y rate GOS ≥ 4).23 It is even m ore difficult to com pare th e outcom es of
an d im proves th e qualit y of life of th e sur vivors.2 Early adm in is- su rgical t reat m en t in differen t pat ien t series, as th ere are m any
t rat ion of t ran exam ic acid m ay be of ben efit in p reven t ing re- factors causing select ion bias. Th ese in clude th e clin ical con di-
bleeding from a r u pt u red IA. t ion before t reat m en t , an eu r ysm locat ion , t im ing of t reat m en t ,
m et h od of ou tcom e evalu at ion , len gt h of follow -u p , an d p ro -
sp ect ive versu s ret rospect ive n at u re of th e data.
Cerebral Vasospasm
Cerebral vasosp asm is d efin ed as d elayed n ar row in g of in t ra-
Factors Predicting Outcome
cran ial arteries often associated w ith dim in ish ed perfusion in
th e territor y of th e affected ar ter y, u lt im ately leading to hypoxia. Factors th at are gen erally recogn ized to predict ou tcom e after
Angiograph ic vasospasm is detected in 50 to 75% of pat ien t s, SAH are n eurologic grade on adm ission , age, am oun t of blood on
w ith a t ypical on set of 3 to 5 days after SAH.20 With ou t t reat - th e p reop erat ive CT scan , ICH, IVH, an d an eu r ysm locat ion .24 Of
m en t , h alf of th ese p at ien t s develop clin ical sym ptom s of isch - th ese factors, th e n eu rologic grade on adm ission h as th e st ron -
em ic n eu rologic deficit s, an d som e even die. Com bin ed m or t al- gest effect on outcom e. In pat ien ts w ith an in it ial clin ical grade
it y an d m orbidit y associated w ith cerebral vasospasm is eviden t of IV or V, a favorable resu lt w as seen in on ly 30 to 50% irresp ec-
in 15% of SAH pat ien ts. So far, n o single t reat m en t to effect ively t ive of th e t reat m en t m eth od, w h ereas a good preop erat ive clin i-
preven t vasospasm h as been iden t ified. cal grad e (grad e I or II) p red icted a favorable resu lt in 80 to
90% of th e pat ien ts. Th e secon d m ost im port an t factor is age.24
Younger patients are m ore likely to tolerate system ic st ress caused
Additional Complications of by acu te SAH, an d th erefore recover bet ter th an th e elderly. Th ick
Subarachnoid Hemorrhage blood clots in basal cistern s (Fish er grade ≥ 3), a risk factor for
develop m en t of delayed vasosp asm , also p redict a less favorable
Ad d it ion al com p licat ion s related to acu te SAH in clu d e hyd ro -
outcom e.25 Neu rologic grade, age an d blood on a CT scan seem to
ceph alus, expan sive ICHs, hypon at rem ia, seizures, an d, less fre-
be m ore im p or tan t th an oth er factors in predict ing th e outcom e
qu en t ly, card iac ar rhyt h m ia, card iac dysfu n ct ion , m yocard ial
after SAH.24
inju r y, pu lm on ar y edem a, acu te lu ng injur y, ren al dysfu n ct ion ,
an d h epat ic dysfun ct ion .21 Th u s, SAH n ot on ly affect s th e brain
but also h as im p act on th e w h ole body. Long -Term Outcome After
Subarachnoid Hemorrhage
Aneurysm Treatment Modalities De Novo Aneurysms and Rebleeding
In t racran ial an eur ysm s can be occluded eith er by m icron euro- Th e risk of rebleeding from a t reated an eu r ysm is of m ajor con -
su rgical m ean s, u su ally by p lacing an an eu r ysm clip across th e cern during long-term follow -u p of pat ien t s w ith good recover y
an eur ysm n eck, or by en dovascu lar m ean s such as packing th e after an eur ysm al SAH. Mult iple an eur ysm s, usually presen t al-
an eur ysm dom e from in side w ith coils. At presen t , both tech - ready at th e first SAH or rarely developing later (de n ovo), are
n iques are rou t in ely u sed for th e t reat m en t of IAs. Select ion of detected in abou t on e-th ird of SAH p at ien t s. Th ey are con sidered
th e m ost ap propriate tech n iqu e is a m u lt ifactorial decision . An a- to be a p red isp osing factor for recu r ren t SAH, toget h er w it h
tom ic an d flow -related factors m ay favor eith er m eth od, as can sm oking and hypertension. The cum ulative rupt ure rate in creases
th e p at ien t’s age an d clin ical con dit ion . Fin an cial cost s also h ave w ith follow -up, an d th e relat ive risk com pared w ith th e gen eral
to be con sidered; in m any coun t ries en dovascu lar tech n iques populat ion is h igh er.
st ill rem ain s m ore exp en sive. Last bu t n ot least is th e exp erien ce De n ovo an eu r ysm s develop ed w ith an an n u al rate of 0.85%in
of th e team t reat ing th e pat ien t . Treat m en t results are m ore de- Fin n ish an d Japan ese follow -up st udies an d w ere m u ch h igh er
pen den t on th e overall experien ce of th e su rgical team th an on than the 0.26%rate for regrow th of com pletely clipped an eur ysm .8
th e m eth od u sed. An eu r ysm occlu sion is ju st on e par t of th e A st u dy from th e Net h erlan ds fou n d th e in ciden ce of recu rren t
t reat m en t p rocess. For ru pt u red an eu r ysm s, th e risk of rebleed- SAH after clip p ing of r u pt u red an eu r ysm s in a 10-year follow -u p
ing after t reat m en t is sm all (less th an 1% in m ean follow -u p of to be 3.2%, w ith 77%of th em due to de n ovo an eur ysm s.26 Un for-
9 years), w ith less risk in clip ped th an in coiled an eur ysm s.22 t u n ately, t h ere are n o p op u lat ion -based st u d ies on SAH w it h
m edian follow -u p t im es of 15 to 20 years. Th e p resen t th in king
is th at pat ien ts w ith m ult iple an eu r ysm s an d a h istor y of SAH
are at in creased risk of developing n ew an eu r ysm s in the long
■ Outcome of Ruptured Aneurysms run , but th ese an eur ysm s are likely to h ave th e sam e r upt ure risk
as oth er u n rupt u red an eur ysm s.
Treatment Outcome
Alt h ough t h e case-fat alit y rates of SAH h ave been d eclin ing
Long -Term Mortality
sligh tly over th e p ast th ree decades, th ey are st ill as h igh as 35 to
50%.2 Th e outcom e depen ds st rongly on th e adm ission policy of Relat ively lit tle is kn ow n abou t long-term su r vival after an eu r ys-
th e h osp it al an d esp ecially on th e p rop or t ion of p oor-grade p a- m al SAH. Most studies report a “long-term ” outcom e as being 6 or
t ien ts. In cen ters w ith act ive adm ission p olicy an d lit tle select ion 12 m on th s after SAH. Th ere are on ly a few populat ion -based SAH
bias so th at even poor-grade pat ien t s are t reated, 60 to 80% of st u dies w ith a m edian follow -u p of over 5 years. Th ese st u d ies
patients have a favorable outcom e (Glasgow Outcom e Scale score sh ow th at pat ien ts w ith previou sly t reated an eu r ysm al SAH h ave

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466 V Cerebral and Spinal Aneurysms

sign ifican t excess m ortalit y com pared w ith m atch ed gen eral pop - overrep resen ted in t h is an alysis, so t h at for m ost an eu r ysm s
ulation during long-term (> 5 years) follow -up.27 At least par t of th e r isk is p robably low er. Th e ISUIA rep or ted 1.5 to 2.3% m or-
th e excess m or talit y is probably exp lain ed by sh ared risk factors t alit y an d 10 to 12% m orbid it y in a p rosp ect ive follow -u p .28 It
for cardiovascular diseases, such as sm oking an d hyper ten sion . seem s t h at an ap p rop r iate r isk/ben efit an alysis requ ires t h or-
ough kn ow ledge of th e t reat m en t result s of th e par t icular cen ter.
Un like in ru pt ured an eur ysm s, w h ere th e in it ial im pact of SAH
st ron gly d eter m in es t h e m an agem en t ou tcom e, in u n r u pt u red
■ Unruptured Aneurysms an eu r ysm s it is th e exp er ien ce, kn ow ledge, an d skill of t h e
In th e m an agem en t of pat ien ts w ith un rupt ured IAs, th e risk of t reat ing p hysician an d team th at h ave th e m ain im p act on th e
t reat m en t h as to be w eigh ed again st th e risk of ru pt u re in differ- outcom e.
en t p op u lat ion s an d su bsequ en t com plicat ion s. Th e an n u al ru p - W hen considering prevent ive treat m ent, special em phasis has
t u re rate for u n ru pt u red an eu r ysm s h as been est im ated to be to be placed on th e safet y an d durabilit y of the treatm ent m ethod.
1%.7 Risk factors for an eu r ysm r u pt u re in clu d e fem ale gen d er, Regarding safet y, th ere are m any large series on un r upt ured an -
sm oking, older age, an d h igh blood pressu re. Of th ese, sm oking eu r ysm s t reated both w ith m icrosu rger y as w ell as en dovascu lar
seem s to h ave t h e h igh est at t r ibu t able r isk—alm ost 50%. Even coiling th at dem on st rate th e safet y of t h ese tech n iqu es. For du -
if th e p at ien t stop s sm oking, th e risk of SAH rem ain s h igh er th an rabilit y, th ere are far few er long-term dat a available, especially
in n on sm okers.9 Th e largest st u dy on u n ru pt u red an eu r ysm s, for en dovascular tech n iques. Som e repor ts foun d th at r upt ure of
th e In tern at ion al St u dy of Un r u pt u red In t racran ial An eu r ysm s previou sly clip p ed u n ru pt u red an eu r ysm is an ext rem ely rare
(ISUIA), iden t ified in th e m ult ivariate an alysis of its prospect ive even t w ith a m edian follow -u p of 10 years. For coiling, data are
coh or t on ly large an eu r ysm size an d p oster ior circu lat ion loca- scarce, an d th ere is lit tle kn ow ledge on w h at h ap pen s to previ-
t ion as p red ictors for r u pt u re.28 In a m et a-an alysis of su rgical ously coiled un rupt u red an eur ysm in th e long r un . It beh ooves
ser ies from 1970 to 1996, t h e m or t alit y an d m orbid it y rates re- all vascular pract it ion ers to base th eir t reat m en t decision s on
lated to t reat m en t of u n r u pt u red IAs w ere 2.6% an d 11%, re - th e n at u ral h istor y dat a as w ell as th eir exp erien ce an d com for t
sp ect ively,29 but gian t an d posterior circu lat ion an eu r ysm s w ere w ith variou s t reat m en t opt ion s.

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arachnoid hem orrhage visualized by com puterized tom ographic scanning. r u pt ured In t racran ial An eur ysm s Invest igators. Unrupt ured in t racran ial
Neurosurger y 1980;6:1–9 an eur ysm s: n at ural h istor y, clin ical outcom e, an d risks of surgical an d
26. Wer m er MJ, Greebe P, Algra A, Rin kel GJ. In cid en ce of recu r ren t su b - en dovascu lar t reat m en t . Lan cet 2003;362:103–110
arachn oid hem orrh age after clipping for ruptured in tracranial aneur ysm s. 29. Raaym akers TW, Rin kel GJ, Lim bu rg M, Algra A. Mor t alit y an d m orbidit y
St roke 2005;36:2394–2399 of surger y for un rupt ured in t racran ial an eur ysm s: a m et a-an alysis. St roke
27. Hu t t un en T, von u n d zu Fraun berg M, Frösen J, et al. Saccular in t racran ial 1998;29:1531–1538
an eu r ysm d isease: d ist r ibu t ion of site, size, an d age suggest s d ifferen t

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39 Subarachnoid Hemorrhage
Giuseppe Lanzino and Alejandro A. Rabinstein

th e sam e au th ors obser ved a sligh t decrease in t h e in ciden ce of


■ Definition SAH of 0.6% p er year 1 in th e m ost recen t decad e, reflect ing bet -
Th e term subarachnoid hem orrhage (SAH) refers to th e p resen ce ter con t rol of kn ow n risk factors for SAH such as sm oking an d
of blood in th e subarach n oid space. Tradit ion ally, SAH h as been hyper ten sion . Despite th is declin e, th e degree of reduct ion w as
classified as t rau m at ic or sp on t an eou s. Th e lat ter t yp e is often substan t ially less th an th e on e obser ved for st roke in gen eral.
but n ot alw ays related to rupt ure of an in t racran ial an eur ysm . Th e in ciden ce an d lifet im e risk of SAH in th e gen eral p op u la-
Th is ch apter discu sses th e gen eral ch aracterist ics of an eu r ysm al t ion is h igh ly variable based on th e p resen ce or absen ce of kn ow n
SAH (aSAH), an d review s n ew er an d em erging con cept s regard- risk factors.8 In a m odel th at con siders sex, age, fam ily h istor y of
ing less com m on form s of sp on t an eou s SAH, su ch as SAH in th e aSAH, sm oking, hyper ten sion , an d hyperch olesterolem ia, th e in -
con text of reversible vasocon st r ict ion syn d rom e an d n on an eu - ciden ce an d th e lifet im e risk of aSAH varies from 0.4/100,000 to
r ysm al SAH. 298/100,000 person -years an d lifet im e bet w een 0.2% an d 7.2%8
based on th e variou s com bin at ion s of, or lack of, th ese factors.
A season alit y in th e occurren ce of SAH h as been suggested by
several st u dies, an d a m eta-an alysis in deed fou n d th at aSAH oc-
cu rs m ore com m on ly in w in ter th an in su m m er an d stat ist ically
■ Incidence m ore com m on ly in th e m on th of Jan uar y th an in th e su m m er
Sp on t an eou s SAH accou n t s for on ly 5% of all st rokes. How ever, m on th s of Ju n e to Septem ber.9 Th e reason s for th is season alit y
as it affect s m any you n g p eop le in t h e m ost p rod u ct ive years of are un kn ow n because data on the in fluen ce of m eteorologic fac-
t h eir life, it accou n t s for a sign ifican t p rop or t ion of h ealth care tors on SAH are con flict ing.9
exp en dit u re for st roke in gen eral.
Th e overall in ciden ce of SAH is est im ated to be 9 per 100,000
person -years in pu blish ed st u dies.1 How ever, th is figu re sh ow s
w ide region al variabilit y.1 Th e h igh est in ciden ce is obser ved in
Jap an (22.7 p er 100,000 p erson -years) an d Fin lan d (19.7/100,000
■ Modifiable Risk Factors
person -years), w h ereas low er rates are n oted in Sou th Am erica Several longit u din al an d case-con t rol epidem iological st u dies
(4.2/100,000 person -years). The obser ved incidence in the United h ave invest igated th e poten t ial role of m odifiable risk factors on
St ates is 6.9 to 9.4 p er 100,000 p erson -years.2,3 Th e factors re- aSAH. Curren t an d form er sm oking h as a h igh prevalen ce in pa-
spon sible for such w ide region al variabilit y are m ostly specula- t ien ts w ith aSAH an d it is obser ved to accou n t for 45 to 75% of
t ive, as th e t ru e reason s are u n kn ow n .1 In addit ion to variat ion s affected pat ien t s in North Am erica an d Europe, w h ich is h igh er
in in ciden ce of an eur ysm al SAH across coun t ries w ith differen t th an th e 20 to 35%p revalen ce repor ted in th e gen eral adu lt p op -
racial an d et h n ic com p osit ion s, t h ere are d ifferen ces in in ci- u lat ion .10 Argu ably th e st rongest eviden ce for an im por tan t role
d en ce across racial/eth n ic groups w ith in th e Un ited States. Afri- for sm oking com es from the Helseundersøkelsen i Nord-Trøndelag
can Am erican s an d Hispan ics h ave a h igh er in ciden ce of aSAH (HUNT) st udy con du cted in Nor w ay,11 in w h ich subject s w ere
th an w h ite Am erican s.3–5 en rolled bet w een 1983 an d 1986 an d follow ed p rosp ect ively.
Th e m ean age of p at ien t s w it h aSAH in creased from 52 to For m er sm okers (h azard rat io [HR], 2.7) an d cu r ren t sm okers
62 years bet w een 1973 an d 2002,6 an d th is in crease w as seen (HR, 6.1) h ad a m uch h igh er risk for aSAH com pared w ith n ever
equ ally in m en an d w om en . W h en differen t age grou ps are re- sm okers.11 In a m eta-an alysis, cu rren t sm okers w ere foun d to
view ed, th e in ciden ce of SAH in creases w ith in creasing age, an d h ave a 2.2- to 3.1-fold in crease in th e risk of aSAH com pared w ith
overall th ere is a con sisten t predilect ion for w om en . How ever, n ever an d form er sm okers com bin ed.10 Th e risk in form er sm ok-
th e sex dist ribu t ion is also affected by age. Th e in cid en ce of SAH ers w as t w ice th e risk in n ever sm okers.10 Oth er st udies h ave
is h igh er in m en in th e 25- to 45-year age grou p, bu t is sign ifi- con firm ed t h at p reviou s sm oking is st ill associated w ith an in -
can tly h igh er in w om en in th e 55- to 85-year age group .1 creased risk of aSAH, alth ough n ot as m uch as th at seen in cur-
Several st udies have reported a consistent reduction in the in - ren t sm okers.12 Factors respon sible for th e in creased risk of aSAH
cidence of stroke of 2%per year in the past t w o decades. How ever, in sm okers are u n kn ow n . Nicot in e p er se m ay n ot be respon -
th e in ciden ce of SAH h as rem ain ed relat ively st able, alth ough a sible.12 No associat ion w ith in creased risk w as obser ved in users
progressive decrease h as been repor ted in recen t years. In 1996, of sm okeless tobacco, w h ich h as a m u ch h igh er con cen t rat ion of
Linn an d cow orkers,7 in a m eta-an alysis, fou n d th at th e overall n icot ine th an cigaret tes.
in ciden ce of SAH h ad rem ain ed st able over th e 35 years p reced - Systolic blood pressure is an oth er m odifiable risk factor th at
ing th eir review. How ever, in a su bsequ en t u p date of th eir w ork, h as been convin cingly sh ow n to be posit ively associated w ith an

468

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39 Subarachnoid Hemorrhage 469

in creased risk for aSAH.11 In th e HUNT st udy, su bjects w ith a sys- Occasion ally, an d esp ecially in th e case of th e n on an eu r ysm al
tolic blood pressure bet w een 130 an d 139 m m Hg h ad an in - perim esen ceph alic h em orrh age, p at ien ts m ay refer th e on set of
creased risk of aSAH (HR, 2.3) w h en com pared w ith th e referen ce h eadach e to th e occipital/upper n eck area. Alth ough severe, of
pop u lat ion (< 130 m m Hg systolic). Th e HR w as 3.3 in su bjects su dden on set , an d persisten t , th e ch aracterist ics of h eadach e in
w ith systolic blood pressure > 170 m m Hg at th e t im e of en roll- th e set t ing of SAH is variable, w h ich in som e cases can m ake th e
m en t in th e st u dy.11 diagn osis ch allenging, especially in pat ien ts evalu ated in a p ri-
Th e effect s of alcoh ol con su m pt ion on th e risk of aSAH are n ot m ar y care set t ing. Am ong pat ien ts evaluated in a gen eral clin ical
qu ite as w ell defin ed as th e in creased risk seen w ith sm oking pract ice set t ing, on ly 10% of th ose presen t ing w ith su dden , se-
an d hyper ten sion . Several coh or t an d case-con t rol st udies h ave vere h eadach e en d up h aving aSAH.20 In pat ien t s seen in a p ri-
suggested th at in creased alcoh ol con su m pt ion (> 150 m g/w eek) m ar y care set t ing, un aw aren ess of th e acute on set of h eadach e
m ay in crease th e risk of aSAH in depen den t of its associat ion on th e par t of th e prim ar y care physician , pat ien t’s prior h istor y
w ith sm oking an d hyper ten sion .13 of h eadach e, an d pat ien t’s delay in seeking m edical at ten t ion
Th e obser vat ion th at th e differen ce in t h e risk of aSAH be- w ere all factors th at in creased th e likelih ood of delay in referral
t w een m en an d w om en does n ot em erge u n t il th e age of 50 or for fur th er evalu at ion for aSAH.21 Som e pat ien ts m ay n ot seek
older h as t riggered research on th e possible role of h orm on al m edical at ten t ion at t h e on set of th e h eadach e, bu t m ay presen t
factors. Sm oking an d hyper ten sion , an d to a lesser exten t alcoh ol a few days later due to th e persisten ce of th eir sym ptom s or to
con su m pt ion , w h ich are th e m ost im p or t an t m odifiable risk fac- th e aggravat ion of sym ptom s related to hydrocep h alu s or vaso-
tors for aSAH, are m ore prevalen t in m en th an in w om en . Th u s, spasm . Pat ien t s presen t ing in a delayed fash ion are often dehy-
th e differen t dist ribu t ion of th ese risk factors does n ot explain drated, as th ey h ave been h om e in p ain , w ith lim ited oral inp u t
th e differen t sex d ist ribu t ion of an eu r ysm s an d aSAH after th e an d often suffering episodes of em esis. In th ese cases, prom pt
age of 50.14 A m et a-an alysis of p u blish ed st u d ies suggest s an hydrat ion alon e often ach ieves im provem en t of th e severit y of
in creased risk for aSAH am ong cu rren t oral con t racept ive u sers th e h eadach e.
an d an in creased risk for post m en opau sal as opposed to pre- Neck st iffn ess is often p resen t du e to m en ingeal irrit at ion , bu t
m en opausal w om en of th e sam e age.14 Moreover, it appears th at it m ay be absen t in p at ien t s w ith a sm all SAH.19 Neck st iffn ess
w om en w h o h ave u sed h or m on al rep lacem en t t h erapy h ave a m ay be absen t at th e on set an d m ay take 7 to 10 hours to m an i-
redu ced risk, w h ereas pregn an cy, deliver y, an d th e p uerperium fest. Nausea and vom iting are also com m only present in patients
do n ot seem to in crease th e risk of SAH. w ith aSAH, but m ay be absen t in pat ien ts w ith m ilder form s.
Associat ion w ith oth er risk factors is qu est ion able. Hyp erch o- Vom it ing is n ot a dist in ct ive feat ure because it can be presen t in
lesterolem ia an d diabetes m ay be associated w ith a decreased u p to 50% of pat ien t s presen t ing w ith th u n derclap h eadach e n ot
risk, bu t th e eviden ce is n ot st rong.10 In creased body m ass in dex associated w ith SAH.22
(BMI) has also been reported to be associated w ith reduced risk,15 Tran sien t loss of con sciou sn ess is com m on in pat ien ts w ith
w h ereas data are in con sisten t on th e role of lean body m ass an d aSAH an d is probably related to th e sudden rise in in t racran ial
vigorou s p hysical exercise.10 Recen tly, an associat ion bet w een pressu re, w h ich m ay app roach or equ al p erfu sion pressu re, re-
th e risk of aSAH an d decreased lung fun ct ion h as been suggested su lt ing in a t ran sien t (for su r viving pat ien ts) con dit ion of flow
in a p rosp ect ive coh or t st u dy.16 In su ch p at ien t s, th e p u t at ive arrest . Flow arrest is on e of th e m ech an ism s leading to arrest of
m ech an ism m ay be related to a com m on p ath ogen et ic m ech a- blood ext ravasat ion in su r vivors. In pat ien t s w ith sudden on set
n ism (involved in vessel w all degradat ion respon sible for an eu - of severe h eadach e, t ran sien t loss of con sciou sn ess in th e pres-
r ysm form at ion ) as w ell as degradat ion of lu ng paren chym a (re- en ce of SAH is th e h allm ark of an eu r ysm ru pt u re becau se loss of
spon sible for decreased resp irator y fu n ct ion ). con sciou sn ess is n ot seen in pat ien t s w ith n on an eu r ysm al SAH.23
Most risk factors seem to be m ore h azardou s in w om en , an d Tw o th irds of pat ien t s evalu ated on day 0 in th e In tern at ion al
th is m ay in part explain th e sex differen ces in aSAH.10 Th ere is St u dy on Tim ing of An eu r ysm Su rger y h ad som e d egree of d e-
in teract ion bet w een cu rren t sm oking an d risk of aSAH bet w een p ressed level of con sciou sn ess.24 Focal n eu rologic d eficit s are
th e sexes, w ith w om en at h igh er risk th an cu rren tly sm oking often present in patients w ith intraparenchym al hem atom as, but
m en .17 Th e join t effect of hyp er ten sion an d sm oking com bin ed th ey m ay also be p resen t in th e absen ce of in t raparen chym al
is h igh er th an th e sum of each factor, suggest ing an addit ive in - h em orrh age. In pat ien ts w ith out an in t raparen chym al h em or-
teract ion bet w een th e t w o.18 In a p rospect ive st u dy, th e HR for rhage, neurologic decline is probably related to the transient focal
aSAH w as 13.3 t im es h igh er for sm okers w ith hyper ten sion th an or diffuse spasm , w h ich occurs at th e t im e of th e rupt u re an d is
for su bjects w ith out th ese t w o factors.18 In terest ingly, n o in ter- on e of th e possible m ech an ism s leading to th e arrest of blood
act ion w as fou n d in t h is sam e st u dy bet w een hyp er ten sion or ext ravasat ion in su r viving p at ien ts. At yp ical presen t at ion s an d
sm oking an d alcoh ol con su m pt ion . m isdiagn oses in clu de hyper ten sive crisis w ith p sych osis du e to
the frequent association of dram atically in creased system ic blood
pressure, and, especially in unresponsive patients, m yocardial in -
farct ion w ith cardiac arrhyth m ia, given th e frequen t an d at t im es
dram at ic ch anges presen t on th e elect rocardiogram (ECG).
■ Clinical Presentation Early n eurologic deteriorat ion after adm ission to th e h ospital
Su dden on set of severe h eadach e, “th e w orst h eadach e of m y is n ot un com m on an d it is obser ved in up to 35% of p at ien t s.25
life,” is th e h allm ark of SAH in aw ake p at ien t s. More th an th e Factors predict ive of early n eu rologic deteriorat ion in clu de older
severit y of h eadach e, th e su dden on set is ver y im p or tan t an d is age, in creased clot bu rden , an d th e p resen ce of in t racran ial h em -
som et im es difficult to elicit by h istor y.19 Th e h eadach e is ch arac- orrh age on th e in it ial com puted tom ography (CT) scan .25 Early
terist ically diffuse an d u sually persist s for a few days after on set . n eu rologic deteriorat ion is associated w ith an in creased risk of

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470 V Cerebral and Spinal Aneurysms

com p licat ion s an d longer h osp it al st ays, an d is an in depen den t Table 39.1 Clinical Scales to Assess Severity of Presentation in
predictor of death . Aneurysmal Subarachnoid Hemorrhage

Grade Hunt and Hess Scale WFNS Scale

I Asymptomatic or m ild GCS sum score 15 without


■ Diagnosis headache hem iparesis
II Moderate to severe GCS sum score 13–14
A CT scan don e w ith in 6 h ours an d in terpreted by an experi- headache, nuchal rigidit y, without hemiparesis
en ced n eu rorad iologist h as a sen sit ivit y of vir t u ally 100% in no focal deficits other than
p at ien t s p resen t ing w it h acu te t yp ical h eadach e suggest ive of cranial nerve palsy
aSAH.26 In th ese p at ien t s, cerebrosp in al flu id (CSF) an alysis is n ot III Confusion, lethargy, or mild GCS sum score 13–14 with
required. Th e abilit y of CT scan to diagn ose aSAH is depen den t focal deficits other than hem iparesis
on th e t im e from th e in it ial even t , th e am oun t of blood, th e qual- cranial nerve palsy
it y of th e scan n er, an d th e abilit y of th e in terpret ing p hysician .19 IV Stupor or m oderate to severe GCS sum score 7–12 with or
If presen t , associated in t raparen chym al h em atom a h as a h igh er hem iparesis without hemiparesis
localizing value (for th e offen ding an eu r ysm ) th an th e dist ribu- V Coma, extensor posturing, GCS sum score 3–6 with or
t ion of cistern al blood.19 moribund appearance without hemiparesis
In p at ien t s w ith a n egat ive CT an d a st rong clin ical h istor y, or Abbreviations: WFNS, World Federation of Neurosurgical Societies; GCS, Glasgow
in th ose w ith at ypical presen tat ion , a lu m bar pu n ct u re sh ou ld Coma Scale.
be perform ed, especially if m ore th an 6 h ou rs h ave elapsed from
th e on set of h eadach e.26 Th e lu m bar p u n ct u re in th e set t ing of a
su spected SAH can be t ricky an d often difficu lt to in terpret du e
to dich otom ize eith er scale in to good grades (grades I to III) an d
to th e possibilit y of a t raum at ic tap. Th e presen ce of xan th och ro-
poor grades (grades IV an d V). Th is sim p le dist in ct ion , essen -
m ia (related to oxyh em oglobin degradat ion products an d in dica-
t ially based on th e level of con sciou sn ess at th e t im e of grading,
t ive of p reexist ing blood dist ingu ish able from th e “fresh ” blood
is usefu l in pract ice.
of a t raum at ic tap) is n ot eviden t un t il 6 to 12 h ours after th e
Alth ough th ere is con sen sus th at pat ien ts w ith an eur ysm al
h em orrh age. Collect ion of m ult iple sequen t ial t ubes of CSF an d
SAH sh ould be categorized early u sing on e of th ese t w o validated
evalu at ion of cell cou n t s, often suggested as a m ean s of d iffer-
clin ical scales, determ in ing th e best t im ing for clin ical grading
en t iat ing a t rau m at ic from a p osit ive t ap , is n ot alw ays reliable.
h as n ot received su fficien t at ten t ion . Most often , grading is per-
W h en a spin al t ap is p erform ed, it is im p or t an t to m easu re th e
form ed at th e t im e of th e first evalu at ion of th e pat ien t . Yet w h en
open ing pressure.19 An elevated open ing pressu re in a pat ien t
com paring grading up on presen t at ion versus grading at n adir or
w ith a sudden , severe h eadach e an d clear (on in spect ion ) CSF
after in it ial cerebral an d system ic resuscit at ion m easures, th e
can be suggest ive of du ral ven ou s th rom bosis or bacterial m en -
clin ical grade p ost resu scit at ion is th e m ost accu rate at predict-
ingit is, t w o life-th reaten ing con dit ion s th at m ay m im ic th e pre-
ing fu n ct ion al ou tcom e.32
sen tat ion of aSAH. On th e oth er h an d, a low p ressu re w ith clear
Evaluat ion of th e baselin e CT scan is u sefu l to est im ate th e
CSF m ay be in dicat ive of in t racran ial hyp oten sion , a con dit ion
risk of delayed vasosp asm an d cerebral isch em ia. For years, th e
th at occasion ally can m im ic SAH as w ell.19
m ost com m on ly used grading system w as th e on e developed by
Magn et ic reson an ce im aging (MRI) is im p ract ical in th e rou -
C.M. Fish er an d colleagu es in th e early days of CT scan n ing.33
t in e evalu at ion of p at ien t s w ith aSAH, an d in th e first few h ou rs
How ever, th is scale h as several lim it at ion s: it star t s from a grade
is n ot bet ter th an a rou t in e CT scan in detect ing it .27 In th e su b -
1 th at act ually represen ts th e absen ce of blood on th e CT scan , it
acute ph ase, on ce blood h as redist ributed an d m ay n ot be readily
is n ot lin ear (e.g., th e risk of vasosp asm in creases from grades 1
visible on CT, MRI is m ore sen sit ive, esp ecially if fluid-at ten u ated
to 3, but is low er w ith grade 4 th an w ith grade 3), an d, m ost im -
inversion recover y (FLAIR) an d T2* sequ en ces are obtain ed.28,29
por t an tly, it does n ot accoun t for th e addit ion al risk of delayed
Magn et ic reson an ce im aging can be h elp fu l in diagn osing rare
cerebral ischem ia associated w ith the presence of intraventricular
n on an eur ysm al cau ses of SAH in p at ien ts w ith a n egat ive cath e-
h em orrh age accom panying th e h em orrh age in th e subarach n oid
ter angiograp hy. How ever, th e rou t in e u se of MRI in p at ien ts
cistern s. Th e score described by Hijdra et al34 h as greater predic-
w ith n on an eur ysm al perim esen ceph alic h em orrh age is n ot in di-
t ive p ow er th an th e classic Fish er scale, bu t it is m ore laboriou s
cated, except in th ose p at ien t s in w h om th e on set of th e h ead-
an d st ill fails to accou n t for t h e ad dit ive effect of in t raven t r icu -
ach e m ay poin t to th e cer vical or th e th oracic spin e as a source of
lar h em orrh age on th e risk of delayed isch em ia. A m odificat ion
th eir SAH.
to th e classic Fish er scale h as been described, an d it h as quickly
gain ed accept an ce.35,36 Th is m odified Fish er scale star ts w ith a
grade 0 rep resen t ing th e absen ce of blood on th e CT scan ; th e
scale is lin ear (i.e., t h e h igh er t h e grad e, t h e h igh er t h e r isk of
■ Neurologic and Radiological Scales d elayed isch em ia) an d it in cor p orates t h e am ou n t of in t raven -
Th e severit y of n eu rologic im p airm en t u pon presen t at ion is on e t r icu lar h em or rh age in t h e est im at ion of isch em ic r isk (Table
of th e st rongest predictors of clin ical ou tcom e. Th e Hun t an d 39.2).
Hess 30 scale relies on su bject ive in form at ion , w h ich m ay com - Regardless of w h ich scale is u sed, on ly early CT scan s sh ou ld
prom ise its con sisten cy across exam in ers. Th u s, w e favor th e be u sed w h en d eterm in ing t h e rad iological grade. CT scan s p er-
sim p licit y an d object ivit y of th e World Federat ion of Neu rosu r- form ed m ore th an 48 hou rs after th e t im e of bleeding lose pre-
gical Societ ies (W FNS) grading scale (Table 39.1).31 It is com m on dict ive value.37

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39 Subarachnoid Hemorrhage 471

Table 39.2 Radiological Scales for the Estimation of Delayed Th e classic perim esen cephalic pat tern identifies a benign form
Ischemia in Aneurysmal Subarachnoid Hemorrhage of SAH con fin ed to th e perim esen ceph alic cistern , w ith th e epi-
cen ter of th e h em orrh age located in fron t of th e m idbrain (pre-
Grade Fisher Scale Modified Fisher Scale
truncal), w ithout hem orrhage in the interhem ispheric and lateral
0 No SAH or IVH sylvian fissu res, an d w ith m in im al or n o in t raven t ricu lar h em or-
1 No SAH or IVH Minimal/thin SAH, no IVH in rh age.39 Th is pat tern can be iden t ified w ith good in terobser ver
both lateral ventricles reliabilit y, but differen t obser vers do n ot alw ays agree.40 Th us, it
2 Diffuse, thin SAH, no clot Minimal/thin SAH with IVH is alw ays p r u d en t to p u rsu e vascu lar im aging even in pat ien t s
> 1 mm in thickness in both lateral ventricles
w it h a classic p er im esen cep h alic p at ter n of h em or rh age. Th e
3 Thick layer of SAH of Thick SAH, no IVH in both
cau se of t h ese p er im esen cep h alic h em or rh ages is n ot kn ow n ,
localized subarachnoid clot lateral ventricles
but a ven ous source h as been proposed.41 Th is hypoth esis w ou ld
> 1 mm in thickness
exp lain th e clin ical obser vat ion s th at th e h eadach e associated
4 Predominant IVH or Thick SAH with IVH in both
w ith perim esen ceph alic SAH ten ds to be less su dden th an w ith
intracerebral hemorrhage lateral ventricles
an eur ysm rupt ure an d n ot associated w ith loss of con scious-
without thick SAH
n ess.23 Acute com plications (hydrocephalus, vasospasm ) are rare,
Abbreviations: IVH, intraventricular hem orrhage; SAH, subarachnoid hemorrhage
progn osis is ver y favorable, an d recurren ces are except ion al.
Angiograph ically n egat ive, n on -perim esen ceph alic SAH cases
represent a diagn ostic ch allenge. Som e of th ese patients can pre-
■ Nonaneurysmal Subarachnoid sent w ith a fairly t ypical aneur ysm al pat tern. In these instances
repeat angiogram s are recom m en ded. Thanks to their im proving
Hemorrhage qu alit y, n on invasive an giogram s can som et im es be su fficien t
Th e d iagn ost ic evalu at ion , in clu d in g at least on e conven t ion al to detect th e source of h em orrh age.42 How ever, repeat ing th e
cat h eter an giogram , d oes n ot reveal a r u pt u red an eu r ysm in cath eter angiogram offers a bet ter yield an d is ju st ified w h en th e
15% of pat ien ts w ith acute n on t rau m at ic SAH, th ough est im ates cau se of th e SAH rem ain s un cer tain .43–46 Even a th ird angiogram
var y w idely across series.38 Several radiological pat tern s of an - m ay be n ecessar y to d etect t h e cu lp rit vascu lar an om aly.47
giograph ically n egat ive SAH h ave been recogn ized: a perim esen - Th ree-dim en sion al angiograp hy can be p ar t icu larly u sefu l to
ceph alic pat tern (Fig. 39.1), a n on -p erim esen ceph alic (an eu r ys- iden t ify sm all arterial abn orm alit ies, su ch as blister an eur ysm s.
m al) pat tern w ith or w ith out in t raven t ricular h em orrh age, an d a Pat ien ts w ith angiograph ically n egat ive n on -perim esen ceph alic
convexit y (or sulcal) p at tern . SAH are at risk of hydrocep h alu s an d delayed isch em ia du ring

Fig. 39.1 A patient with sudden onset of occipital head-


ache that rapidly became holocephalic. Computed tomog-
raphy (CT) of the head shows subarachnoid blood centered
in the prepontine cistern with m inim al extension in other
cisterns. This pat tern is strongly suggestive of a nonaneu-
rysm al, pretruncal/perim esencephalic hem orrhage.

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472 V Cerebral and Spinal Aneurysms

th e acu te p h ase.38 Th eir progn osis is bet ter th an in an eu r ysm al Because sm oking an d hyp erten sion are m ore prevalen t in pa-
SAH an d recover y is gen erally favorable, but n eurologic sequelae t ien ts w ith aSAH th an in age- an d sex-m atch ed con t rols, p at ien ts
can occur.48 w ho sur vive an aSAH h ave a decreased life expect an cy 57 ; th ose
Convexit y SAH is ch aracterized by bleeding rest ricted to th e w h o sur vive at least 1 year h ave alm ost a t w ofold in crease in th e
su lci in th e convexit y of th e cerebral h em isp h eres, t ypically on risk of dying com p ared w ith th e m atch ed gen eral p op u lat ion .58
on e side. Traum a sh ould alw ays be carefully exclu ded in th ese Th e risk is p rim arily related to a h igh er in ciden ce of fat al cere-
cases. Non t rau m at ic cases are m ost often related to reversible brovascular disorders (ICH an d isch em ic in farct ion ) in su r vivors
cerebral vasocon st rict ion syn drom e in younger pat ien ts an d ce- of aSAH.58 Sim ilarly, in th e In tern at ion al Subarach n oid An eu-
rebral am yloid angiopathy in older patients.49 Mycot ic aneur ysm s r ysm Trial (ISAT), th ere w as an un expected h igh er m ort alit y rate
an d in fect ive vasculit is are m uch less com m on , but sh ou ld be in pat ien t s w h o h ad u n dergon e surgical t reat m en t bu t n ot en do-
con sidered in th e righ t clin ical scen ario. Prim ar y cerebral vascu - vascu lar t reat m en t at m idterm follow -u p.59
litis is an except ion al cau se of convexit y SAH; w h en arterial ir- Th e old n ot ion t h at “fixing” th e an eu r ysm resu lted in resolu -
regularit ies are foun d in th ese pat ien ts, th e m ost likely diagn osis t ion of th e disease in a p at ien t w ith aSAH h as been overr u led by
is reversible cerebral vasocon st rict ion syn drom e. th e recen t con cept of an eu r ysm s an d SAH as ch ron ic diseases.56
Pat ien ts w ith aSAH are at risk for a n ew aSAH. Th is risk in on e
st u dy w as fou n d to be 15-fold h igh er th an in age-m atch ed con -
t rols.60 Late recurren t aSAH in th ese pat ien t s origin ates from in -
■ Aneurysmal Subarachnoid com pletely closed aneur ysm s (Figs. 39.2 and 39.3), n ew ly form ed
an eur ysm s (Fig. 39.4), or regrow th of previously closed an eu-
Hemorrhage r ysm s. Younger age, cu rren t sm oking, fam ily h istor y of aSAH,
Dat a on th e overall n at u ral h istor y of aSAH are based on older an d m ult iple an eu r ysm s at first aSAH seem to be associated w ith
studies. In contem porar y series, m ost patients considered to have an in creased risk of recu rren t aSAH.61 Th e frequen cy an d in ter val
a ch an ce of sur vival an d recover y h ave un dergon e t reat m en t of of follow -up im aging in pat ien t s w ith t reated r upt ured an eu -
t h e offen d in g an eu r ysm . In u n t reated p at ien t s w it h r u pt u red r ysm s rem ain s a m at ter of debate.56
an eur ysm , about a th ird w ill su ccu m b to rebleeding w ith in 6
m on th s after SAH.50 Th e cu m u lat ive risk of rebleeding after aSAH
is 50% at 6 m on th s. After 6 m on th s, th e in ciden ce of rebleeding
drop s to 3% per year.
Overall, 1-m onth case-fatalit y rates after aSAH have decreased
by 0.6% per year or 18% over th e 30-year in ter val span n ing from
1973 to 2002.6 Sim ilarly to th e in ciden ce of SAH, repor ted case-
fat alit y rates sh ow w ide region al variabilit y, ranging from 44.4%
in Eu rop e (exclu d ing Fin lan d an d n or t h Sw ed en ), to 42.9% in
Fin lan d an d n or th Sw eden , 35.8% in Asia exclu ding Japan , 26.7%
in Jap an , an d 32.2% in th e Un ited St ates.6 Ap p roxim ately 8 to
12% of pat ien t s die before arriving at th e h ospit al.6,51 Th e ch an ce
of a pat ien t sur viving an aSAH h as in creased to 65%.6,52,53 In a
st u dy en com passing th e in ter val bet w een 1997 an d 2008 in th e
Neth erlan ds, of 11,263 p at ien t s adm it ted w ith a diagn osis of
n on t raum at ic SAH, 6,999 (62%) pat ien ts sur vived m ore than 3
m on t h s.54 In a sim ilar st u dy bet w een 1987 an d 2003 in Sw e-
d en , of 17,705 pat ien ts w ith SAH, 11,374 (64%) sur vived at least
3 m on th s.55
Neu rologic con dit ion is th e m ost im p or t an t p redictor of fin al
outcom e.6 A recen t st u dy h as sh ow n th at th e assessm en t of pa-
t ien t con d it ion after n eu rologic an d system ic st abilizat ion is a
m u ch m ore im p or t an t p rogn ost icator th an t h e n eu rologic con -
d it ion upon arrival at th e h ospit al. Th is is especially t r ue w h en
con fou n ding factors, an d in par t icu lar th e effect s of in creased
in t racran ial p ressu re, m ay be p resen t .32 Alth ough ver y few p op -
ulat ion -based st udies h ave looked at overall fu n ct ion al outcom e,
it is est im ated t h at 35 to 55% of su r vivors of aSAH can ach ieve a
an accept able good fun ct ion al outcom e (m odified Ran kin Scale
Fig. 39.2a–c Delayed rehem orrhage from an incompletely treated aneu-
score of 0–3) at follow -u p.6 Pat ien ts w h o sur vive aSAH w ith ou t
rysm . (a) This 71-year-old wom an with a history of sm oking, fam ily history
residu al physical deficits often su ffer from cogn it ive dysfu n ct ion of aneurysm al subarachnoid hem orrhage (SAH), and poor pulm onary func-
an d m ood disorders, w h ich greatly affect th eir overall qualit y of tion requiring chronic oxygen therapy presented with a decreased level of
life.56 consciousness and diffuse high-grade SAH.
(text cont inues on page 476)

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39 Subarachnoid Hemorrhage 473

b c

Fig. 39.2a–c (continued ) (b) Catheter angiography reveals a complex bolization was perform ed. To m inim ize the danger of comprom ising the
broad-based internal carotid artery (ICA) aneurysm proxim al to a fetal pos- dom inant PCoA while achieving som e degree of protection against re-
terior com m unicating artery (PCoA). Given the patient’s poor neurologic bleeding, the aneurysm was loosely coiled. (c) 3D angiographic reconstruc-
condition, advanced age, and pulm onary comprom ise, endovascular em - tion dem onstrates the final coiled m ass.

a b

Fig. 39.3a–f After ventriculoperitoneal (VP) shunting, the patient in Fig. but given the risks no further treatm ent was recom m ended. (b) Eight
39.2 m ade a good recovery. (a) Follow-up angiography 4 m onths later m onths after the original bleed, she suffered a recurrent hem orrhage with
showed stable appearance of the incompletely treated aneurysm . Origi- intraventricular extension. (continued on page 474)
nally, the patient was considered for pipeline em bolization of the residual,

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474 V Cerebral and Spinal Aneurysms

c d

e f

Fig. 39.3a–f (continued ) (c) Catheter angiography showed further growth recoiling and m ade a full recovery. (f) The follow-up head CT after shunt
of the residual aneurysm (arrows), with very slow empt ying of the distal revision dem onstrates no evidence of ischem ic lesions. The patient is now
“pseudoaneurysm al” site of rupture (d, arrowheads). (e) She underwent in the process of being considered for placem ent of a flow diverter.

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39 Subarachnoid Hemorrhage 475

a b

c d

Fig. 39.4a–d Recurrent SAH from de novo aneurysm formation, 13 years ography showed a de novo ACoA aneurysm adjacent to the previously
after prior aSAH. This 68-year-old patient presented in 1999 with an aneu- coiled one. The aneurysm was treated with surgical clipping. At surgery, a
rysm al SAH (aSAH) from a ruptured anterior comm unicating artery (ACoA) new aneurysm completely separated from the previous one and arising
aneurysm. The patient underwent coil embolization and made a full recovery. from the opposite ACoA wall was identified and treated. ICA, internal ca-
(a) Follow-up catheter angiography 4 years later showed adequate obliter- rotid artery. (d) Postoperative catheter angiography confirm ed obliteration
ation of the aneurysm , which was again confirm ed by a follow-up m agnetic of the aneurysm with a very sm all neck rem nant at the site of t wo sm all
resonance angiography 8 years after coiling. (b) The patient represented AcoA perforating vessels.
13 years after the original bleed with a recurrent aSAH. (c) Catheter angi-

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476 V Cerebral and Spinal Aneurysms

rad iological scales h ave been p rop osed for t h e evalu at ion of
■ Conclusion p at ien t s w it h aSAH. Scales t h at are easy to rem em ber are n ot
An eur ysm al SAH accoun ts for 5% of all st rokes. Th e overall in ci- too com plicated to apply in rou t in e clin ical pract ice, an d th ose
den ce is 9 per 100,000, alth ough it h as h igh region al variabilit y. w ith a reason able in terobser ver reliabilit y an d progn ost ic sig-
Sm oking an d hyper ten sion are w ell-est ablish ed m odifiable risk n ifican ce are th e on es m ost u sed. Non an eur ysm al SAH is n ow a
factors for an eur ysm form at ion an d r upt ure. Th e role of oth er w ell-establish ed clin ical con dit ion diagn osed in up to 15% of pa-
m odifiable risk factors is n ot w ell est ablish ed. Sudden on set of t ien ts presen t ing w ith SAH. Due to im p roved n eu rocrit ical m an -
h eadach e is th e clin ical “h allm ark” of aSAH, an d clin ical presen - agem en t an d develop m en t of m in im ally invasive en dovascu lar
tat ion varies in relat ion to th e am oun t of ext ravasated blood an d tech n iques, th e progn osis of pat ien t s w ith aSAH h as im proved
degree of in creased in t racran ial p ressu re. Modern h ead CT is over th e past few decades. Case-fatalit y rates h ave sh ow n con sis-
ver y sen sit ive to th e presen ce of subarach n oid blood, especially ten t decrease over t im e. Despite th ese im provem en ts, a sign ifi-
if p er for m ed w it h in 6 h ou rs of clin ical on set . Lu m bar p u n ct u re can t p rop or t ion of pat ien t s su r viving th e acu te bleed are left
is st ill n ecessar y in a ver y sm all subset of pat ien t s w h o com e to w ith cogn it ive dist urban ces th at affect th eir qu alit y of life.
m ed ical at ten t ion in a d elayed fash ion . Var iou s n eu rologic an d

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of angiograph ic vasospasm after an eur ysm al subarach n oid h em orrh age: rology 2010;74:1494–1501
value of the Hijdra sum scoring system . Neurocrit Care 2009;11:172–176 54. Nieuw kam p DJ, Vaar tjes I, Algra A, Rin kel GJ, Bot s ML. Risk of cardiovascu-
38. Kim YW, Law son MF, Hoh BL. Non an eur ysm al subarach n oid h em orrh age: lar even t s an d death in th e life after an eu r ysm al su barach n oid h aem or-
an u p date. Cu rr Ath eroscler Rep 2012;14:328–334 rh age: a n at ionw ide st udy. In t J St roke 2012
39. van Gijn J, van Dongen KJ, Verm eu len M, Hijdra A. Perim esen cephalic 55. Nieuw kam p DJ, Algra A, Blom qvist P, et al. Excess m or t alit y an d cardio-
hem orrh age: a n on an eur ysm al an d ben ign form of su barach n oid h em or- vascular events in patients sur viving subarachnoid hem orrhage: a nation-
rh age. Neu rology 1985;35:493–497 w ide st udy in Sw eden . St roke 2011;42:902–907
40. Brinjikji W, Kallm es DF, W h ite JB, Lan zin o G, Morris JM, Cloft HJ. In ter- 56. Rin kel GJ, Algra A. Long-term outcom es of pat ien t s w ith an eu r ysm al sub -
an d in t raobser ver agreem ent in CT ch aracterizat ion of n on an eur ysm al arach n oid h aem orrh age. Lan cet Neu rol 2011;10:349–356
p er im esen cep h alic su barach n oid h em or rh age. AJNR Am J Neu rorad iol 57. Ron kain en A, Niskan en M, Rin n e J, Koivisto T, Hern esn iem i J, Vapalah t i M.
2010;31:1103–1105 Eviden ce for excess long-term m or t alit y after t reated subarachn oid h em -
41. van der Sch aaf IC, Velth uis BK, Gouw A, Rin kel GJ. Ven ous drain age in orrh age. St roke 2001;32:2850–2853
perim esen ceph alic h em orrh age. St roke 2004;35:1614–1618 58. Korja M, Silven toin en K, Laat ikain en T, Jousilah t i P, Salom aa V, Kaprio J.
42. Delgado Alm an doz JE, Jagadeesan BD, Refai D, et al. Diagn ost ic yield of Cause-specific m ortalit y of 1-year sur vivors of subarachnoid hem orrhage.
com puted tom ography angiography an d m agnetic resonan ce angiography Neurology 2013;80:481–486
in patients w ith catheter angiography-negative subarachnoid hem orrhage. 59. Molyn eu x AJ, Kerr RS, Birks J, et al; ISAT Collaborators. Risk of recu rren t
J Neu rosu rg 2012;117:309–315 subarachn oid h aem orrh age, death , or depen dence and st an dardised m or-
43. Topcuoglu MA, Ogilvy CS, Car ter BS, Buon an n o FS, Koroshet z W J, Singhal t alit y rat ios after clipping or coiling of an in t racran ial an eur ysm in th e
AB. Su barach n oid h em orrh age w ith out eviden t cau se on in it ial angiogra- In tern at ion al Su barach n oid An eu r ysm Trial (ISAT): long-term follow -u p.
phy st udies: diagn ost ic yield of subsequen t angiography an d oth er n euro- Lan cet Neu rol 2009;8:427–433
im aging test s. J Neurosu rg 2003;98:1235–1240 60. Ep idem iology of an eu r ysm al su barach n oid h em orrh age in Au st ralia an d
44. Ju ng JY, Kim YB, Lee JW, Hu h SK, Lee KC. Sp on t an eou s su barach n oid New Zealan d: in ciden ce an d case fat alit y from th e Au st ralasian Coopera-
h aem orrh age w ith n egat ive in it ial angiography: a review of 143 cases. t ive Research on Su barach n oid Hem orrh age St udy (ACROSS). St roke 2000;
J Clin Neu rosci 2006;13:1011–1017 31:1843–1850
45. An daluz N, Zuccarello M. Yield of fu r ther diagn ost ic w ork-up of cr ypto- 61. Werm er MJ, Greebe P, Algra A, Rin kel GJ. In ciden ce of recurren t su barach -
gen ic subarach noid h em orrh age based on bleeding pat tern s on com puted noid h em orrhage after clipping for rupt ured in tracranial an eur ysm s. St roke
tom ograp h ic scan s. Neu rosu rger y 2008;62:1040–1046, discu ssion 1047 2005;36:2394–2399

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40 Cerebral Vasospasm and Delayed
Ischemic Complications Associated
w ith Subarachnoid Hemorrhage
Guarav Gupta and E. Sander Connolly

vasospasm in du ced by w h ole blood is greater th an th at in duced


■ Pathophysiology and Natural History by free h em oglobin .7 Furth erm ore, disrupt ion s in calciu m an d
of Disease m agn esiu m cycling, dysregulated product ion of n it ric oxide, an d
path w ays involving arach id on ic acid m et abolites, free radicals,
Desp ite th e em ergen ce of en dovascu lar tech n iqu es an d advan ces
seroton in , aden osin e, an d bilir u bin oxidat ion prod u ct s h ave all
in n eu rocr it ical care, t h e n at u ral h istor y of an eu r ysm al su b -
been im p licated in t h e cascad e p reced ing t h e on set of vessel
arach n oid h em or rh age (SAH) rem ain s p oor, w it h 25 to 35%
sp asm .8–11 Th e im p or t an ce of t h e en d oth elin A p at h w ay h as
m or talit y on average, an d u p to 67% m or talit y in som e series.1,2
been w ell described in th e path ogen esis of large arter y vaso-
Advan ces in t reat m en t paradigm s h ave led to im provem en t in
spasm ,12 an d accordingly en doth elin h as long been a path w ay of
outcom es over th e past th ree decades; popu lat ion -based st udies
therapeut ic interest . At th e genetic level, upregulation of th e rho-
d em on st rate t h at in com p ar ison w it h 25 years ago, p at ien t s
kin ase p ath w ay, an d it s in teract ion w ith protein kin ase C-delt a,
experien ce a sh orter m edian delay to in ter ven t ion al t reat m en t ,
appears to be im por tan t in th e on set of vasospasm in experi-
w h ich h as con t ribu ted to a 50% redu ct ion in case fatalit y rates.
m en t al preparat ion s.13
Post-SAH vasosp asm , defin ed as th e n arrow ing of large- an d
Many of th ese path w ays h ave been st u d ied for th e develop -
m ediu m -caliber cerebral vessels during postbleed days 4 to 10,
m en t of targeted th erapies, eith er via select ively design ed ph ar-
rem ain s a sign ifican t con t ribu tor to poor ou tcom e. Alth ough in -
m aceu t icals or ap p licat ion s of exist in g d r ugs. From a clin ical
sigh t in to th e sign ifican ce of vasosp asm h as in creased, n o good
p erspect ive, m any h ave n oted th at th e am ou n t of subarach n oid
dat a exist to prove th at th e in ciden ce or sequ elae of vasospasm
blood, as quan t ified on im aging, correlates w ith th e risk of vaso-
h ave decreased. Cerebral vasospasm occurs in 45% of pat ien ts
spasm . Treatm ent efforts have also centered on clearance of blood
w ith an eur ysm al SAH, an d angiograph ically con firm ed vaso-
from th e su barach n oid space. Clin ically th ere is also an im p or-
sp asm is st rongly associated w it h st roke an d d eat h follow ing
tant divide bet w een system ic and local therapies. Local therapies,
SAH.3 Alt h ough it is n ow ap p aren t t h at cerebral vasosp asm is
alth ough occasion ally dem on st rat ing m ore im m ediate efficacy,
n ot th e sole cau se of isch em ic inju r y an d in farct in SAH p at ien t s,
in t rodu ce th e possibilit y of in fect ion an d also com e laden w ith
preven t ion an d t reat m en t of vasosp asm presen ts a sign ifican t
th e risks related to su rgical or bedside access to th e cistern al
opport un it y for im proving th e n at ural h istor y of an eur ysm al
sp aces. A “fin al com m on path w ay” h as th u s far eluded scien t ist s
SAH. To th is en d, th ere h as been a substan t ial effor t tow ard u n -
in th e laborator y an d p hysician s at th e bedside. Accordingly, clin -
derstan ding th e cellu lar level even ts th at u n derlie th e on set an d
ical t rials of m on oth erapies t arget ing in dividu al m olecu lar p ath -
determ in e th e severit y of vasosp asm . Th ese h ave form ed th e
w ays h ave gen erally p roduced disappoin t ing result s.
basis for th e developm en t of targeted th erapies, m any of w h ich
h ave sh ow n sign ifican t prom ise in early ph ase test ing, on ly to
flounder in a large-scale, random ized controlled trial (RCT). These Delayed Ischemic Complications
failu res u n d erscore t h e ch allen ges n eu rosu rgeon s an d n eu ro - Are Multifactorial
in ten sivists face in t reat ing cerebral vasospasm .
Delayed isch em ic com p licat ion s, defin ed as alterat ion s in th e
level of arou sal or n ew focal n eu rologic d eficit s, t ypically occu r
du ring p ostbleed days 3 to 14, an d are w idely accepted to be
Molecular Pathw ays in Cerebral Vasospasm m ultifactorial in origin . Im portan t con t ributors to delayed isch -
Post-SAH vasospasm is a ph en om en on ch aracterized by both re- em ic com plications include form ation of m icrothrom bi,14 cortical
versible vasocon st rict ion as w ell as failure of cerebral vascu lar spreading depolarizat ion ,15 dist al sm all ar ter y vasospasm (ver-
autoregu lat ion .4 Th e pat tern of vessel con st rict ion often involves sus large an d m edium ar ter y spasm ), an d in flam m at ion .16
p roxim al vessels at th e base of t h e brain in t h e circle of W illis. Th e possibilit y of m icroth rom bi leading to delayed isch em ic
A w ide array of cellular an d m olecular m ediators seem s to be com plicat ion s arose from obser vat ion s th at seru m levels of co-
dysregulated in th e cascade preceding th e on set of vasospasm . agulat ion m arkers seem to correlate w ith th e develop m en t of
Th e p rocess is th ough t to be t riggered in it ially by th e breakdow n delayed isch em ic com plicat ion s an d cerebral in farcts in th e p ost-
prod u ct s of blood in th e cistern s; th ere is con siderable eviden ce SAH p opu lat ion .17 Th ese m arkers in cluded β-th rom boglobulin ,
th at oxyh em oglobin is a m ajor in cit ing agen t in t h e cascade lead- th rom boxan e B2 , an d p latelet-act ivat ing factor.18 From th ese an d
ing to vessel spasm .5,6 Th is con clu sion is su pp or ted by dat a sug- oth er st udies, it seem s readily app aren t th at th e coagulat ion cas-
gest ing th at er yth rocytes are th e crit ical com pon en t of blood for cad e is act ivated in t h e first 2 to 4 days after ict u s. Th is t im e
th e in du ct ion of vasosp asm after exp erim en t al SAH. It h as also cou rse im p lies t h at elevat ion of t h ese m arkers can also be u sed
been dem on st rated that in experim en tal m odels, th e severit y of as early predictors of delayed isch em ic com plicat ion s an d u lt i-

478

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40 Cerebral Vasospasm and Delayed Ischemic Complications 479

m ately p oor ou tcom e, alt h ough t h ere are n o rep or t s of th is In flam m at ion appears to play a role in th e on set of cerebral
st rategy being applied clin ically. More directly, Giller et al19 vasospasm . Du m on t et al26 h ave dem on st rated th at th ere is a
dem on st rated th at m icroem boli cou ld be detected on t ran scra- rapid up regu lat ion of in flam m at ion -related gen es in spast ic ar-
n ial Dopp ler (TCD) evalu at ion . In th eir in it ial st u dy, m icroem boli teries. Markers of in flam m at ion su ch as adh esion m olecules an d
w ere obser ved in 4% of pat ien ts w h o un der w en t rou t in e TCD com plem en t cascade p rotein s are n ot on ly presen t in t h e cere-
m on itoring; h ow ever, 82% of SAH pat ien ts w ith obser ved m icro- brospin al fluid an d serum of post-SAH pat ien ts bu t also appear
em boli develop ed hypod en sit y on com p u ted tom ograp hy (CT) to correlate w ith fun ct ion al outcom e after an eur ysm al SAH.27 To
correlat ing w ith cerebral in farct , com p ared w ith ju st 24%of con - th is en d, com plem en t in h ibit ion is an em erging t reat m en t para-
t rol p at ien t s. Rom an o et al20 fu r th er sh ow ed th at m icroem bolic digm for post-SAH vasospasm .
ph en om en on w ere detectable in u p to 70% of p at ien ts, an d w ere At ten t ion h as also recen t ly ret u rn ed to t h e role of m icrocir-
m ore frequ en tly obser ved in pat ien t s w h o dem on st rated w h at cu lator y sp asm . Th e occu rren ce of vasospasm in dist al vessels
w as th en referred to as “sym ptom at ic vasosp asm ,” an d w h ich w e h as been w ell docum en ted for n early t w o decades; path ological
n ow kn ow w as likely th e early sign s of delayed isch em ic com pli- exam in at ion of an im al vessels after exp erim en t al SAH dem on -
cations. Alterations in the fibrin olyt ic cascade also seem to play a st rates n arrow ing of in t rap aren chym al ar teries an d ar terioles,
role; gen et ic variat ion s th at con fer im p aired fibrin olyt ic act ivit y below th e caliber of vessels th at can be im aged reliably.28 Th ese
place pat ien ts at greater risk for delayed isch em ic com p licat ion s fin dings h ave been replicated in h um an s as w ell.29 Th e im plica-
after SAH.21 t ion s of t h is rem ain u n clear; t h ere h ave been n o r igorou s inves-
Cor t ical sp reading depolarizat ion , altern ately referred to as t igat ion s in to w h et h er in ter ven t ion s aim ed at reversin g large
cort ical sp reading dep ression in th e literat u re, is a ph en om en on ar ter y spasm , such as system ic an d local deliver y of n im odipin e
th at w as first described in 1944.22 Alth ough w ell ch aracterized an d in t raar terial calcium ch an n el blockade, h ave th e sam e effect
for decades, th e sign ifican ce of cor tical spreading depolarizat ion on th e m icrocircu lat ion .
in th e clin ical set t ing is on ly recen tly com ing to ligh t; for m any In sigh t in to th e path ogen esis of vasospasm an d delayed isch -
years it w as th ough t to be an elect roen ceph alograp h ic correlate em ic com p licat ion s are in evolu t ion . Clearly, vasosp asm is an
to m igrain e auras. It is defin ed as a self-propagat ing w ave of n eu- im p or t an t p rogn ost ic factor an d h igh ly associated w it h p oor
ronal and glial depolarization, traveling bet ween 2 and 5 m m /m in, outcom e an d th e developm en t of isch em ic sequelae after SAH.
w h ich can be t riggered by local isch em ia or oth er in sult .23 On Th erefore, invest igat ion in to it s p ath ogen esis an d at tem pt s to
elect rocor t icograp hy, th ere is an associated p eriod of d epressed fin d n ew th erapies are crit ical to im proving th e outcom es of pa-
cor t ical act ivit y. More im port an tly, th ere is an associated redu c- t ien ts w h o su ffer an eu r ysm al SAH. Con sen su s recom m en dat ion s
t ion in cerebral blood flow th at t ravels w ith th e dep olarizat ion dict ate th at all pat ien ts w ith angiograp h ically con firm ed vessel
w ave (referred to as sp read ing isch em ia), an d a con com itan t in - spasm sh ould be t reated m edically an d, if n eeded, w ith m ore ag-
crease in en ergy requirem en t s as sodium an d calcium pum ps in gressive en dovascular in ter ven t ion s. How ever, th e scien t ific an d
th e n eu ron al an d glial cell m em bran e are act ivated to re-equili- m ed ical com m u n it ies h ave clearly n oted t h at vasosp asm alon e
brate ion ic gradien ts. is n ot th e cause of cerebral in farct an d poor outcom e in th is pa-
Alth ough th e ph en om en on of spreading depolarizat ion w as t ien t p op u lat ion . At ten t ion h as t u r n ed tow ard gain in g in sigh t
w ell characterized in experim ental preparat ions, it w as only w ith in to, an d developing t reat m en t s for, post-SAH in flam m at ion , m i-
th e ap p licat ion of su bdu ral elect rode st rip s th at th e occu rren ce croth rom bus form at ion , m icrocirculator y spasm , an d spreading
of th is p h en om en on w as obser ved in brain inju r y, in cluding an - dep olarizat ion .
eu r ysm al SAH.24 In a series of elegan t experim en t s, Dreier et al24 Fin ally, it is h as been p rop osed t h at rat h er t h an any on e
im plan ted su bdu ral st rip s w ith recording elect rodes an d opto- m ech an ism , it is th e in teract ion am ong m ult iple path w ays act-
des for laser Dopp ler flow m et r y in 13 p at ien t s w ith an eu r ysm al ing in con cert th at leads to a self-propagat ing cycle resu lt ing in
SAH after su rgical clip ping. Th ey dem on st rated th at in 12 of 13 irreversible crit ical isch em ia an d in farct . For in st an ce, som e h ave
pat ien ts, pat tern s of cor t ical sp reading dep olarizat ion w ere t ak- hypoth esized th at th e large ar ter y vasospasm , th e form at ion of
in g p lace, associated w it h in creases an d d ecreases in cerebral m icroem boli, an d th e presen ce of by-products of h em olysis all
blood flow th at w ere dubbed “hyperem ic” an d “oligem ic” depo- w ork in con cert to low er the thresh old for the initiat ion of spread-
larizat ion s, respect ively. In a select grou p of p at ien t s w h o also ing depolarizat ion ; fu rth er invest igat ion is required before any
h ad oxygen probes in ser ted to record th e t issue par t ial pressure defin it ive con clusion s can be m ade.
of oxygen in adjacen t t issue, hyperem ic depolarizat ion s led to
brain hyperoxia, an d oligem ic depolarizat ion s led to brain hy-
poxia. Perh ap s th e m ost im por t an t t ren d related to clu sters of
dep olarizat ion s in five p at ien ts; th ese clu sters w ere con sisten tly ■ Patient Outcomes w ith
associated w ith brain hypoperfusion , decreases in t issue par t ial
pressure of oxygen, and electrocorticographic depression.25 These
Various Interventions
su stain ed p eriods, in w h ich affected cor tex exh ibit s clu sters of Th is sect ion review s th e relevan t clin ical dat a regarding th era-
dep olarizat ion , are believed to be an im p or tan t con t ributor to pies an d in ter ven t ion s aim ed at redu cing p ost-SAH vasosp asm
isch em ia an d in farct . More invest igat ion is requ ired to elu cidate an d delayed isch em ic com plicat ion s, an d discu sses th e early re-
th e role of th is ph en om en on in th e post-SAH p opulat ion . For in - p or t s of related fu t u re an d em erging t h erap ies. Th e crosst alk
st an ce, con t roversy rem ain s over w h eth er th ese sp reading dep o- bet w een clin ical st rategies being tested an d t h e p osited m ech a-
larizat ion s predate th e on set of crit ical isch em ia, or are sim ply n ism s of cor t ical sp read ing d ep olar izat ion , in flam m at ion , m i-
a pat tern of disch arges given off by n euron s an d glia th at h ave crocircu lator y sp asm , an d form at ion of m icrot h rom bi is also
already su ffered en ergy an d flow failu re. discu ssed .

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480 V Cerebral and Spinal Aneurysms

“Triple -H” Therapy CONSCIOUS-2 t rial, a p h ase 3 RCT com paring clazosen t an w ith
placebo, w h ich took p lace bet w een Decem ber 2007 an d April
Triple-H therapy, w hich entails h em odilution , hypervolem ia, and
2010.38 In th is st udy, pat ien t s w ere ran dom ized to clazosen tan
hyp er ten sion , h as lon g been t h e m ain st ay of m an agem en t of
(n = 768) or placebo (n = 389) for u p to 14 days p ost-SAH in p a-
vasospasm . Th ere is overall a paucit y of reliable data dem on -
t ien ts t reated w ith su rgical clip p ing. Treat m en t w ith clazosen tan
st rat ing im p rovem en t in ou tcom e w ith t rip le-H t h erapy or it s
dem on st rated n o sign ifican t effect on th e p rim ar y en d p oin t of
in dividu al com pon en ts, alth ough th is is n ot u n expected in a dis-
m ortalit y or vasospasm -related m orbidit y 6 w eeks after SAH. The
ease w ith such poor n at u ral h istor y. Th e osten sible goal of t riple-
st u dy did allow for aggressive rescu e th erapy in both t reat m en t
H th erapy is to im prove cerebral blood flow. In par t icu lar, it is
arm s, in clu ding in t raven ous vasopressor th erapy, in t ra-ar terial
th ough t th at h em odilu t ion m ay be deleteriou s; in fact , h igh er-
calcium ch ann el blocker therapy, an d cerebral angioplast y, w hich
th an -baselin e h em oglobin levels h ave been p rop osed as a poten -
m ay h ave obscu red th e effect of th e t reat m en t . Notably, an d in
t ial t reat m en t aven u e, w ith a ph ase 2 t rial cu rren tly en rolling
keep in g w it h t h e resu lt s of CONSCIOUS-1, t h ere w as a sign ifi-
pat ien ts.30 Non eth eless, use of in duced hyper ten sion as a rescue
can t redu ct ion in u se of in ter ven t ion al rescu e th erapy for angio-
th erapy in th e set t ing of develop ing n eu rologic deficit s w ill likely
grap h ic vasospasm in th e clazosen t an t reat m en t arm . Non eth e-
rem ain in place at m ost institutions based on clinical experience.
less, alth ough th e t reat m en t of vasospasm is n ecessar y, th ese
dat a in dicate th at vasospasm alon e is n ot th e cau se of p ost-SAH
m orbidit y an d m or t alit y. Com m en tators h ave suggested th at a
Calcium Channel Blockers
differen t , p ossibly m ore cerebru m -select ive en doth elin -receptor
Nim odip in e, an oral dihydropyridin e calcium ch an n el blocker, is an tagon ist m igh t sh ow greater ben efit th an clazosen tan .39
th e on ly dr ug p roven to redu ce th e in ciden ce of delayed isch em ic
com p licat ion s (DIC) an d im p rove clin ical ou tcom es in SAH in an
eviden ce-based m an n er.31 Osten sibly, n im odipin e prom otes th e Thrombolytic Therapy, Cisternal/Ventricular
relaxat ion of sm ooth m u scle in th e cerebral vasculat u re. In ter- Lavage, and Early Lumbar Drainage
est ingly, st u dies h ave sh ow n th at n im odipin e reduces th e in ci-
den ce of DIC w ith ou t reducing th e in ciden ce of vasosp asm .32 It As m en t ion ed earlier, clearan ce of cistern al blood h as been at-
h as been dem on st rated th at n im odipin e in creases fibrin olytic tem pted as a m ean s of reducing th e risk of vasospasm . Th e deliv-
act ivit y, w h ich m ay accou n t for it s ben eficial or p rotect ive effect er y of th rom bolyt ics, eith er t issu e-t ype plasm in ogen act ivator
in t h e p ost -SAH p op u lat ion .33 Th e efficacy of n im od ip in e en - (t-PA) or u rokin ase, h as been at tem pted in n um erous sm all se-
su res th at it w ill rem ain t h e backbon e of t reat m en t regim en s ries. Kram er an d Fletch er,40 in a m et a-an alysis of five RCTs of
w orldw ide. th rom bolyt ic th erapy (n = 465), w ere able to d em on st rate a re-
du ct ion in th e in ciden ce of vasosp asm as w ell as a red u ct ion in
th e develop m en t of delayed isch em ic com plicat ion s. Differen ces
Endovascular Interventions, Including in m eth odology an d defin it ion preclu de draw ing clear pract ice
recom m en dat ion s from th ese t rials. A com pan ion to th e adm in -
Intra-Arterial Therapy
ist rat ion of th rom bolyt ic agen t s is t h e u se of so-called kin et ic
En d ovascu lar in ter ven t ion s, in clu d in g ar ter ial d eliver y of p a- th erapy, w h ich con sist s of u sing h ead-sh aking tech n ology or lat-
p averin e, n icardip in e, or verap am il, as w ell as angioplast y, h ave eral rot at ion al regim en s to assist in clearan ce of cistern al blood.
becom e a m ain stay of m odern t reat m en t of vasospasm . Th ese Th ese h ave been t ried along w ith th e ad m in ist rat ion of th rom -
techniques have show n efficacy in reversing angiographic spasm .34 bolyt ics, w ith th e goal of achieving a syn ergist ic effect .41,42 Early
Alth ough th ere is n o su bst an t ive eviden ce lin king th ese in ter- lu m bar drain age h as also been p roposed as a m eth od of redu cing
ven t ion s to im proved fun ct ion al outcom e, pat ien t s w ith vaso- th e bu rden of blood in th e su barach n oid sp ace, w ith prelim in ar y
spasm refractor y to m edical in ter ven t ion w ill likely con t in ue to dat a on th is tech n iqu e sh ow ing decreased in ciden ce of vaso-
un dergo en dovascu lar rescue th erapy at m ost in st it u t ion s. Th e spasm .43 Alth ough th e result s of th ese prelim in ar y invest igat ion s
refin em en t of en dovascular tech n ologies w ill con t in ue in th is are prom ising, m ore rigorous studies on the use of throm bolytics,
realm , an d n ew tech n iqu es w ill u n doubtedly be added to th e ar- kin et ic th erapy, an d early lum bar drain age are pen ding.
m am en t arium . Th e use of in dw elling m icrocath eters h as already
been reported,35 an d even bedside applicat ion s su ch as aor t ic
balloon occlusion to im p rove cerebral p erfu sion .36 Magnesium
Magn esium is a physiological calcium com pet itor. At th e level of
th e cell m em bran e, m agn esiu m is kn ow n to com p et it ively block
Endothelin Receptor Antagonists
calciu m ch an n els. In an im al st u dies of SAH, m agn esiu m in fu sion
En d ot h elin -1 h as lon g been im p licated in t h e p at h ogen esis of appears to reduce th e in ciden ce of both vasospasm an d delayed
vasospasm ; fur th erm ore, th e select ive en doth elin -1A receptor isch em ic com p licat ion s.44 Addit ion ally, ph ase 2 dat a h ad dem on -
an tagon ist clazosen tan ap peared to redu ce vasospasm in an im al st rated p rom ise for redu ct ion in delayed isch em ic com p licat ion s.
m odels of SAH. Th e ph ase 2 t rial Clazosen tan to Overcom e Neu- In a ph ase 3 t rial, In t raven ous Magn esium Su lfate for An eur ys-
rological Isch em ia an d In farct ion Occu rring After Subarach n oid m al SAH (IMASH), pat ien ts in th e t reat m en t arm w ere assign ed
Hem or rh age 1 (CONSCIOUS-1) d em on st rated a sign ifican t an d to receive MgSO4 in fusion s t it rated to a seru m Mg 2+ con cen t ra-
dose-dep en den t redu ct ion in angiograp h ic vasospasm , w ith ou t t ion of t w ice baselin e for 10 to 14 days. Th e st u dy failed to
clearly dem on st rat ing an im p rovem en t in ou tcom e.37 Th e prom - d em on st rate a sign ifican t differen ce in n um ber of pat ien ts w ith
ise in h eren t in t h is fin ding w as tem pered by th e result s of th e favorable ou tcom e defin ed by th e Glasgow Ou tcom e Scale at 6

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40 Cerebral Vasospasm and Delayed Ischemic Complications 481

m on th s. Th ere w as likew ise n o sign ifican t differen ce in th e m od- basal cistern in close proxim it y to cerebral vessels w as at tem pted
ified Ran kin Scale score or oth er secon dar y ou tcom e m easu res. as a st rategy to red u ce t h e in cid en ce of vasosp asm . Th ese p el-
Notably, th e side effect s of h igh -dose m agn esiu m in fu sion , w h ich let s release t h e d r ug over a p er iod of 14 days. Th e st u dy took
can in clu d e hypoten sion an d bradycardia, are often u n desirable p lace across m u lt ip le in st it u t ion s in Tokyo, an d obser ved a d e-
in th e p ost-SAH pop u lat ion . Prop on en ts h ave argued th at h igh er crease in t h e in cid en ce of vasosp asm an d im p rovem en t s in t h e
serum m agn esium levels m ay be required to dem onst rate efficacy, clin ical ou tcom e. As an in creasin g n u m ber of p at ien t s are u n -
due to th e low cerebrospin al fluid pen etration of intravenous d ergoing en d ovascu lar t h erapy, t h e feasibilit y of u sing in t ra-
Mg 2+.45 To t h is en d , adm in ist rat ion of m agn esiu m via m icro- ven t ricular n icardipin e prolonged-release im plan ts h as also been
cath eter in to th e cistern a m agn a h as been tested in can in es.46 dem on st rated.53
Th is m ay be an area w ith p rom ise for fu t u re developm en ts.

Fasudil
Nitric Oxide Donors Fasu d il, a rh o-kin ase in h ibitor, h as been st u died for th e t reat-
Deficien t p rodu ct ion of th e free radical n it ric oxide, w h ich m edi- m en t of vasospasm , an d appears to reduce th e in ciden ce of vaso-
ates vascu lar sm ooth m u scle rela xat ion , h as long been th ough t spasm w ith out an appreciable ch ange in fun ct ion al outcom e in
to con t ribute to th e path ogen esis of vasospasm .47 From a clin ical m ultiple sm all t rials.54 Due to differen ces in tech n ique an d defi-
st an dp oin t , n it ric oxide don ors su ch as sodiu m n it rop ru sside n it ion , th ere is n o reliable data proving th e efficacy of fasudil in
an d n it roglycerin are ch aracterized by a sh or t h alf-life, an d h ave th e p ost-SAH populat ion .31
th e n ot able side effect of system ic hyp oten sion , w h ich is u n de-
sirable in th e post-SAH p op u lat ion . With resp ect to n it ric oxide
don ors, th eir efficacy in t reat ing vessel sp asm is n ot in qu est ion ,
bu t con t roversy rem ain s over t h e select ion of an ap p rop riate ■ Discussion
deliver y veh icle. Sodium n it rite, NaNO2 , w h ich can be in fu sed in -
t raven ou sly, h as been tested in p rim ate SAH m odels an d sh ow n We h ave highlighted the chronological developm ent of our under-
to redu ce vasospasm , an d addit ion ally has been sh ow n to be w ell st an ding of th e path ogen esis of th e on set of cerebral vasosp asm
tolerated in h um an s.48,49 Alth ough at presen t th ere is n o evi- after an eu r ysm al SAH. We h ave also ou t lin ed th e sign ifican t
den ce su p p or t ing th e rout in e u se of n it ric oxide d on ors for th e con t roversies th at defin e th e field today, n am ely th e discon n ect
t reat m en t of vasosp asm , th is area seem s a likely target for fu r- bet w een effect ive t reat m en t of vasospasm an d effect ive protec-
th er develop m en t an d test ing in cluding clin ical t rials. t ion again st delayed isch em ic com p licat ion s. Th is discon n ect
w as h igh ligh ted m ost recen tly by th e h igh ly visible CONSCIOUS-2
t rial. In an all-too-fam iliar cycle, th e sign ifican t p rom ise dem on -
Statins st rated in early test ing of en doth elin -1A receptor an t agon ist s
w as tem p ered by th e lack of clin ical efficacy w h en expan ded to a
St at in s h ave long been ap preciated to h ave p leiot rop ic effects. m ulticenter, random ized, double-blind, placebo-controlled study.
With respect to th eir app licat ion in SAH, th ey are believed to re- How ever, th e data w ere valu able in th at th ey u n derscored th e
du ce p rodu ct ion of react ive oxygen sp ecies an d u pregu late n it ric m ultifactorial n at ure of isch em ic com plicat ion s. Cer t ain ly, prog-
oxide syn th ase (NOS), an d m ay at ten u ate glu tam ate excitotoxic- ress h as been m ade in term s of elu cidat ing can didate path w ays
it y. Th ere is n o reliable data as to th e p en et rat ion of stat in s across th at are involved in th e developm en t of isch em ic deficit s; it is
th e blood–brain barrier; h ow ever, invest igat ion s in to th eir pleo- n ow w idely accepted th at sm all ar ter y spasm , in flam m at ion , for-
tropic effects suggest th at they preven t dam age to tigh t junct ions m at ion of m icroth rom bi, an d cort ical spreading depolarizat ion s
an d slow n eut roph ils in filt rat ion in to th e paren chym a.50 Tw o are im p or t an t p h en om en a in t h is p at ien t p op u lat ion . To date,
ph ase 2 t rials involving th e u se of sim vastat in an d p ravast at in t h erap ies t arget in g t h ese m ech an ism s h ave been n o m ore su c-
seem ed to sh ow red u ct ion in th e in ciden ce of delayed isch em ic cessfu l in im p rovin g ou tcom es t h an th e t h erap ies d irected to-
com plicat ion s an d im provem en t in m or talit y.51 Addit ion ally, im - w ard t reat ing vasospasm .
m ediate st at in th erapy in th e post-SAH populat ion is accepted as St ill, th ere is reason for opt im ism . Th ere are several p en ding
safe, w ith rou t in e m on itoring of h ep at ic fu n ct ion tests. A m u lt i- ph ase 3 invest igat ion s, as ou tlin ed earlier, in clu ding th e u se of
center RCT, Sim vastatin in Aneur ysm al Subarachnoid Hem orrhage im m ediate stat in th erapy, in t raven ou s m agn esiu m in fu sion , an d
(STASH), recen tly reported th eir results w ith pat ien t s w h o w ere early lum bar drain age, w h ich m ay yield posit ive resu lt s. If th eir
ran dom ized to receive sim vastatin 40 m g daily for 21 days versu s m eth odology is deem ed appropriate, th ese in ter ven t ion s m ay
placebo, beginning w ithin 96 hours of ictus. The prim ary out- becom e th e stan dard of pract ice. Likew ise, several th erapies an d
com e w as t h e m odified Ran kin Scale score at 6 m on th s, w ith tech n ologies curren tly in developm en t m ay m at ure in to im por-
secon dar y ou tcom es in clu ding th e Med ical Ou tcom es St u dy 36- tan t t reat m en t protocols. For in stan ce, th e use of sodium n it rite
Item Sh or t-Form Health Su r vey (SF-36), m or talit y, an d length of in fu sion , an d placem en t of n icardip in e release pellet s eith er at
st ay. Th e t rial dem on st rated n o ben efit for th e use of sim vastat in t h e t im e of su rger y or via in t raven t r icu lar im p lan t at ion , n eed
for long-term or sh or t-term outcom e.55 to be d evelop ed fu r t h er an d m ove beyon d th e m ere test ing
st age. It is fu r th er likely th at m any n ovel t reat m en t algorith m s
are being tested in th e Un ited St ates an d w orldw ide bu t h ave yet
Local Nicardipine Delivery to be repor ted. For in stan ce, at ou r in st it ut ion w e are invest igat-
Kasuya 52 repor ted th e result s of a clin ical t rial in w h ich place- ing th e u se of in t rath ecal n icardipin e adm in ist rat ion for refrac-
m en t of n icardipin e delayed-release im plan ts (“pellets”) in th e tor y vasospasm .

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482 V Cerebral and Spinal Aneurysms

of vasospasm an d th e developm en t of delayed isch em ic com pli-


■ Conclusion cat ion s follow ing an eu r ysm al SAH is at an excit ing crossroads.
Pract ice p arad igm s at m ajor n eu rosu rgical an d n eu rocr it ical Recen t disappoint m ents not w ith standing, it seem s probable that
care cen ters w ill con t in u e to evolve. As th e on ly m ed ical th erapy n ew an d im por tan t m ech an ist ic an d clin ical un derstan ding w ill
backed by class I eviden ce, adm in ist rat ion of n im odipin e w ill of evolve from th e explosion of research in to th is field. As a profes-
cou rse rem ain th e con st an t in all t reat m en t regim en s. Desp ite sion , w e seem to be on t h e cu sp of im p or t an t breakt h rough s
th e lack of ran dom ized con t rolled dat a, in du ced hyper ten sion in t h is area, w it h m ajor im p licat ion s for ou r afflicted p at ien t
an d en dovascular rescue tech n iques for m edically refractor y va- pop u lat ion s.
sosp asm w ill likely also rem ain in u se. Ou r in sigh t in to th e on set

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subarach n oid h em orrhage: st udy protocol for a ran dom ized con t rolled 54. Liu GJ, Wang ZJ, Wang YF, et al. System at ic assessm ent an d m et a-an alysis
t rial. Trials 2011;12:203 of th e efficacy an d safet y of fasu dil in t h e t reat m en t of cerebral vaso-
44. Suarez JI; Par t icipan t s in th e In ternat ion al Mult idisciplin ar y Con sen sus spasm in pat ien t s w ith subarach n oid h em orrh age. Eur J Clin Ph arm acol
Con feren ce on th e Crit ical Care Man agem en t of Su barach n oid Hem or- 2012;68:131–139
rh age. Magn esium sulfate adm in ist rat ion in subarach noid h em orrhage. 55. Kirkpat rick PJ, Turn er CL, Sm ith C, Hutch inson PJ, Murray GD; STASH Col-
Neu rocrit Care 2011;15:302–307 laborators: Sim vastatin in aneurysm al subarachnoid haem orrhage (STASH):
45. Wong GK, Poon WS, Chan MT, et al; IMASH Invest igators. In t raven ous a m u lt icen tre ran dom ised ph ase 3 t rial. Lan cet Neu rol 2014;13:666–675.
m agn esium sulph ate for an eur ysm al subarach n oid h em orrh age (IMASH):

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41 Medical Management of
Subarachnoid Hemorrhage
Shaw n Eugene W right

been in adequ ately st ud ied . In terest ingly, h ow ever, th e great m a


■ Pathophysiology and Natural History jor it y of an eu r ysm s t h at d o r u pt u re are sm all—often less t h an
of Subarachnoid Hemorrhage 10 m m in size.11 Alth ough in t im al dam age don e to in t racran ial
vessels by ath erosclerosis du e to m et abolic disease (hyper ten
Su barach n oid h em orrh age (SAH) is on e of th e m ost seriou s an d
sion , hyperlipidem ia, an d hyp erglycem ia) an d to sm oking is be
dram at ic crit ical care em ergen cies. Su ccessfu l m an agem en t of
lieved to be th e m ain cau se of an an eu r ysm form at ion , oth er
th e p at ien t w ith SAH requ ires rap id an d focu sed care by th e crit
n on acquired con dit ion s also play a role.
ical care physician from in it ial presen tat ion th rough th e often
Th e associat ion of in t racran ial an eu r ysm w ith h erit able con
storm y in ten sive care u n it (ICU) cou rse u n t il disch arge to th e
n ect ive t issue disorders an d th e fam ilial pat tern of in t racran ial
n eu ro reh abilitat ive care team .
an eur ysm s is w ell described but accoun ts for on ly a sm all per
cen tage of all SAH. In disorders such as autosom al dom in an t
polycyst ic kidn ey d isease (ADPKD), an eu r ysm s arise in u p to 10%
Epidemiology of p at ien t s. In fam ilial in t racran ial an eu r ysm (FIA) syn d rom e,
Th e in ciden ce of SAH in m ost p op u lat ion s is bet w een 6 an d 10 an eu r ysm s are often m u lt ip le an d p resen t earlier in life. A recen t
per 100,000 p erson s.1,2 Th e in ciden ce m ay be double th at in Fin gen om e w ide associat ion st udy of an eur ysm s in Fin n ish , Du tch ,
lan d an d Jap an .1 SAH rem ain s com m on in you ng adults, w ith h alf an d Japan ese patien ts iden t ified five gen et ic loci for FIA.12 Th ese
of all cases occurring before th e age of 55.2 Racial d ifferen ces an eu r ysm r isk loci exp lain on ly 5% of t h e fam ilial r isk of in t ra
h ave been repor ted as w ell, w ith blacks dem onst rat ing a t w ofold cran ial an eu r ysm s. Rare gen et ic disorders su ch as Eh lers Dan los
greater risk th an w h ites of su ffering SAH.3 An eu r ysm al r u pt u re syn drom e an d Klip p el Tren au n ay Weber syn drom e cau se a loss
accoun ts for 85% of all SAHs, w ith th e rem ain ing 15% at t ributed of vascular m edia in tegrit y an d dysfun ct ion al elast icit y an d are
to n on an eur ysm al sou rces such as t rau m a, in fect ion , vasculit is, et iologies for in t racran ial an eu r ysm form at ion .
drugs, m alignancies, and the relatively ben ign perim esenceph alic Per im esen cep h alic SAH (PMSAH) accou n t s for 10% of all
pat tern SAH (Table 41.1).4 Mor t alit y rates associated w ith SAH SAHs. Bleed in g occu rs at t h e m id brain cister n s an d d oes n ot
var y from 45% to over 60%.5,6 Alth ough certain t y is lacking, a dem on st rate in t raven t ricu lar exten sion . St u dies dem on strat ing
m eta an alysis est im ates 12.4%of SAH pat ien ts die su dden ly prior prim itive venous drainage around the m idbrain support a venous
to reach ing t h e h osp it al.7 Mor t alit y rates aside, th e m orbidit y origin of PMSAH.13 Th ese pat ien ts h ave m uch bet ter outcom es
associated w it h SAH is sign ifican t . Pat ien t ou tcom es after SAH, th an pat ien t s w ith stan dard SAH.
m easu red in qu alit y of life an d abilit y to perform p rem orbid ac
t ivit ies, are often p oor. A m ajorit y exp erien ce deficit s in m em
or y, cogn it ive fu n ct ion , an d lan gu age skills.8 Im p rovem en t in
fu n ct ion al an d p sych osocial ou tcom e h as occu rred over t h e past ■ Clinical Presentation and Diagnosis
decade, bu t m orbidit y rem ain s h igh .9 Tran sfer to h igh volum e
cen ters w ith n eu rocrit ical care p hysician s is associated w ith im Pat ien t s w it h SAH com m on ly p resen t w it h hyp er ten sion t h at
proved h ospital disch arge in p at ien ts w ith an eu r ysm al SAH.10 is often severe. Oth er vital sign abn orm alit ies m ay in clude a low
grade fever, relat ive bradycardia, an d bradypn ea. Th e cardin al
sym ptom of SAH, th e “w orst h eadach e of m y life,” is presen t in a
Pathophysiology of Aneurysmal m ajorit y of cases, an d alm ost 80%of th e t im e it occurs abruptly.14
Lesser h eadach e con foun ds th e diagn osis an d m ay delay a pa
Subarachnoid Hemorrhage tient’s presentat ion several days after an eur ysm al rupt ure. Sym p
In t racran ial an eur ysm s arise at any age an d are n ot due to con tom s accom panying th e severe h eadach es in clude sudden onset
genital vascular disorders per se.11 Most of these aneurysm s never of nausea, vom iting, seizures, and altered level of consciousn ess.
rupt ure. An eur ysm s com m on ly develop as a resu lt of com m on Alth ough th ese sym ptom s are n ot path ogn om on ic of SAH, in th at
acqu ired factors su ch as su st ain ed hyp er ten sion an d at h ero th ey are often p resen t w ith n on an eu r ysm al h eadach e as w ell,
sclerot ic disease. An eur ysm s ten d to form at poin ts of “vascular th ey are alm ost alw ays p resen t w h en an eu r ysm ru pt u re an d SAH
su scept ibilit y,” su ch as ben ds, bifurcat ion s, an d defects of vessel occur. Seizure act ivit y w ith h eadach e is in dicat ive of an eur ysm
w all in tegrit y du e to ath erosclerosis. It is w ell kn ow n th at an eu r u pt u re. Seizu re act ivit y is p resen t at on set of SAH in 8% of
r ysm s h ave a risk of ru pt ure rough ly proport ion al to an eur ysm p at ien t s an d in up to 26% p rior to th e an eur ysm being secured.
diam eter, alth ough th e physics of p redict ing th e an n u al risk h as Seizure por ten ds a poor outcom e.15

484

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41 Medical Management of Subarachnoid Hemorrhage 485

Table 41.1 Causes of Subarachnoid Hemorrhage r ysm al source m ust be iden t ified. CTA is h igh ly accurate in de
tect ing 94% of an eur ysm s greater th an 3 m m in diam eter but
Aneurysm rupture 85%
on ly 70% of th ose less th an 3 m m . Conven t ion al cath eter angiog
Nonaneurysmal 15%
Vascular raphy or digital subt ract ion angiography (DSA) rem ain s th e st an
Perimesencephalic hem orrhage dard for diagn osing an eu r ysm w ith n early 100% sen sit ivit y an d
Arteriovenous malform ations specificit y, even for an eu r ysm s less th an 3 m m in diam eter.19
Arterial dissection DSA also provides th e oppor t un it y to in ter ven e using en dovas
Dural arteriovenous fistula cular techniques w hen indicated. W hen aneur ysm al SAH is highly
Moyamoya syndrom e su spected, CTA rath er th an DSA m ay be u sefu l if th e p at ien t is
Inflammatory/infectious eith er u n st able or in ap propriate for invasive angiograp hy (fu lly
Vasculitis an t icoagu lated or n on sur vivable) or if DSA is un available.
Mycotic aneurysm
Cocaine related
Trauma
Neoplastic ■ Initial Neurocritical Care
Coagulopathies
Medical Evaluation
Pat ien t s w it h su sp ected or con fir m ed SAH sh ou ld be m an aged
at a h igh volum e cen ter of excellen ce if at all feasible. A m ult idis
ciplin ar y n eurocrit ical care team is associated w ith im proved
A w axing an d w an ing level of aler t n ess is eviden ce of th e in outcom es in th e care of pat ien ts w ith an eur ysm al SAH.10 Th e
flam m ator y an d irritat ing effect of acute subarach n oid blood on prim ar y focu s of th e crit ical care p hysician m u st be on basics
th e brain . Sim ilarly, n u ch al rigidit y is an in dicator of an irrit ated su ch as p roviding an adequ ate air w ay an d en su ring ap propriate
su barach n oid sp ace; h ow ever, th is sign requ ires several h ou rs to h em odyn am ic stabilit y. Secon dar y elem en ts of th e assessm en t ,
develop , an d th u s m ay n ot be a sen sit ive clin ical sign early on . w h ich provide a glim pse in to th e progn osis, in clude th e n eu ro
Rarely, pat ien ts m ay com plain of visu al dist urban ces an d blin d logic exam at adm ission an d th e early im aging st udies.
spot s at clin ical presen t at ion . Ocular h em orrh ages are repor ted Th e d egree of n eu rologic im p air m en t on ad m ission cor re
in 17 to 40% of p at ien t s w ith SAH. Abru pt an d severe elevat ion s lates w ith outcom e.20 Clin ical grading scales such as th e Glasgow
in in t racran ial pressu res are believed to be th e cau se. Hem or Com a Scale (GCS), th e Hu n t an d Hess (HH) scale, th e Fish er scale,
rh age in to th e vit reou s h u m or (Terson’s syn drom e) is ver y com and the World Federation of Neurosurgical Societies (W FNS) scale
m on in pat ien t s w ith devast at ing SAH. Fun du scopic exam in at ion h ave been used for m any years to provide a basic “language” of
of un respon sive pat ien t s w ith SAH is essen t ial, as it m ay reveal clin ical severit y so that clin ician s m ay describe th e injur y, seri
th is con dit ion , w h ich is associated w ith a great ly in creased m or ally follow exam s, an d ren der progn osis on pat ien t s w ith n euro
talit y.16 Classically, th ird n er ve dysfu n ct ion can h elp localize th e logic dysfu n ct ion from SAH. Th e ubiquitous GCS is used in SAH
an eur ysm to th e posterior com m un icat ing ar ter y as it bran ch es grading to establish th e severit y of th e in it ial n eurologic in sult
off th e in tern al carot id ar ter y. an d to assist w ith im m ediate n eurocrit ical care n eeds. Low scores
A sent in el h em orrh age m ay occu r in up to on e in five pa (< 7–9) correlate w ith a poor level of con sciousn ess an d th e n eed
t ien ts.17 Th is clin ical presen tat ion m ay be sim ilar to th e severe to provide an altern ate air w ay. Th e HH, Fish er, an d W FNS scales,
h eadach e of an eu r ysm r u pt u re. Com m on ly, h ow ever, an in sidi u n like th e GCS, are design ed to evalu ate SAH. Th e HH scale is an
ous dull h eadach e, less severe th an th e classic SAH rupt u re, is arbit rar y assessm en t of th e com bin ed effect of m en ingeal irrita
seen . Sen t in el bleed s m ay h erald a ru pt u re 2 to 6 w eeks in ad t ion an d n eu rologic dysfu n ct ion from SAH. Th e grading scale
vance in m any patients. A high degree of suspicion is required to ranges from I to V an d is su bject ive (Table 41.2). Not surprisingly,
determ ine w hether the headache associated w ith a sen tin el bleed st u dies in dicate th at pat ien t s w ith HH grades of I to III h ad bet
represents an incipient aneurysm rupture or is sim ply headache ter outcom es th an patien ts w ith grades III to V.20 Th e progn ost ic
from another cause. It rem ains unclear if recognition of these accuracy of th e W FNS scale w as repor ted to be im proved over
“early warning” headaches leads to bet ter patient ou tcom es.18 th at of eith er th e HH scale or GCS alon e; h ow ever, su bsequ en t
Delay in SAH diagn osis u n accept ably exp oses th e p at ien t to st udies h ave called this into quest ion.21 Th e Fish er scale describes
th e risk of death from rebleeding of th e u n secu red an eu r ysm . th e ap pearan ce of su barach n oid blood on th e in it ial CT im aging.
Rebleeds rates from u n secu red an eu r ysm s app roach 80% in th e Th e scale is su bject ive, an d alth ough it is design ed to predict th e
first year.11 Th e fun dam en tal tool of SAH diagn osis is th e n on likelih ood of cerebral vasosp asm , it w as lim ited by th e im aging
con t rast com p u ted tom ograp hy of t h e h ead (CTH). Cu r ren t qu alit y of th e t im e. Th e m odified Fish er scale m ore accu rately
gen erat ion CT im aging detect s 91 to 95% of all SAHs. Tradit ion predicts vasospasm risk an d perm its th e clin ician to address th e
ally, in n egat ive CT st u dies, th e addit ion of cerebrospin al flu id risk early on .22
(CSF) sam pling by lu m bar pun ct ure excluded SAHs in alm ost Th e m edical m an agem en t of th e pat ien t w ith SAH represen ts
100% of p atien ts. Recen tly, CT angiograp hy (CTA) after n egat ive a con t in u u m of care t h rough several u n iqu e st ages of p at h o
CTH h as been repor ted to approach 100% sen sitivit y an d speci p hysiology. Th ese clin ical st ages en t ail d ifferen t cr it ical care
ficit y in exclu d in g an eu r ysm al SAH. CTA after n egat ive CTH st rategies. For th e pu rposes of th is discu ssion , th e m edical m an
offers a rapid , n on invasive, less t im e con su m in g m et h od of d i agem en t of SAH can be divided in to early, in term ediate, an d late
agn osing aneur ysm al SAH. On ce an SAH is diagn osed, th e an eu periods.

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486 V Cerebral and Spinal Aneurysms

Table 41.2 Subarachnoid Hemorrhage (SAH) Grading Scales

Grade Fisher Hunt and Hess WFNS

1 No blood detected on CT Asymptomatic, mild headache, slight nuchal Glasgow Coma Scale score of 15
rigidit y
2 Diffuse thin (< 1 mm) SAH with no clots Moderate to severe headache, nuchal rigidit y, no Glasgow Coma Scale score of 13–14
on CT neurologic deficit other than cranial nerve palsy without deficits
3 Localized clots or layers of blood > 1 mm Drowsiness/confusion, m ild focal neurologic Glasgow Coma Scale score of 13–14
in thickness on CT deficit with focal neurologic deficits
4 Intracerebral or intraventricular blood Stupor, moderate-severe hemiparesis Glasgow Coma Scale score of 7–12
on CT
5 Coma, decerebrate posturing Glasgow Coma Scale score less than 7
Abbreviations: CT, computed tom ography; WFNS, World Federation of Neurosurgical Societies.

■ Critical Care Medicine Management pressure at or below 160 m m Hg. Sodiu m n it roprusside, alth ough
efficacious, is n ot recom m en ded as first lin e th erapy because of
Strategies for Subarachnoid t h e r isk of toxicit y an d elevat ion of in t racran ial p ressu re.25 Ni-
Hemorrhage cardipin e an d esm olol are effect ive an d w idely u sed in pat ien ts
w ith hyper ten sion in th e set t ing of SAH. Th e use of β-blockers
Early Period (0–72 Hours) can be lim ited by adverse even t s su ch as bradycardia, h ear t
Pat ien t s w h o sur vive th e in it ial SAH an d arrive at th e h osp ital block, and bronchospasm . Furtherm ore, they are contraindicated
requ ire rap id n eurological assessm en t to st rat ify th e th erapeu t ic in pat ien t s w ith dep ressed left ven t ricular fun ct ion . Several t ri
opt ion s. Th e en suing 72 h ours involves st abilizat ion , diagn osis, als of th e ult ra–sh or t act ing calcium ch an n el blocker clevidipin e
an d in ter ven t ion so th at rebleeding, th e m ost devastat ing com in dicate th at it is effect ive in t reat ing hyperten sion in th is set
plicat ion of an eu r ysm al SAH, d oes n ot occur. t ing.26 Its u se m ay be lim ited by th e fact th at it is an em u lsified
Th e SAH pat ien t is at risk for respirator y failu re on adm ission lip id , an d t h e m ajor sedat ive u sed in t h e n eu roscien ce ICU is
du e a variet y of cau ses. A depressed level of con sciou sn ess from an oth er lipid based drug, prop ofol.
seizu res, m en ingeal in flam m at ion , elevated in t racran ial pres Hyp ovolem ia is com m on in acu te SAH p at ien t s. Many SAH
su res, brain stem com p ression , an d hydrocep h alu s are com m on p at ient s are fun ct ion ally dehydrated by th e t im e th ey reach th e
cau ses of respirator y failu re. Pat ien t s w ith GCS scores of 8 or less, ICU, and during th e first 24 h ours th ese pat ien ts require careful
th ose requ iring extern al ven t ricu lar d rain age (EVD) placem en t volum e expan sion to preven t en d organ dysfun ct ion such as im
or pat ien t s at risk for early deteriorat ion w ith HH scores of III or pairm en t of effect ive ren al plasm a flow an d gu t isch em ia. Th e
greater an d Fish er grade 3 or greater are can didates for con intravascular space experiences both a salt and a water im balance
t rolled, elect ive in t u bat ion . Mech an ical ven t ilat ion du ring th is in th e early period, an d th erefore n orm al salin e is th e preferred
early period sh ou ld st rive to preser ve adequate oxygen at ion , volum e expan der during th is t im e. Mon itoring fluid stat us u sing
avoid hypercarbia, an d su pport a pH in th e n orm al range. Ven t i cen t ral ven ous pressu res (CVPs) an d en d organ perfusion st at us
lator y st rategies m ost ap p rop riate for th is p eriod in clu d e fu ll is cr it ical to avoid volu m e overload . Alt h ough t h e p u lm on ar y
su p p or t m od es su ch as assist con t rol (AC) or p ressu re con t rol ar ter y cat h eter is n o longer recom m en d ed to m on itor cen t ral
(PC). Th ere is n o evid en ce t h at favors on e m od e over t h e ot h er h em odyn am ic st at u s in m ost SAH p at ien t s, assessm en t of flu id
in an eur ysm al SAH. Hyper ven t ilator y hypocapn ia as a st rategy responsiven ess m ay be accu rately obt ain ed in m ech an ically ven
to reduce elevated in t racran ial pressure rem ain s con t roversial t ilated n eu rosu rgical p at ien ts u sing con t in u ou s cardiac ou t pu t
(alth ough st ill w idely em ployed).23 Deleterious effects of hypo m on itoring an d th e st roke volu m e variat ion (SVV).27
cap n ia on th e brain , as w ell as oth er organ s, are w ell described . Seizu res occu r in 1 to 7% of SAH p at ien t s d u r in g t h is early
Im proved outcom es in brain injur y an d st roke w h en th erapeut ic p eriod.15 Pat ien ts w ith seizures sh ortly after presen t at ion w ith
hypocapn ic ven t ilat ion is u sed h ave n ot been p roven .24 Th e ben - an eur ysm al SAH are m ost likely experien cing rebleeding, w h ich
efit s of in du ced hypocapn ia m ay be ou t w eigh ed by the sum of p or ten ds a ver y p oor p rogn osis.28 All p at ien t s w ith seizu re ac
th e risks; th e u se of th is th erapy sh ou ld be con sidered on ly in t ivit y sh ou ld be con sidered for in t u bat ion to protect th e air w ay,
life threatening cases of m alignant intracranial hypertension and facilit ate ven t ilat ion , an d p er m it em ergen t ad m in ist rat ion of
w h en oth er effor ts h ave failed . an t iconvu lsan t m edicat ion s. Con t rol of seizu res in th is set t ing
Hypertension in SAH is com m on at presentat ion and is, in part , m ay require dosages of an t iconvulsan ts th at exacerbate respira
du e to th e adren ergic “storm ” of th e cerebral inju r y along w ith tor y depression ; protect ion of th e air w ay is param oun t in th is
pain an d gen eral an xiet y. Con t rol of hyp erten sion is essen t ial to in st an ce. Prop hylact ic u se of an t iconvu lsan t s, esp ecially p h e
p reven t rebleed ing from an u n secu red an eu r ysm .25 Th e m ost nytoin , at SAH p resen t at ion is n ot recom m en ded.25 Pat ien t s w h o
effect ive m eth od of hyp er ten sion con t rol involves u sing con t in develop seizu res after th e an eu r ysm is secu red requ ire an t icon
uou s in fusion of an t ihyp erten sive m edicat ion s th at h ave a rapid vulsan t th erapy; h ow ever, t reat m en t m ay be t run cated to 3 to 6
on set of act ion an d sh or t h alf life to m ain tain systolic blood m on th s if th e seizure act ivit y is w ell con t rolled an d if th e pat ien t

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41 Medical Management of Subarachnoid Hemorrhage 487

does n ot h ave a h istor y of seizu re prior to th e SAH. In p oor grade Intermediate Period (4–14 Days)
SAH, n on convu lsive seizu res are n ot u n com m on an d rep resen t
Vasospasm and Delayed Cerebral Ischemia
a sign ifican t cause of n eurologic deteriorat ion during th is early
period.29 Con t in u ou s elect roen ceph alogram (EEG) m on itoring is Th e in term ediate period is dom in ated by th e risk of developing
recom m en d ed to diagn osis an d m on itor th erapy in th ese cases. vasospasm an d cerebral isch em ia. Radiograph ic vasospasm m ay
Approxim ately 25 to 30% of pat ien ts develop hydroceph alus be detected in up to 70% of SAH pat ien ts, but on ly 40% develop
du ring th e early p eriod of ICU t reat m en t of SAH.30 Even in pa- clin ical sym ptom s of vasospasm an d t h e en su ing cerebral isch
t ien ts w ith good clin ical grades on adm ission , hydrocep h alu s is em ia.35,36 Term ed delayed cerebral isch em ia (DCI) becau se it
an in dicat ion for EVD. rarely occu rs du ring th e first 72 h ou rs after SAH (early p eriod),
Rebleeding is a dreaded com p licat ion of SAH. Mor talit y asso th e redu ct ion in region al cerebral blood flow (CBF) an d th erefore
ciated w ith rebleeding of an eur ysm al SAH is 80%, an d th e associ oxygen at ion m ay lead to cogn it ive an d focal n eu rologic deficit s,
ated m orbidit y in th ose w h o su r vive is sign ifican t .11 con fu sion , obt u n dat ion , an d st roke (delayed n eu rologic deterio
Rebleeding in th e first few h ou rs after in it ial r u pt u re an d rat ion [DND]). Alth ough th e developm en t of DCI is poorly u n der
th rough th e first 24 h ou rs of th is early p eriod can occu r in u p to stood, several factors are clearly p redict ive of DCI occu rring in
17% of pat ien ts.31 Risk of early p eriod rebleeding is in creased in SAH, such as th e am oun t of ar terial SAH blood presen t, th e in it ial
pat ien ts w h o h ave h ad a delay in t im e to t reat m en t an d w h o neurologic status of the patient, an d the presen ce of hypovolem ia/
h ave a h istor y of in com pletely secured an eur ysm s.32 Effor t s to hypoten sion at t im e of SAH.11
preven t th is even t in th e p ast h ave involved prim arily bed rest Med ical m an agem en t of vasosp asm an d DCI begin s w ith pre
an d a quiet , n on st im ulat ive environ m en t w ith at tem pts at blood vention and early diagnosis. Institution of oral nim odipine is now
pressu re con t rol. Alth ough th ese are ap p rop riate care m eth od s, standard of care. This inter vention is responsible for a relative risk
th ere is lit tle eviden ce th at th ey alter th e ou tcom e. In p u rsu it of reduction of 33%for DCI and is a class I recom m endation in recent
im proved ou tcom es, early su rgical or en dovascular m an agem en t guidelines.25 Hypotension that m ay result from nim odipine can be
of an eu r ysm r u pt u re h as em erged as t h e st rategy of ch oice lessen ed by low er doses w ith m ore frequen t adm in ist rat ion .
w h erever p ossible. Th e r isk red u ct ion of a p oor ou tcom e in a Becau se im paired cerebrovascu lar autoregulat ion is believed
su rgically secured an eu r ysm com pared w ith con ser vat ive care to occur w ith SAH, m ain tain ing adequate volum e st at us assists
approach es 20%.33 in avoiding poor cerebral perfu sion . Euvolem ia is t h e preferred
Th e role of an t ifibrin olyt ic t h erapy to p reven t rebleeding du r goal at th is poin t , as m ost dat a do n ot su ppor t a ben efit to vol
ing th is early p eriod h as d im in ish ed, as early surgical an d en do u m e “loading.”37 Pu lm on ar y ar ter y cath eters do n ot assist w ith
vascu lar t reat m en t of an eur ysm s h as been advocated. Th e early assessm en t of fluid respon siven ess, an d w e do n ot recom m en d
dat a on an t ifibr in olyt ic t h erapy u sin g agen t s su ch as ep silon th eir rout in e use.
am in ocap roic acid (EACA) an d t ran exam ic acid (TXA) sh ow ed Radiograph ic detect ion of vasosp asm t yp ically involves cere
th at rebleeding cou ld be sign ifican tly redu ced bu t at th e cost of bral angiography and serial transcranial Doppler (TCD) ultrasound.
in creased rates of cerebral isch em ia (vasosp asm ) an d st roke.34 Accurate an d n oninvasive, TCD can detect elevat ion s in CBF ve
As a resu lt of th ese dat a, long cou rse th erapy w ith EACA or TXA locit ies in dicat ive of develop ing vasospasm .37 Th rice w eekly TCD
is n ot recom m en ded. Sh or t cou rse t rials (72 h ou rs or less) of an su r veillan ce is n orm at ive in h igh volu m e in stit u t ion s. Brain t is
t ifibrin olyt ic th erapy in con cer t w ith m icrosu rgical clip p ing of su e oxygen m on itoring (lead dioxide [PbO2 ]) is a n ovel tech n iqu e
an eur ysm s h ave repor ted reduct ion s in rebleeding rates w ith out to diagn ose an d m on itor cerebral vasospasm . St udies sh ow th at
a ch an ge in fu n ct ion al ou tcom es w h en com p ared w it h n o u se redu ct ion s in local PbO2 correlate w ith vasospasm severit y.38
of an t ifibrin olyt ic agen ts. Alth ough it is im p or tan t to avoid an t i Cu r ren t ly, invest igat ion al PbO2 m on itor in g is lim ited by it s in
fibrin olyt ics in pat ien ts w ith risk factors for th rom boem bolic vasive n at ure, an d lim ited brain t issu e is sam pled w ith a single
even ts, the short course use of agen ts such as TXA and EACA m ay cath eter.
h ave ut ilit y in select cases.32 Medical treatm ent of vasospasm is centered on im proving CBF
Th e en d of life care of pat ien t s w h o h ave su ffered a severe, w ith in cerebral vascu lat ure that h as im paired autoregulator y
likely irreversible brain inju r y as th e resu lt of an SAH w arran t s abilit y due to th e SAH. Th e h em odyn am ic m odalit y th at is th e
d iscu ssion . Th ese p at ien t s an d t h eir fam ilies sh ou ld h ave th e m ain stay of t reat m en t for vasospasm is hyperten sive, hyper vol
opt ion of organ don at ion , w h ich sh ould be discussed w ith th em em ic, an d h em odilu t ion al th erapy (also called t rip le H th erapy
before com for t care is in it iated. Train ed don at ion m an agem en t or HHT).25 In d u ced hyp er ten sion m ay be t h e m ost valu able of
person n el from th e local organ p rocu rem en t organ izat ion sh ou ld t h e t h ree com p on en t t h erap ies; a st u dy exam in in g t h e effect
be involved as early as possible in ever y severely injured pat ien t of HHT using sensitive neurom onitoring and hem odynam ic m oni
w ith a GCS of 5 or less on adm ission . Th e crit ical care specialist is toring techn iqu es dem on st rated in creases in CBF on ly w h en in
cen t ral to th e care of th ese pat ien ts. In stead of decelerat ing care, du ced hyp er ten sive th erapy w as em ployed .39 Clin ical en d p oin ts
appropriate m edical m an agem en t of th e pat ien t by th e crit ical for h em odyn am ic augm en t at ion are h ard to glean from t h e lit
care sp ecialist sh ou ld con t in u e p rior to brain death declarat ion erat u re. Typ ical st rategies in clu d e augm en t in g systolic blood
to en sure th e best poten t ial of organ don at ion if th at in deed be pressure in to th e range of 160 to 200 m m Hg or un t il n eu rologic
com es t h e fam ily’s w ish . To assist w it h t h is t ran sit ion al care, deficit s im p rove. Cr ystalloids or colloids can be u sed to m ain tain
special care protocols term ed cat ast roph ic brain injur y guidelin es adequate volum e stat us during th is t im e. Hem odilut ion (to
are ut ilized at our in st it ut ion (Fig. 41.1). Th ese order sets st an ach ieve h em atocrit s of 30%) in th eor y redu ces viscosit y but m ay
dardize an d st ream lin e care of th e devast at ingly brain inju red act ually h ave a n egat ive im pact on PbO2 du e to redu ced oxygen
patien t so th at th e possibilit y of organ d on at ion is preser ved. carr ying capacit y at low ered h em atocrit s.36

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488 V Cerebral and Spinal Aneurysms

Date/time IV: Goal MAP 60–110 mm Hg

D5W at 125 mL/hr IV 500 ml

5% Albumin IV prn to maintain MAP 60–110 mm Hg

Neosynephrine drip (start 50 µg/m in, m ax 300 µg/m in) titrate to keep MAP 60–110 mm Hg. If not m et,

Add vasopressin drip (start at 0.04 units/minute, max 0.2 units/minute) MAP 60–110 mm Hg. If not met,

Add dopamine drip (start at 1.0 µg/kg/min, max 10 µg/kg/min), titrate to keep MAP 60–110 mm Hg. If not m et,

Add levophed drip (start at 1.0 µg/kg/min, max 10 µg/kg/min) to keep MAP 60–110 mm Hg. If not m et,

Titrate vasopressin for urine output < 3 mL/kg/hr, and hold for Na < 135 or SBP > 140.

VENTILATOR:

FIO2 to keep sats > 97%

PEEP same as pre-brain death determination. If no PEEP had been ordered, institute PEEP of 5.

PCV with pressure control to keep volum e 8 m L/kilo. (For Apnea Test the RT m ay place on AC or PRVC m ode

before apnea test to m anage PCO2 level. After apnea test, patient can be placed on previous set ting.)

Rate to keep PCO2 > 40 mm Hg

SVN with unit dose albuterol every 4 hours

ABG’s ½ hour after initial ventilator set tings

LABS:

CBC, CMP, COAGS, ABG, pCXR

BMP every 8 hours

MEDS: Continue current medications

PROTOCOLS goal: urine output > 0.5 mL/kg/hr

Electrolyte protocol

3% NaCl at 30 mL/hr prn NA+ < 130; hold if Na > 155

Insulin drip protocol prn to maintain blood sugars < 150

If urine output > 250 m L/hour, replace mL for m L with 0.45% NS and consider titration of vasopressin.

Ca tastrophic bra in injury guidelines ca n be initia ted by nursing following bra in dea th decla ra tion until ca re

assumed by Donor Net work of Arizona or orga n donation is declined by fa mily. Prior to bra in dea th decla ration,

a physicia n order is required to implement protocool. If orga n dona tion is declined by the fa mily, proceed with

further orders to remove patient from the ventila tor a nd provide comfort care per prima ry service.

Physician signature Date Time

Fig. 41.1 Catastrophic brain injury guidelines. (Courtesy of St. Joseph’s Hospital and Medical Center, Phoenix, Arizona, USA.)

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41 Medical Management of Subarachnoid Hemorrhage 489

Vasoact ive drugs used for h em odyn am ic augm en t at ion h ave Other Intermediate -Period Management Issues
n ot been com parat ively evaluated for efficacy in SAH. Com m on
agen t s in clu de p h enyleph rin e, dop am in e, an d n orep in ep h rin e. It Hypon at rem ia occurs in 30 to 50% of all SAH pat ien ts an d m ay
h as been our pract ice to begin w ith ph enyleph rin e or n orepi exacerbate in t racerebral sw elling. Th e p ath ophysiology of hypo
n eph rin e. If un acceptable cardiac side effect s occur (bradycardia, n at rem ia is m ost often th ough t to be caused by elevated n at ri
arrhyth m ias, depressed left ven t ricular fun ct ion ), com bin at ion s u ret ic p ept ides in th e dam aged brain t issu e, resu lt ing in cerebral
of agen t s in cluding vasopressin an d dobut am in e or m ilrin on e salt w ast ing or in ap p rop riate an t idiu ret ic h orm on e release or
are used. both .44 Th e t w o disorders m ay represen t a dist in ct ion w ith ou t a
differen ce; th e m ost effect ive t reat m en t for both is salt . Most
com m on ly in fu sion s of hyper ton ic salin e an d th e u se of m in er
Cardiac Complications and Myocardial Stunning alocor ticoids such as fludrocor t ison e are m ost h elpfu l in m ain
Cardiac com p licat ion s m ay occu r in u p to 50%of all pat ien t s w ith t ain in g ap p rop r iate ser u m sod iu m levels. Dem eclocyclin e m ay
SAH. Most of th ese are relat ively in n ocuous an d in clude t ran sien t also be u sed to m ain t ain sod iu m levels; h ow ever, it s on set of
electrocardiogram (ECG) ch anges an d arrhythm ias. Approxim ately act ion is slow.
20 to 30% of pat ien t s experien ce m ore serious disorders during Even w ith th e u se of p n eu m at ic com p ression stockings an d
adm ission , result ing in cardiac decom pen sat ion of som e t ype.40 ch em oprophyla xis, deep ven ou s th rom bosis (DVT) m ay be fou n d
Th e decision to p erform cardiac cath eterizat ion in SAH is an in in alm ost 25% of SAH pat ien t s.45 DVT prophyla xis is crit ical in
dividu al on e based on a m u lt it u de of factors. Com p licat ing th e th ese pat ien t s an d sh ou ld begin after th e an eu r ysm al sou rce of
decision to p erform a card iac in ter ven t ion is th e n eed to place bleeding is secu re or by 72 h ours of h ospit alizat ion to preven t
th e pat ien t on an t iplatelet agen t s an d sh or t term an t icoagu la DVT. Both low m olecu lar w eigh t h ep arin (LMW H) an d st an dard
t ion if a coron ar y sten t is placed. Obviously, in th e set t ing of SAH u n fract ion ated h ep arin h ave a good safet y record in prophyla xis
an d p ossible n eu rosu rger y t h is in ter ven t ion m u st be carefu lly of DVT in SAH.45 LMW H sh ould be stopped 24 h ou rs before in
con sidered . ser t ion or rem oval of ven t ricu lar drain s, m on itoring devices, or
Tran sien t left ven t ricu lar dysfu n ct ion (TLVD) in SAH occu rs in lu m bar drain s to redu ce th e risk of bleeding at th ese sites
11%of pat ien t s.41 Often , p u lm on ar y ed em a is th e prim ar y sign of Altern at ive air w ay requirem en t s or feeding routes becom e
con t ract ilit y dysfun ct ion . Th ere are several categories of systolic apparen t in m any SAH pat ien ts ver y early in to th e in term ediate
dysfun ct ion th at occur in th e set t ing of SAH. Som e debate exists period. Poor clin ical grade h em orrh age w ith severe n eu rologic
about w h eth er these are t ru ly separate diagn ost ic en t it ies or im p air m en t an d brain stem involvem en t vir t u ally m an d ate t ra
rath er varian t s on a sp ect ru m of sim ilar p ath op hysiology. TLVD ch eostom y an d gast rostom y su p p or t . W it h aggressive care in
in clu des syn drom es su ch as m yocardial st u n n ing (MCS), apical t h e ICU an d reh abilit at ion , m ost of th ese p at ien ts recover su b
balloon ing syn drom e (ABS), n eurocardiac st un n ing (NCS), an d st an t ially an d h ave th eir su p p or t t u bes rem oved. Percu t an eou s
takotsubo cardiomyopathy (TTC). These entities are differentiated t rach eostom y an d gast rostom y t u bes p laced at th e bedside by
prim arily by ech ocardiograp h ic criteria. Most invest igators h old crit ical care physician s are curren tly th e preferred m eth od of air
th at a su dden an d severe in crease in sym path et ic n er vous act iv w ay an d feeding su p p or t in h igh volu m e n eu roscien ce cen ters
it y resu lt s in an oxygen m ediated free radical “surge.” Th is leads (Jam es Forseth , MD, person al com m un icat ion ).
to t ran sien t calcium overload an d decreased respon siven ess of Hyperglycem ia is com m on in pat ien ts w ith SAH, an d glu cose
con t ract ile elem en t s, cau sing m yocardial failure.42 Most pat ien ts m an agem en t is cen t ral to reducing in fect ion risk an d poor out
begin to im prove in 48 h ou rs, alth ough th e cardiac dysfun ct ion com es in SAH.46 Cau ses of hypoglycem ia in clu de poor con t rol of
m ay be p rofou n d du ring th is p eriod. Ven t ilator sup por t of acu te exist ing d iabetes, st ress in d uced hyperglycem ia, an d glu cocor t i
pu lm on ar y edem a is com m on , an d cardiac su p p or t is requ ired. coid u sage. Many glu cose m an agem en t p rotocols are available. It
Most t reat m en t st rategies for TLVD in SAH are em piric. Ut ilizing is crit ical to avoid hypoglycem ia w ith p rotocol driven glucose
in ot rop ic agen t s su ch as m ilrin on e an d dobu t am in e an d judi m an agem en t . Th ere is con cer n t h at even low n or m al ser u m
cious diuret ics are first lin e th erapies. Serial ech ocardiograph ic glu cose m ay represen t crit ically low cerebral glu cose levels t h at
an d h em odyn am ic m on itoring of th ese pat ien ts is essen t ial. are clearly inju r iou s to already dam aged brain . We u t ilize a
Th e n ovel u se of in t ra aor t ic balloon p u m p (IABP) cou n ter t w o step p rotocol w it h su bcu t an eou s in su lin for m ild to m od
p u lsat ion in t h e m an agem en t of card iac failu re an d SAH w as erate hyperglycem ia an d in t raven ou s in su lin for hyperglycem ia
described in 1996.43 IABP to augm en t blood pressure m ay ben e th at is n ot con t rolled w ith su bcu t an eou s p rotocols. Protocols
fit pat ien ts suffering severe NCS in several aspects. First , IABP perm it au tom atic step u p or step dow n to m ain t ain blood glu
th erapy is effect ive in su pp or t ing m ean ar terial p ressu re in th e cose con t rol.
set t ing of card iogen ic sh ock. Secon d , IABP su p p or t s CBF an d re An em ia is com m on du ring th is ph ase of SAH, an d sign ifican t
d u ces d elayed n eu rologic d eficit s in SAH p at ien t s. Th ird , it en an em ia is associated w ith w orse clin ical outcom es. An em ia of
ables a reduct ion of catech olam in e pressor agen ts, used for HHT, p ost su rgical blood loss an d u n n eed ed p h lebotom y are m ain
th at are th e pu t at ive cau se of NCS. sou rces of an em ia. Acu te gast roin test in al blood loss from st ress
According to on e recen t outcom es st udy of 481 pat ien t s w ith gast rit is is u n com m on w it h p rop er p rop hyla xis. Oth er, m ore
SAH, TLVD associated w it h SAH in creases t h e r isk of cerebral life th reaten ing sources of bleeding require early an d aggressive
in farct ion from vasosp asm , hypoten sion , an d p u lm on ar y edem a, en doscopic m an agem en t . Hem oglobin levels are in tegral in cere
but w ith aggressive ICU suppor t does n ot affect sh or t term sur bral oxygen deliver y:
vival or fun ct ion al outcom e.41 An t ihyper ten sive m edicat ion such
Cerebral O2 Deliver y (CDO2 ) = CBF × CaO2
as th e use of sm all doses of β-blockers m ay reduce th e risk of
catech olam in e m ediated inju r y after SAH. CaO2 = (1.34 × Hb × SaO2 ) + (0.003 × PaO2 )

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490 V Cerebral and Spinal Aneurysms

w h ere CaO2 is t h e ar terial oxygen con ten t , SaO2 is th e ar terial


oxygen sat u rat ion , an d PaO2 is th e par t ial pressure of dissolved
■ Adjunctive But Unproven Therapies
oxygen . New t h erap ies to m an age DCI an d t reat cr it ical com p licat ion s
Becau se CaO2 varies sign ifican tly w ith h em oglobin (Hb) lev of SAH are em erging. Magn esiu m su lfate, stat in s, en doth elin an
els, an em ia m ay fu r th er im p air oxygen d eliver y to brain region s tagon ists, an d er yth ropoiet in , am ong oth ers, are in t riguing tools
w ith redu ced CBF an d could prom ote isch em ia.47 In discrim in ate for th e crit ical care physician in th e m an agem en t of SAH.
red blood cell t ran sfu sion , h ow ever, m ay exp ose p at ien t s to un
desirable risks w ith m argin al ben efits. Th e im m un osu pp ressive,
im m u n ogen ic, an d in fect iou s com p licat ion s w ith blood produ ct Magnesium
t ran sfu sion s sh ou ld n ot be t rivialized . A best p ract ice protocol Th e allu re of m agn esiu m th erapy in SAH stem s from th e p ath o
m ay involve m inim izing phlebotom y and procedural blood losses physiology of cerebral vasosp asm . At m u lt ip le poin t s in th e in
so that transfusion requirem ents are low er and supporting h em o flam m ator y cascade th at con t ributes to vasospasm , m agn esiu m
globin levels at a m in im u m of 8 g/dL. Expert consen sus opin ion h as a role in an tagon izing th e n et effect of vasocon st rict ion .
su p port s th e m ain ten an ce of sligh tly less rest rictive t ran sfu sion Magn esiu m in h ibit s th e Ca 2+ in flu x in to sm ooth m u scle cells of
policies in SAH com p ared w ith n on n eu rosu rgical pat ien t s.47 th e vessel an d preven t s Ca 2+ from bin ding to calm od u lin , leading
Fever is ver y com m on d u r in g t h e in ter m ed iate p er iod, oc to decreased sm ooth m uscle con t ract ion . Alth ough earlier st ud
cu rring in u p to 75% of all p at ien ts an d correlat ing w ith greater ies suggested th at m agn esium in fusion in SAH resu lted in a 20%
su barach n oid an d in t raven t ricu lar blood volu m e.48 Fever is also risk redu ct ion in “p oor ou tcom e,” a recen t m et a an alysis fou n d
associated w ith poor outcom es in SAH as w ell as a prolonged ICU lit tle ben efit overall.52 Alth ough it appears th at m agn esium m ay
cou rse. Sou rce con t rol of fever m u st alw ays occu r, an d w h en an play a role in th e m an agem en t of SAH p at ien ts, fu r th er st u dies
in fect iou s sou rce of fever is reason ably exclu ded, m an agem en t of are n eeded to clarify th at role.
fever using acetam in oph en or n on steroidals is generally effec
t ive. Passive cooling tech n iqu es su ch as fan s, ice p acks, an d cool
ing blan ket s m ay cause u n acceptable sh ivering an d un desirable Statins
sym path et ic drive in SAH pat ien ts. Invasive cooling cath eters are
Th e 3 hydroxy 3 m ethylyglu t ar yl coen zym e A redu ct ase in h ibi
effect ive at red ucing core body tem p erat u re an d are u seful in re
tor drugs, kn ow n as “stat in s,” are un dergoing con t in u ed invest i
fractory fever, but data on neurologic outcom es in SAH are lacking.
gat ion as poten t ial agen t s to reduce vasospasm an d in h ibit DCI
(Sim vast at in in An eur ysm al Subarach n oid Hem orrh age [STASH]
Late Period (More Than 14 Days) t rial). Th is t rial dem on st rated n o ben efit in sh or t term or long
term outcom e of pat ien t s.53 St at in s m ay par t icip ate by fu n ct ion
After th e early period of an eur ysm rupt ure an d stabilizat ion an d
ally in ducing n it ric oxide and in h ibit ing som e proin flam m ator y
after th e in term ediate period in w h ich th e risk of DCI h as largely
cytokin es, resu lt ing in a n europrotect ive effect u p on th e cerebral
passed, th e late p eriod begin s. It is ch aracterized by a clin ical as
vascu lat u re, en h an cing m icrovascu lar in tegrit y, an d ret arding
sessm en t of th e p at ien t’s longer term crit ical care an d reh abilita
vasocon st rict ion .54 Prospect ive st udies h ave failed to reproduce
t ive n eeds an d p rep arat ion for t ran sit ion ou t of th e ICU. Medical
th is effect .55
issu es in th e late period th at com m on ly requ ire at ten t ion in clu de
the need for long term CSF diversion due to hydrocephalus, m an
agem en t of acqu ired m edical p roblem s su ch a DVT, ongoing n u Endothelin Receptor Antagonists
t rit ion al an d resp irator y su p por t , an d th erapy n eed s.
Hydrocephalus persists into this period in 18 to 26%of patients, En doth elin s are pow erfu l vasocon st rict ing pept ides prod u ced
w ith older pat ien ts an d th ose w ith large am oun ts of in t raven prim arily in th e vascu lar en doth eliu m . En doth elin bou n d to re
t ricu lar blood at th e h igh est risk for hydrocep h alu s.49 Perm an en t ceptors resu lt s in con t ract ion of sm ooth m uscle an d st im u lat ion
CSF diversion is requ ired in th ese p at ien ts. of sodium reten t ion an d hyper ten sion , w h ich are deleteriou s in
Long term an t icoagu lat ion n eed s of t h e SAH p at ien t d u e to th e acu te set t ing of an eu r ysm al ru pt u re. En doth elin receptor an
th rom boem bolic com p licat ion s m u st be assessed du ring t h is tagon ists (ERAs) are proven th erapies for cardiac an d pu lm on ar y
period . Ven ou s th rom boem bolism occu rs in up to 50% of SAH disease an d h ave sh ow n prom ise in early st u dies of vasospasm
pat ien ts du ring th eir h ospit al cou rse.45 Clin ical dat a su p por t th e preven t ion in SAH. A recen t m eta an alysis in clu ding alm ost 900
safet y of full anticoagulation in these patients after the aneurysm p at ien t s t reated w it h ERA dem on st rated redu ct ion s in rad io
has been secured and no further invasive procedures are required.50 graph ic eviden ce of vasospasm , but again th ere w as n o differen ce
In pat ien t s diagn osed w ith addit ion al u n ru pt u red an eu r ysm s, it in pat ien t outcom es com p ared w ith con t rols,56 an d th e resu lt s of
w ould be pr u den t to con sider ven a cava filter placem en t . th e recen t CONSCIOUS 2 t rial do n ot su ppor t th eir u se.57
Cogn it ive, social, an d fu n ct ion al d eficit s abou n d in su r vivors
of SAH an d m ay persist for years despite th erapy. Kn ow ing th is,
th e crit ical care p hysician sh ou ld h ave all app rop riate reh abilit a
Erythropoietin
t ive sp ecialist s involved in t h e p at ien t ’s care by t h e late p er iod . Er yth ropoiet in (EPO) is a h igh ly glycosylated protein th at plays a
In addit ion to physical an d occu p at ion al th erapy, speech an d key role in st im u lat ion of er yth rocyte produ ct ion . Research h as
n eu rocogn it ive th erapy is required in a m ajorit y of SAH pat ien t s d em on st rated t h at EPO levels are m arked ly elevated in brain
du e to th e fact th at in st r u m en t al act ivit ies of daily living (IADLs), t issu e th at h as su stain ed isch em ic or hyp oxic dam age. Th is fact
w hich are com plex activities such as m anaging finances and h ouse h as led som e to con sider a n europrotect ive role for EPO in SAH.
keeping, are im paired in a significant portion of SAH sur vivors.51 Som e research h as sh ow n a ben eficial effect on vasosp asm an d

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41 Medical Management of Subarachnoid Hemorrhage 491

im proved ou tcom es.58 Becau se EPO crosses th e blood–brain bar tean presen tat ion com plicates th e st rategies th at th e crit ical care
rier poorly, dosing is difficu lt . physician m u st bring to th e bedsid e. Th e m edical m an agem en t
of subarach n oid h em orrh age requires th e crit ical care physician
to m ove rapidly th rough various stages of in ten sive care w ith
greatly var ying goals of care for a single p at ien t during a single
adm ission . Recogn it ion of th ese differen t ph ases of disease an d
■ Conclusion th e abilit y to sh ift th e clin ical care plan is essen t ial in th ese pa
Th e p at ien t w it h SAH m ay be d evast at in gly ill, n early asym p tients. A m ult idisciplinar y team approach w ith neurosurgical and
tom at ic, or anyw h ere on th e con t in uum in bet w een . Th is pro neurologic colleagues is m andator y to im prove patient outcom es.

References
1. Lin n FH, Rin kel GJ, Algra A, van Gijn J. In ciden ce of subarach noid h em or 19. Lu bicz B, Levivier M, Fran çois O, et al. Sixt y fou r row m u lt isect ion CT
rhage: role of region , year, an d rate of com puted tom ography: a m et a angiography for detect ion an d evalu at ion of r upt ured in t racran ial an eu
an alysis. St roke 1996;27:625–629 r ysm s: in terobser ver an d in ter tech n ique reproducibilit y. AJNR Am J Neu
2. Epidem iology of an eur ysm al subarach n oid hem orrh age in Aust ralia an d roradiol 2007;28:1949–1955
New Zealan d: in ciden ce an d case fat alit y from th e Aust ralasian Coopera 20. Rosen DS, Macd on ald RL. Su barach n oid h em or rh age grad ing scales: a
t ive Research on Subarach n oid Hem orrh age St udy (ACROSS). St roke 2000; system at ic review. Neu rocrit Care 2005;2:110–118
31:1843–1850 21. Hirai S, On o J, Yam au ra A. Clin ical grading an d ou tcom e after early sur
3. Labovit z DL, Halim AX, Bren t B, Boden Albala B, Hauser WA, Sacco RL. ger y in aneur ysm al subarach n oid h em orrh age. Neurosurger y 1996;39:
Subarachn oid hem orrhage in cidence am ong W hites, Blacks and Caribbean 441–446, discu ssion 446–447
Hispan ics: th e Nor th ern Man hat t an St udy. Neuroepidem iology 2006;26: 22. Fron tera JA, Claassen J, Sch m idt JM, et al. Pred ict ion of sym ptom at ic vaso
147–150 spasm after subarach n oid h em orrh age: the m odified fish er scale. Neuro
4. Sch w ar t z TH, Solom on RA. Perim esen ceph alic n on an eur ysm al su barach su rger y 2006;59:21–27, discu ssion 21–27
n oid h em orrh age: review of th e literat u re. Neurosurger y 1996;39:433– 23. Laffey JG, Kavan agh BP. Hyp ocapn ia. N Engl J Med 2002;347:43–53
440, discussion 440 24. Cu rley G, Kavan agh BP, Laffey JG. Hyp ocap n ia an d th e inju red brain : m ore
5. Broderick JP, Brot t TG, Duldn er JE, Tom sick T, Leach A. In it ial an d recurren t harm th an ben efit . Crit Care Med 2010;38:1348–1359
bleeding are th e m ajor causes of death follow ing subarach n oid h em or 25. Bederson JB, Con n olly ES Jr, Batjer HH, et al; Am erican Hear t Associat ion .
rh age. St roke 1994;25:1342–1347 Guidelin es for th e m anagem en t of an eur ysm al subarachnoid hem orrh age:
6. Stegm ayr B, Eriksson M, Asplund K. Declining m ortalit y from subarachnoid a statem ent for healthcare professionals from a special w riting group of the
hem orrh age: ch anges in in ciden ce an d case fat alit y from 1985 th rough Stroke Council, Am erican Heart Association. Stroke 2009;40:994–1025
2000. St roke 2004;35:2059–2063 26. Bekker A, Did ehvar S, Kim S, et al. Efficacy of clevidip in e in con t rolling
7. Huang J, van Gelder JM. Th e probabilit y of sudden death from r upt ure perioperat ive hypertension in neurosurgical patients: initial single center
of in t racranial an eur ysm s: a m et a analysis. Neurosurger y 2002;51:1101– exp erien ce. J Neu rosu rg An esth esiol 2010;22:330–335
1105, discussion 1105–1107 27. Mu toh T, Ish ikaw a T, Su zu ki A, Yasu i N. Con t in u ou s card iac ou t p u t an d
8. Mayer SA, Kreiter KT, Copelan d D, et al. Global an d dom ain specific cogn i near in frared spect roscopy m onitoring to assist in m anagem en t of sym p
t ive im pairm ent and outcom e after subarachn oid h em orrhage. Neurology tom at ic cerebral vasosp asm after su barach n oid h em orrh age. Neu rocrit
2002;59:1750–1758 Care 2010;13:331–338
9. Lovelock CE, Rin kel GJ, Roth w ell PM. Tim e t ren ds in ou tcom e of subarach 28. Bu t zku even H, Evan s AH, Pit m an A, et al. On set seizu res in dep en den tly
n oid h em orrh age: Populat ion based st udy an d system at ic review. Neu predict p oor ou tcom e after su barach n oid h em orrh age. Neu rology 2000;
rology 2010;74:1494–1501 55:1315–1320
10. Sam uels O, Webb A, Culler S, Mar t in K, Barrow D. Im pact of a dedicated 29. Lit tle AS, Kerrigan JF, McDougall CG, et al. Non convu lsive st at u s ep ilept i
n eurocrit ical care team in t reat ing pat ien t s w ith an eur ysm al subarach cus in pat ien t s suffering spon t an eous subarach n oid h em orrh age. J Neuro
n oid h em orrh age. Neurocrit Care 2011;14:334–340 su rg 2007;106:805–811
11. van Gijn J, Kerr RS, Rin kel GJ. Subarach n oid h aem orrh age. Lan cet 2007; 30. Sh eeh an JP, Polin RS, Sh eeh an JM, Baskaya MK, Kassell NF. Factors associ
369:306–318 ated w ith hydrocep h alu s after an eu r ysm al su barach n oid h em orrh age.
12. Ruigrok YM, Rin kel GJ. From GWAS to th e clin ic: risk factors for in t racra Neurosurger y 1999;45:1120–1127, discussion 1127–1128
n ial an eur ysm s. Gen om e Med 2010;2:61 31. Laidlaw JD, Siu KH. Ultra early surger y for aneur ysm al subarachn oid hem
13. van der Sch aaf IC, Velt h u is BK, Gouw A, Rin kel GJ. Ven ous drain age in orrhage: outcom es for a con secutive series of 391 pat ien ts not selected by
perim esen ceph alic h em orrh age. St roke 2004;35:1614–1618 grade or age. J Neurosurg 2002;97:250–258, discussion 247–249
14. Lin n FH, Rin kel GJ, Algra A, van Gijn J. Headach e ch aracterist ics in sub 32. St arke RM, Con n olly ES Jr; Par t icip an t s in th e In tern at ion al Mu lt i Disci
arach n oid h aem orrhage an d ben ign th u nderclap h eadach e. J Neurol Neu- plin ar y Con sen su s Con feren ce on th e Crit ical Care Man agem en t of Su b
rosurg Psych iat r y 1998;65:791–793 arach n oid Hem orrh age. Rebleeding after an eu r ysm al su barach n oid h em
15. Pin to AN, Can hao P, Ferro JM. Seizures at th e on set of subarach n oid h aem orrh age. Neurocrit Care 2011;15:241–246
orrh age. J Neurol 1996;243:161–164 33. Brilst ra EH, Algra A, Rin kel GJ, Tu lleken CA, van Gijn J. Effect iven ess of
16. Sung W, Arnaldo B, Sergio C, Julian a S, Mich el F. Terson’s syn drom e as a neurosurgical clip applicat ion in pat ien t s w ith an eu r ysm al subarach n oid
progn ost ic factor for m ort alit y of spon t an eous subarach n oid h aem or hem orrh age. J Neurosurg 2002;97:1036–1041
rh age. Act a Oph th alm ol (Copen h ) 2011;89:544–547 34. Roos YB, Rin kel GJ, Verm eu len M, Algra A, van Gijn J. An t ifibrin olyt ic th er
17. Polm ear A. Sen t in el headach es in an eur ysm al subarach n oid h aem or apy for an eu r ysm al su barach n oid h aem orrh age. Coch ran e Dat abase Syst
rh age: w h at is th e t ru e in ciden ce? A system at ic review. Cep h alalgia 2003; Rev 2003;2:CD001245
23:935–941 35. Keyrou z SG, Diringer MN. Clin ical review : preven t ion an d th erapy of va
18. Lin n FH, Wijdicks EF, van der Graaf Y, Weerdesteyn van Vliet FA, Bar telds sospasm in subarachn oid h em orrh age. Crit Care 2007;11:220
AI, van Gijn J. Prospect ive st udy of sen t in el h eadache in an eur ysm al sub 36. Lazaridis C, Naval N. Risk factors an d m edical m an agem en t of vasospasm
arach n oid h aem orrh age. Lan cet 1994;344:590–593 after su barach n oid h em orrh age. Neu rosu rg Clin N Am 2010;21:353–364

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37. Marsh all SA, Nyquist P, Ziai WC. Th e role of t ran scran ial Doppler ult raso 48. Fernandez A, Schm idt JM, Claassen J, et al. Fever after subarachnoid hem or
n ography in the diagn osis an d m an agem en t of vasospasm after an eu r ys rhage: risk factors and im pact on outcom e. Neurology 2007;68:1013–1019
m al subarach n oid h em orrh age. Neurosurg Clin N Am 2010;21:291–303 49. Dorai Z, Hyn an LS, Kopit n ik TA, Sam son D. Factors related to hydroceph a
38. Deshaies EM, Jacobsen W, Singla A, Li F, Gorji R. Brain t issue oxygen m oni lus after aneur ysm al subarach n oid hem orrh age. Neurosurger y 2003;52:
toring to assess rep erfu sion after in t ra ar terial t reat m en t of an eu r ysm al 763–769, discussion 769–771
subarach n oid h em orrh age in duced cerebral vasospasm : a ret rospect ive 50. Collen JF, Jackson JL, Sh orr AF, Moores LK. Preven t ion of ven ou s th rom
st u dy. AJNR Am J Neuroradiol 2012;33:1411–1415 boem bolism in n eurosurger y: a m et aan alysis. Ch est 2008;134:237–249
39. Muen ch E, Horn P, Bauh uf C, et al. Effect s of hyper volem ia an d hyper ten 51. Al Kh in di T, Macdon ald RL, Sch w eizer TA. Cogn it ive an d fun ct ion al out
sion on region al cerebral blood flow, in t racran ial pressure, an d brain t is com e after an eu r ysm al su barach n oid h em or rh age. St roke 2010;41:
sue oxygen at ion after subarach n oid h em orrh age. Crit Care Med 2007;35: e519–e536
1844–1851, quiz 1852 52. Wong GK, Boet R, Poon WS, et al. In t raven ous m agn esium sulph ate for
40. Rose JJ, Van h ecke TE, McCullough PA. Subarach n oid h em orrh age w ith an eur ysm al subarach n oid h em orrh age: an updated system ic review an d
neurocardiogenic stunning. Rev Cardiovasc Med 2010;11:254–263 m et a an alysis. Crit Care 2011;15:R52
41. Tem es RE, Tessitore E, Sch m idt JM, et al. Left ven t ricular dysfun ct ion an d 53. Kirkp at r ick PJ, Tu r n er CL, Sm it h C, Hu tch in son PJ, Mu r ray GD; STASH
cerebral in farct ion from vasospasm after subarach n oid h em orrh age. Neu Collaborators: Sim vast at in in an eur ysm al subarach n oid h aem orrh age
rocrit Care 2010;13:359–365 (STASH): a m u lt icen t re ran dom ised p h ase 3 t rial. Lan cet Neu rol 2014;
42. Bolli R, Marbán E. Molecular an d cellular m ech an ism s of m yocardial st un 13:666–675.
n ing. Physiol Rev 1999;79:609–634 54. Vaugh an CJ, Delan t y N. Neuroprotect ive proper t ies of st at in s in cerebral
43. Ap ostolid es PJ, Green e KA, Zabram ski JM, Fit zgerald JW, Sp et zler RF. isch em ia an d st roke. St roke 1999;30:1969–1973
In t ra aor t ic balloon pu m p coun terpulsat ion in th e m anagem en t of con 55. Kram er AH, Gurka MJ, Nath an B, Du m on t AS, Kassell NF, Bleck TP. St at in
com it an t cerebral vasosp asm an d card iac failu re after su barach n oid use w as n ot associated w ith less vasospasm or im proved outcom e after
h em orrh age: tech n ical case repor t . Neu rosu rger y 1996;38:1056–1059, subarach n oid h em orrh age. Neurosurger y 2008;62:422–427, discu ssion
discu ssion 1059–1060 427–430
44. Rabin stein AA, Bruder N. Managem en t of hyponat rem ia an d volum e con 56. Kram er A, Fletch er J. Do en doth elin receptor an t agon ist s preven t delayed
t ract ion . Neu rocrit Care 2011;15:354–360 n eurological deficit s an d poor outcom es after an eur ysm al subarachn oid
45. Ray W Z, St rom RG, Blackburn SL, Ashley W W, Sicard GA, Rich KM. In ci h em orrh age?: a m et a an alysis. St roke 2009;40:3403–3406
den ce of deep ven ou s th rom bosis after su barach n oid h em orrh age. J Neu 57. Macdon ald RL, Higash ida RT, Keller E, Mayer SA, Molyn eu x A, Raabe A,
rosurg 2009;110:1010–1014 Vajkoczy P, Wan ke I, Bach D, Frey A, Marr A, Rou x S, Kassell N. Clazo
46. Latorre JG, Ch ou SH, Nogueira RG, et al. Effect ive glycem ic con t rol w ith sen t an , an en doth elin receptor an t agon ist , in pat ien t s w ith an eur ysm al
aggressive hyp erglycem ia m an agem en t is associated w ith im proved ou t subarach n oid h aem orrh age un dergoing su rgical clipping: a ran dom ised,
com e in an eur ysm al su barach n oid h em orrh age. St roke 2009;40:1644– dou ble blin d , p lacebo con t rolled ph ase 3 t rial (CONSCIOUS 2). Lan cet
1652 Neu rol. 2011;10:618–625
47. Dh ar R, Zazulia AR, Videen TO, Zipfel GJ, Derdeyn CP, Diringer MN. Red 58. Tu rn er JD, Mam m is A, Prest igiacom o CJ. Er yt h rop oiet in for t h e t reat
blood cell t ran sfusion in creases cerebral oxygen deliver y in an em ic pa m en t of subarachn oid hem orrh age: a review. World Neurosurg 2010;73:
t ients w ith subarachnoid hem orrhage. St roke 2009;40:3039–3044 500–507

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42 Endovascular Management of
Subarachnoid Hemorrhage
Nohra Chalouhi, Pascal Jabbour, Aaron S. Dum ont, L. Fernando Gonzalez,
Robert Rosenw asser, and Stavropoula I. Tjoum akaris

En dovascu lar th erapy h as em erged as a m in im ally invasive, safe, low er risk of h em orrh age com pared w ith th ose w h o n ever u sed
an d efficien t t reat m en t for in t racran ial an eur ysm s. Ran dom ized aspirin , an d post u lated th at th is protect ive effect of aspirin stem s
con t rolled t rials h ave p resen ted firm an d convin cing eviden ce from it s an t i-in flam m ator y effect s. Mu ch w ork rem ain s to be
th at en dovascu lar an eu r ysm em bolizat ion is an effect ive t reat- don e, h ow ever, to fu lly u n derstan d th e p ath op hysiology of an eu -
m en t m odalit y for rupt ured in t racran ial an eur ysm s.1–3 Rapid r ysm form at ion an d r u pt ure.
advan ces in th e field an d developm en t of n ew tech n iques h ave Oth er cau ses of SAH in clu de ar terioven ou s m alform at ion s/
exp an ded th e spect ru m of an eu r ysm s am en able to en dovascu lar fist ulas, t raum a, vasculit is, in t racran ial ar terial dissect ion s, am y-
t reat m en t . loid angiopathy, an d bleeding diath eses. Ar terioven ous m alfor-
m at ion s are t h e lead in g cau se of in t racerebral h em or rh age in
t h e you ng p opu lat ion an d accou n t for 9% of all cases of SAH.8
Dural ar terioven ous fist ulas m ay presen t w ith subarach n oid or
■ Pathophysiology of Aneurysmal lobar h em orrh ages especially in th e presen ce of cor t ical ven ou s
drain age (Borden t ypes II an d III, Cogn ard t yp es IIb to IV). En do-
Subarachnoid Hemorrhage vascu lar th erapy h as becom e an im por t an t tech n ique for ar terio-
Th e in ciden ce of an eu r ysm al su barach n oid h em orrh age (SAH) ven ou s m alform at ion s an d fist ula t reat m en t eith er as a single
ranges from 2 to 16 per 100,000.4 Fem ale sex, sm oking, hyp er- or m u lt im odalit y ap p roach . Recen t ly, t h e in t rod u ct ion of Onyx
ten sion , excessive alcoh ol con su m pt ion , an d cocain e abuse are (ev3, Ir vin e, CA) h as ad d ed an im p or t an t elem en t to t h e en d o -
im por t an t risk factors for SAH.5 A h istor y of previous SAH an d a vascular arm am en tarium an d revolut ion ized th e t reat m en t of
fam ily h istor y of an eur ysm s or SAH are addit ion al risk factors. th ese lesion s. Several invest igators h ave rep or ted rem arkably
Th e risk of SAH in creases su bst an t ially w ith th e n u m ber of af- h igh cure rates w ith th is em bolic agen t , w ith a h igh propor t ion
fected first-degree relat ives.6 In a p opu lat ion based case-con t rol of t reat m en ts com pleted in a single session .12 Th is ch apter dis-
st u dy, th e odds rat io of SAH w as 2.15 for in dividu als w ith on e cusses th e diagn osis an d en dovascular m an agem en t of an eur ys-
affected first-degree relat ive an d as h igh as 51 for th ose w ith t w o m al SAH.
affected first-degree relat ives.7 Th e risk of SAH is in creased by
th e p resen ce of sym ptom at ic, large (> 7 m m ), an d p oster ior cir-
cu lat ion an eu r ysm s as w ell as cer t ain gen et ic syn d rom es, su ch
as au tosom al dom in an t polycystic kidn ey disease, t ype IV Eh lers-
Dan los syn drom e, an d fibrom u scu lar dysp lasia.6,8 Act ivit ies p re-
■ Clinical Presentation
ced ing SAH, su ch as p hysical exercise, sexu al in tercou rse, or Th e su dden in crease in in t racran ial pressu re an d sym path et ic
st rain ing are repor ted in on ly 20% of cases.9 outflow at th e t im e of r upt ure m ay cause im m ediate death in 10
An eur ysm s arise m ost com m on ly at sites of ar terial bran ch - to 15% of all pat ien t s.13 Th e m ost ch aracterist ic sym ptom of SAH
ing, usu ally w ith in t h e circle of Willis it self or at a n earby bran ch - in th e aw ake pat ien t is th e com plain t of “th e w orst h eadach e of
in g p oin t , w h ere excessive h em odyn am ic st resses are exer ted m y life.” Th e h eadach e is usually d escribed as ext rem ely sudden
on ar terial w alls. Eviden ce suggest s th at in flam m at ion is a key an d im m ediately reach ing m axim al in ten sit y. A sen t in el h ead-
m ech an ism in th e form at ion an d rupt ure of in t racran ial an eu- ach e due to a m in or leak m ay precede an eur ysm rupt ure in 10 to
r ysm s.10 An eu r ysm form at ion begin s w ith a h em odyn am ically 43% of pat ien ts.13 Most pat ien ts w ith SAH also h ave depressed
in du ced en doth elial dysfu n ct ion follow ed by th e develop m en t of level of con sciou sn ess (65%) an d n au sea or vom it ing (77%) on
an inflam m ator y reaction w ith resultant w eakening of the tunica ad m ission . Nu ch al r igid it y (35%) m ay t ake u p to 12 h ou rs to ap -
m edia and expan sion of th e vessel w all. Furth er in flam m at ion , p ear an d m igh t n ot develop at all in com atose p at ien t s or in
vessel w all degen erat ion , an d cell death ult im ately culm in ate in th ose w ith m in or h em orrh ages. Cran ial n er ve com pression , p a-
an eur ysm rupt u re. Several th erapies th at t arget th e in flam m a- ren chym al h em atom a, or focal isch em ia m ay lead to focal n euro-
tor y respon se, in clu ding n uclear factor-kappa B in h ibitors an d logic deficits. Despite th e classic p resen t at ion of SAH, u p to 12%
m at rix m et alloprotein ases in h ibitors, appear to at ten uate an eu - of pat ien t s are in itially m isdiagn osed due to in correct evaluat ion
r ysm form at ion an d p rogression in an im al m od els of cerebral of th e h eadach e characterist ics, failure to obtain a com pu ted to-
an eu r ysm s.10 In a recen t case-con t rol st u dy from su bject s en - m ograp hy (CT) scan of th e h ead, failu re to p erform lu m bar pu n c-
rolled in t h e In ter n at ion al St u dy of Un r u pt u red In t racran ial t u re, or in correct in terp ret at ion of cerebrosp in al flu id fin dings.14
An eu r ysm s, Hasan et al11 foun d th at pat ien t s w ith un r upt ured Because m isdiagnosis is associated w ith increased m orbidit y an d
an eur ysm s w h o used aspirin at least th ree t im es w eekly h ad a m or talit y, clin ician s sh ou ld m ain tain a h igh level of suspicion for

493

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494 V Cerebral and Spinal Aneurysms

SAH an d a low th resh old for obtain ing a h ead CT in pat ien t s w ith
acu te on set of severe h eadach e.
■ Endovascular Treatment of
Ruptured Aneurysms
Random ized controlled trials have sh ow n that endovascular coil-
ing is the preferred treatm ent m odalit y for patients w ith ruptured
■ Perioperative Evaluation in t racran ial an eu r ysm s.1–3,23 Th e In tern at ion al Su barach n oid
If SAH is suspected based on presen t ing sign s an d sym ptom s, a An eu r ysm Tr ial (ISAT) en rolled 2,143 p at ien t s w it h r u pt u red
n on con t rast h ead CT sh ou ld be th e first invest igat ion . Th e sen si- in t racran ial an eu r ysm s across 42 n eu rosu rgical cen ters, m ostly
t ivit y of h ead CT is m a xim al (> 95%) in t h e first 3 days follow - in Europe, an d ran dom ly assign ed th em to m icrosu rgical clip -
in g SAH, after w h ich it decreases sign ifican tly as blood in th e ping (n = 1,070) or en dovascu lar coiling (n = 1,073).2 On ly pa-
su barach n oid sp ace recircu lates an d get s reabsorbed. A lu m bar t ien ts w ith an eur ysm s th at w ere ju dged to be suitable for eith er
pun ct u re, th erefore, is n ecessar y to detect xan th och rom ia in p a- tech n ique w ere en rolled in th e t rial. Th e prim ar y outcom e w as
t ien ts w ith clin ical su sp icion of an SAH an d a n egat ive CT scan . th e risk of death or d ep en den cy at 1 year, an d secon dar y ou t-
Xan th och rom ia m ay be presen t as early as 6 h ours after bleeding com es in clu ded th e risk of seizu res an d th e risk of reh em orrh age.
an d is usu ally invariably seen after 12 h ours.15 It is assessed by After 1 year of follow -u p, th ere w as a 22.6% relat ive risk reduc-
visu al in spect ion an d gen erally con firm ed by spect rop h otom e- t ion in depen den cy or death w ith en d ovascular th erapy as com -
t r y. Alth ough rarely u sed in clin ical pract ice, m agn et ic reson an ce pared w ith m icrosu rger y, a fin ding likely at t ribut able to th e
im aging (MRI)—gradien t ech o, flu id-at ten uated inversion recov- low er rate of procedu ral com p licat ion s in th e coiling (8%) versus
er y, proton den sit y, an d diffusion -w eigh ted im aging—can en able th e clipp ing grou p (19%). Th e risk of ep ilep sy w as su bst an t ially
th e diagn osis of SAH in pat ien t s w ith a n egat ive CT scan , th u s low er in p at ien ts allocated to en dovascu lar t reat m en t, bu t th e
obviat ing th e n eed for lu m bar pun ct ure. MRI is as sen sit ive as CT risk of late rebleeding w as h igh er (2.9%after en dovascular repair
in th e early period after SAH an d m ore sen sit ive th an CT w h en vs 0.9% after op en su rger y). Crit icism of th e st u dy focused on a
scan n ing is p erform ed several days after SAH.16 poten t ial “ch err y-p icking” bias becau se 80% of th e p at ien t s w h o
Digital subtraction angiography (DSA) w ith three-dim ensional w ere in it ially screen ed w ere even t ually excluded (7,416/9,559)
rotat ion al angiograp hy is th e gold stan dard to iden t ify th e pres- from th e t rial. Also qu est ion s w ere raised abou t th e variable level
en ce of an an eu r ysm in p at ien t s w ith SAH, defin e it s an atom ic of exp er t ise of t h e p ar t icip at in g n eu rosu rgeon s (som e w it h
feat ures, an d determ in e w h eth er it is am en able to en dovascu lar lim ited vascular experien ce) an d en dovascu lar specialist s. In a
em bolizat ion . DSA h as th e h igh est diagn ost ic accu racy an d can follow -up repor t of th e ISAT, th e sur vival ben efit w ith en dovas-
be p erform ed w ith ver y low com plicat ion rates (< 1%).17 In m ost cular th erapy rem ain ed sign ifican t after 5 years, although th e
n eu rovascular cen ters, DSA is th e diagn ost ic m odalit y of ch oice propor t ion of in depen den t pat ien ts am ong su r vivors did n ot dif-
in p at ien t s w ith SAH for an eu r ysm detect ion , ch aracterizat ion , fer bet w een th e t w o group s.24
an d possibly en dovascular em bolizat ion . Never th eless, CT angi- Th e Barrow Ru pt u red An eu r ysm Trial (BRAT) is a p rospect ive
ography (CTA) h as h igh diagn ost ic accuracy in th e detect ion of ran dom ized con t rolled t rial w ith an in ten t-to-t reat design th at
in t racran ial an eur ysm s an d h as rep laced DSA in m any cen ters as com pared en dovascu lar coiling an d su rgical clipp ing in p at ien t s
th e in it ial vascu lar im aging m eth od for p at ien t s w ith SAH.18 w ith r upt ured an eur ysm s.1 In respon se to th e sh or tcom ings of
How ever, th e sen sit ivit y of CTA in th e d etect ion of ver y sm all th e ISAT, th e BRAT invest igators in clu d ed all pat ien t s w ith SAH
an eur ysm s (< 3 m m ) is st ill low er th an DSA.19,20 As su ch , m ost adm it ted during th e st u dy period. Treat m en t w as perform ed by
auth orit ies st ill recom m en d perform ing a DSA if CTA is n egat ive, exp erien ced an d h igh ly skilled vascu lar an d en dovascu lar n eu ro-
except p erh aps in pat ien ts w ith perim esen cep h alic SAH.13 su rgeon s. A total of 472 p atien t s w ere en rolled an d assign ed to
Th e clin ical severit y of SAH on presen t at ion sh ou ld be deter- an eu r ysm clip p ing (n = 239) or coil em bolizat ion (n = 233). As
m in ed by t h e u se of sim p le validated scales su ch as th e Hu n t in t h e ISAT, p oor ou tcom es at 1 year in t h e BRAT w ere fou n d to
an d Hess scale or th e World Federat ion of Neu rological Societ ies be less com m on in pat ien ts treated w ith en dovascu lar t reat m en t
scale, both of w h ich are reliable predictors of pat ien t ou tcom e. (23.2% vs 33.7%). Alth ough t reat m en t d u rabilit y w as a sign ifi-
Initial care should be focused on m anaging early neurologic com - can t con cern in th e ISAT, n o p at ien t in th e BRAT experien ced a
plicat ion s an d p reven t ing reh em orrh age. Acu te hydroceph alu s is rebleeding episode after endovascular therapy. This im provem ent
m an aged by extern al ven t ricular drain age an d usually result s in in en dovascular t reat m en t efficacy is likely th e resu lt of recen t
sign ifican t n eu rologic im p rovem en t . Th e risk of early an eu r ysm advan ces an d refin em en t s in em bolizat ion tech n iques. More re-
reh em orrh age is h igh (4 to 13.6% of p at ien ts w ith in th e first 24 cen tly, th e 3-year follow -up from th e BRAT revealed equipoise
h ours) an d results in death or severe disabilit y in 80% of pa- bet w een m icrosurgical clipping an d en dovascular th erapy for
tients.21 Aneur ysm s, therefore, should be urgently secured by en- an terior circu lat ion an eur ysm s.25 Th e pat ien ts t reated w ith m i-
dovascular or m icrosu rgical m ean s, preferably w ith in 24 h ou rs. crosurgical clipping had a significantly higher degree of aneurysm
It is also recom m ended to m ain tain systolic blood pressure below obliterat ion an d a sign ifican tly low er rate of recurren ce an d re-
160 m m Hg to reduce the risk of rebleeding until aneurysm oblit- t reat m en t as com pared w ith th e en dovascular group .
erat ion had been ach ieved. An t ifibrin olyt ic dr ugs such as am in o- Th e best t reat m en t m odalit y for p at ien t s w ith sm all r u pt u red
cap roic acid can h elp p reven t rebleeding, bu t a n et ben efit in th e an eur ysm s rem ain s u n clear. Th e ISAT invest igators excluded all
overall fun ct ion al outcom e h as n ot been dem on st rated.22 In th e pat ien ts w ith sm all an eu r ysm s from th eir st u dy an d th e BRAT
absen ce of con t rain dicat ion s, sh or t-term (< 72 h our) u se of th ese invest igators assign ed t h ese pat ien t s preferen t ially to th e su rgi-
drugs m ay be con sidered in pat ien ts w ith a h igh risk of reh em or- cal arm . Sm all an eu r ysm s pose sign ifican t tech n ical ch allenges
rh age an d an u n avoidable delay in an eu r ysm obliterat ion . to en dovascular th erapy due to difficu lt ies in cath eterizing th e

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42 Endovascular Management of Subarachnoid Hemorrhage 495

an eu r ysm , st abilizing t h e m icrocat h eter, an d safely d ep loying 24 to 35% for p osterior circu lat ion an eu r ysm s, 18 to 32% for
coils. Several authors have reported a h igh risk of intraprocedural m id dle cerebral ar ter y an eu r ysm s, 37% for posterior com m u n i-
rupt ure w ith coiling of sm all an eur ysm s.26 For th ese reason s, cat ing ar ter y an eu r ysm s, 25%for an terior com m u n icat ing arter y
su rgical clip ping h as been con sidered to be th e p referred t reat- an eu r ysm s, 26% for carot id op h t h alm ic ar ter y an eu r ysm s, 40%
m en t for th ese lesion s. We h ave recen tly com pared su rgical an d for caver n ou s an eu r ysm s, an d 12 to 29% for p araclin oid an eu -
en d ovascu lar opt ion s in 151 p at ien t s w ith sm all rupt u red an eu - r ysm s.33 Th e Cerebral An eu r ysm Rer u pt u re After Treat m en t
r ysm s t reated at our in st it u t ion (91 w ith endovascular th erapy (CARAT) st udy iden t ified th e degree of an eur ysm occlusion after
an d 60 w ith surgical clipping).27 We foun d a sign ifican tly low er in it ial coiling as a st rong predictor of su bsequen t h em orrh age,
rate of procedural com plication s w ith endovascular therapy (9.8%) prom pt ing an em p h asis on ach ieving bet ter in it ial an eu r ysm oc-
com pared w ith op en su rger y (23.3%). Im por t an tly, on ly 3.7% of clu sion . Th e u se of sten t ing an d balloon rem odeling tech n iqu es
pat ien ts experien ced an in t rap rocedu ral an eu r ysm r upt u re du r- yields h igh er degrees of an eu r ysm occlu sion an d im p roves t reat-
ing en dovascu lar t reat m en t . Th ese fin dings in d icate th at en do- m en t durabilit y.32,34,35 Fu t ure advan ces an d refin em en t s in en do-
vascu lar th erapy, if tech n ically feasible, m ay ser ve as a t reat m en t vascu lar devices w ill fur th er im prove th e long-term efficacy of
altern at ive for sm all r upt ured aneu r ysm s, alth ough ran dom ized en d ovascu lar th erapy. Despite prom ising early results, th e re-
con t rolled t rials are requ ired to provide defin it ive in form at ion cen tly publish ed Cerecyte coil t rial sh ow ed th at bioact ive coils
on th e best th erapeu t ic approach . do n ot con fer any ben efit in term s of angiograp h ic ou tcom e com -
Th e ch oice bet w een su rgical an d en d ovascu lar opt ion s for th e pared w ith bare plat inum coils.36
t reat m en t of SAH sh ou ld t ake in to con siderat ion several factors,
in clu ding an eu r ysm locat ion , con figu rat ion , clin ical grade. an d
m edical com orbidit ies. Middle cerebral arter y an eur ysm s pose
sign ifican t tech n ical ch allenges to en dovascu lar coiling an d, in ■ Endovascular Techniques
th is par t icu lar locat ion , su rgical clip ping p rovides m ore favor-
able result s.13 Pat ien t s w ith a large in t rap aren chym al h em atom a
Aneurysm Coiling
sh ou ld u n dergo open su rger y for an eu r ysm clipp ing an d sim u l- In ou r in st it u t ion , all p at ien t s w it h SAH u n d ergo ar ter ial lin e
tan eous clot evacuat ion an d decom pression . It sh ou ld be n oted an d cen t ral ven ou s lin e p lacem en t preoperat ively. Pat ien ts w ith
that in selected patien ts w ith an eur ysm al SAH an d associated in- Hu n t an d Hess grade III or h igh er also are m on itored w ith ven -
t raparen chym al h em atom a, en dovascu lar an eu r ysm obliterat ion triculostom y and Sw an-Gan z cath eters. En dovascular procedures
prior to su rgical decom p ression is also an acceptable altern at ive are perform ed un der gen eral en dot rach eal an esth esia an d con -
th at can sim plify open su rger y for h em atom a evacu at ion an d de- t in u ou s n eu rophysiological m on itoring, in clu ding som atosen -
com pression .28 In gen eral, surgical clipping is preferred in young sor y evoked poten t ials an d elect roen cep h alography. Brain stem
pat ien ts becau se of its long-term durabilit y. Th e auth ors of th e auditor y-evoked respon ses are also m on itored in posterior cir-
ISAT n oted th at th e advan tage of coiling over surgical clipping is culat ion an d posterior com m un icat ing arter y an eur ysm s. Th e
lower in patients < 50 years of age than it is for those ≥ 50 years of goals of an esth esia m an agem en t in clu de h em odyn am ic con t rol
age. The study concluded that th e long-term protection from SAH to m in im ize t h e r isk of reh em or rh age, in t racran ial p ressu re
afforded by surgical clipping could give th is t reat m en t m odalit y con t rol, an d paralyzing th e p at ien t to opt im ize im age qu alit y
an advantage in life expectancy over coiling for young patients.29 an d procedure accuracy. An t icoagulat ion w ith h eparin in fusion
In a recen t st udy, w e perform ed an analysis on a series of young to preven t th rom boem bolic even ts is u sed based on physician
patien ts (age < 35 years) w ith SAH t reated at our in st it ut ion an d discret ion . Gen erally, a h alf bolus of h eparin (50 un its/kg) is ad-
foun d th at en dovascular th erapy provides adequate protect ion m in istered follow ing deploym en t of th e first coil. Th e presen ce
again st reh em or rh age an d resu lt s in favorable ou tcom es in u p of an in t raparen chym al h em atom a or recen t ven t ricu lostom y
to 85%of cases.30 Conversely, elderly pat ien t s an d th ose p resen t- placem en t (w ith in th e previou s 2 h ou rs) lim its th e u se of in tra-
ing w ith poor n eurologic grades (Hu n t an d Hess grades IV an d V) operat ive an t icoagu lat ion .
are m ore likely to ben efit from an en dovascular procedure.13 In Ar terial access is obt ain ed th rough fem oral pun ct ure by use of
our in st it ut ion , Hun t an d Hess grade V pat ien t s are gen erally th e Seldinger tech n iqu e, an d an ar terial sh eath is in ser ted an d
con sidered for en d ovascu lar m an agem en t on ly follow ing clin ical secu red w ith a st itch . Typically a 7-Fren ch (F) diam eter sh eath
im provem en t w ith p lacem en t of ven t ricu lostom y. Pat ien ts w ith is u t ilized in m ost cases. Th e gu iding cath eter (t ypically a 6F) is
m ultiple m edical com orbidities, bleeding diathesis, or throm botic in t roduced an d n avigated in to each st udied vessel w ith th e aid of
disease requ iring ch ron ic an t icoagu lat ion are also con sidered for a guidew ire. A six-vessel angiogram , in cluding bilateral extern al
en dovascu lar t reat m en t . Likew ise, for basilar t ip an eu r ysm s, en - carot id, in tern al carot id, an d ver tebral ar teries is requ ired w h en
dovascu lar th erapy h as yielded m ore favorable resu lts th an m i- th e sou rce of SAH locat ion is u n clear. Th ree-dim en sion al (3D)
crosu rger y.31 In our in st it ut ion , posterior circulat ion an eur ysm s, angiography en ables precise m easurem en ts of th e an eur ysm
in gen eral, an d basilar t ip an eu r ysm s, in p art icular, are alm ost size an d dom e-to-n eck rat io w ith accu rate dep ict ion of th e an -
alw ays t reated by en dovascu lar m ean s.32 Pat ien t s w ith m u lt iple eu r ysm n eck an d it s relat ion to p aren t an d bran ch ing vessels.
in t racran ial an eur ysm s an d u n kn ow n source of bleeding sh ou ld An eur ysm s w ith a sm all n eck (< 4 m m ) an d a favorable dom e-to-
also be con sidered for th is ap p roach . Fin ally, th e presen ce of sig- n eck rat io (≥ 2) can u sually be coiled w ith out sten t or balloon
n ifican t vasospasm , m oderate ath erosclerosis, an d tor t u osit y of assist an ce. Th e 3D recon st ruct ion facilitates opt im al w orking
proxim al vessels is u su ally a con t rain dicat ion to en dovascu lar biplan e project ion s for an eur ysm t reat m en t . Th rough th e gu id-
t reat m en t . ing cath eter, a m icrocath eter is advan ced over a m icroguidew ire
Treat m en t du rabilit y h as been th e m ajor con cern w ith en do- and subsequently placed in the aneur ysm lum en, preferably aw ay
vascu lar t reat m en t of cerebral an eur ysm s. Th e recurren ce rate is from the n eck. The m icrocath eters of our choice are SL-10 (Boston

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496 V Cerebral and Spinal Aneurysms

a b

c d

Fig. 42.1a–d A three-dim ensional (3D) reconstruction (a) and lateral view (SAH). The aneurysm was successfully em bolized with coils. Lateral views
(b) of digital subtraction angiography (DSA) showing a 5.5-m m carotid of the initial (c) and 6-m onth follow-up (d) angiogram s demonstrate 100%
ophthalm ic artery aneurysm in a patient with subarachnoid hem orrhage occlusion of the aneurysm .

Scien t ific, Nat ick, MA) an d Ech elon (ev3). Th e lat ter is p referred arin in conju n ct ion w ith th e u se of an t ip latelet agen t s in sten t
for cases requiring coiling an d/or liquid em bolizat ion w ith Onyx. placem en t procedu res. In our experien ce, th e first an d th e last
The m icroguidew ires of our choice are Synchro-2 and Synchro-10 coil play a key role in m in im izing th e occurren ce of th rom boem -
(Boston Scien t ific) for sm all an eu r ysm s. Next , coils are deployed bolic even t s. Th e first coil sh ou ld be placed w ith as few at tem pt s
un der direct angiograph ic guidan ce (Fig. 42.1). Th e m ean arterial as p ossible to m in im ize th e risk of disr u pt ing any fresh th rom bu s
pressu re is low ered by 15 to 20%du ring coil dep loym en t . Coils of w ith in th e an eu r ysm or on th e coil it self. Th e fin al coil p laced
var ying sh apes (h elical, sph erical), length s (1–30 m m ), diam e- sh ould p rovide adequate an eu r ysm occlu sion w ith out causing
ters, softn ess, an d design (bioact ive versu s bare plat in um ) are coil h ern iat ion in to th e paren t vessel, because th is creates a
available. Th e in it ial coil is usu ally com plex-sh aped an d fills th e th rom bogen ic su rface for delayed th rom boem bolic even t s. In th e
an eur ysm in a basket-like con figurat ion . On ce opt im al posit ion - even t of coil h ern iat ion in to th e paren t vessel du ring u n r u pt u red
ing is achieved, th e coil is det ach ed. Addit ion al coils of progres- cases, h eparin is adm in istered for 12 h ours w ith 24- to 48-h our
sively decreasing size and variable shapes are then deployed until dext ran in fusion an d at least 6 w eeks of single or dual an t ip late-
com plete an eu r ysm obliterat ion is ach ieved (i.e., n o an eu r ysm let th erapy. Cer tain ly, in th e set t ing of SAH, an t icoagulat ion an d
filling is n oted in at least th ree dist in ct biplan e view s an d un der an t iplatelet th erapies are used sparingly, an d th e risk/ben efit
n orm al blood pressu re). Th e last “fin ish ing” coils are u sually h e- rat io sh ou ld be carefu lly assessed . Th ese t h erap ies are m ore
lical sh aped to allow for bet ter filling of th e residu al an eu r ysm . com m on ly u t ilized in t h e set t ing of t h rom boem bolic even t s in
Follow ing an eu r ysm obliterat ion th e m ean ar terial p ressu re is low Hu n t an d Hess an d Fish er grad e p at ien t s. If a m ajor t h rom -
m ain tained at bet w een 90 an d 100 m m Hg to preven t vasospasm boem bolic com p licat ion an d vessel occlu sion is recogn ized in -
an d th rom boem bolic even t s. t rap roced u rally, t h e an eu r ysm sh ou ld be rap id ly em bolized
an d secu red follow ed by in t ra-ar ter ial t h rom bolysis, w it h m e-
ch an ical or ch em ical th rom bectom y. Th e m ost com m on ly used
Thromboembolism
throm bolytic agents include tissue plasm inogen activator and gly-
Th rom boem bolic com p licat ion s are a m ajor con cern du ring en - coprotein s IIb/IIIa in h ibitors (t irofiban , abcixim ab, an d ept ifiba-
dovascu lar an eu r ysm t reat m en t . With h igh ly sen sit ive im aging t ide). Th e lat ter group is in creasingly u sed both as a prophylact ic
st u d ies like d iffu sion -w eigh ted MRI, t h rom boem bolic even t s t reat m en t an d as a rescue th erapy for th rom boem bolic even t s
can be detected in as m any as 60% of en dovascu lar procedu res occu rring in t rap rocedu rally.38
despite system ic anticoagulat ion.37 Stent-assisted procedures are
par t icu larly pron e to su ch even t s given th e th rom bogen icit y of
Aneurysm Rupture
en dovascular sten ts and the difficulties associated w ith the treat-
m en t of large an d w ide-n ecked an eu r ysm s. Avoidan ce of su ch In t raprocedural an eur ysm ru pt u re is a poten t ially devastat ing
com plications requires careful m onitoring of the response to h ep - com p licat ion (20%m or t alit y rate) th at occu rs in 2 to 8%of coiling

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42 Endovascular Management of Subarachnoid Hemorrhage 497

p roced u res d u r in g in t rod u ct ion of t h e m icrogu id ew ire or m i- ventriculostom y placem ent, aneur ysm al rebleeding, and possible
crocat h eter in to t h e an eu r ysm an d d u ring coil d ep loym en t .39 n eed for fu t u re invasive p roced u res. In ou r exp er ien ce, sten t-
Sm aller an d ru pt u red an eu r ysm s h ave a h igh risk of in t rap roce- assisted coiling of acu tely r u pt u red an eu r ysm s car r ies an ac-
du ral ru pt u re. With p rop er tech n iqu e, th e occu rren ce of th is cept able r isk of p er iop erat ive com p licat ion s (15%) an d yield s
com plicat ion can be m in im ized. To avoid u n con t rolled advan ce- favorable ou tcom es in as m any as 63% of pat ien t s.40 Likew ise, in
m en t of th e m icrocath eter, th e in ter ven t ion alist sh ould en sure a recen t system at ic review of th e literat ure, Bodily et al41 fou n d
th at n o for w ard pressu re is ap p lied to t h e m icrocath eter before th at th rom boem bolic com p licat ion s w ere reason ably w ell con -
en tering t h e an eu r ysm an d rem ove th e gu idew ire slow ly u n d er t rolled, an d ven t ricu lostom y-related h em orrh agic com p licat ion s
direct flu oroscopic con t rol. To m in im ize ten sion again st an eu - w ere un com m on after sten t-assisted coiling of acutely rupt ured
r ysm w all, th e first coil sh ou ld preferably be soft , hydroph ilic, an eur ysm s. Oth ers, h ow ever, h ave en coun tered h igh m or t alit y
an d un dersized by 1 to 2 m m w ith respect to th e m axim al diam - rates w ith stenting of ruptured aneurysm s and recom m ended such
eter of t h e an eu r ysm . An eu r ysm overp acking in creases ten sion an approach only w hen less risky options have been excluded.13,42
in th e fu n du s an d in creases th e r isk of r u pt u re an d sh ou ld be For sten t-assisted p rocedu res p erform ed in th e set t ing of SAH
avoided. W h en an eur ysm perforat ion occurs, h eparin sh ould be at ou r in st it u t ion , p at ien t s are loaded w ith 600 m g clop idogrel
im m ediately reversed w ith p rot am in e, an d th e offen ding agen t in t rap rocedu rally an d a 50-U/kg h eparin bolus after deploym en t
left in place becau se it act s as a tem p orar y p lug at th e perfora- of th e first coil, w ith m ain ten an ce of daily doses of clopidogrel
t ion site. W h en p erforat ion occu rs w ith th e m icrocath eter, th e (75 m g) an d aspirin (81 m g) for 6 w eeks follow ing th e in ter ven -
first coil is deployed in th e subarach n oid space to occlude th e t ion . Tw o t yp es of sten ts are cu rren tly available for u se in th e
perforat ion site, an d th e m icrocath eter is th en p u lled back, w ith Un ited St ates: th e Neuroform (St r yker Neurovascular, Frem on t ,
su bsequ en t p lacem en t of addit ion al coils u n t il th e an eu r ysm is CA) an d th e En terprise (Cordis Neurovascular, Miam i, FL). Sten t-
obliterated. If r upt ure occurs during coil placem en t , coil detach - assisted coiling is usually perform ed in on e of th ree w ays: (1) th e
m en t an d rapid deliver y of addit ion al coils is th e m an agem en t of sten t is in it ially deployed follow ed by coil em bolizat ion th rough
ch oice. In th e set t ing of u n con t rolled an eu r ysm r u pt u re, a bal- th e st ru t s of th e sten t; (2) th e coil m icrocath eter is p osit ion ed
loon , su ch as Hyperglide (ev3) sh ou ld be qu ickly in t roduced an d w ith in th e an eur ysm before sten t deploym en t , an d an eur ysm
in flated across th e n eck of th e an eu r ysm to con t rol th e h em or- coiling p roceeds above th e sten t (“jailing tech n iqu e”); or (3) th e
rhage. The balloon is deflated once aneurysm coiling is com plete. sten t is placed after coiling to p reven t an t icip ated coil h ern iat ion
in to th e paren t vessel or to secu re a h ern iated coil. Th e ch oice
b et w e e n t h ese m et h od s m ay d e p e n d on t h e in t e r ve n t ion ist ’s
Stent-Assisted Techniques exp e r ie n ce a n d t h e va scu la r a n at om y a n d vessel t or t u osit y. In
Fusiform , w ide-necked, and m orphologically com plex aneurysm s ou r exp er ien ce, t h e jailing tech n iqu e p rovid es greater m icro -
pose sign ifican t ch allenges to conven t ion al coiling. Su ch an eu - cath eter st abilit y du ring coil dep loym en t an d redu ces th e likeli-
r ysm s w ere previously referred for surgical clipping. With th e h ood of coil h ern iat ion . In addit ion , an eur ysm m icrocath eteriza-
adven t of sten t tech n ology, com p lex an eu r ysm s are n ow am e- t ion is m ore ch allenging follow ing sten t dep loym en t , especially
n able to en d ovascu lar t reat m en t (Fig. 42.2). Most clin ician s, for closed-cell d esign sten ts an d sm all an eur ysm s.
h ow ever, are relu ct an t to p er for m sten t -assisted coilin g in t h e Th e u se of a sten t en ables den ser an eu r ysm p acking by pro-
set t ing of SAH becau se of t h e n eed for d u al an t ip latelet t h er- viding a scaffold for coils an d im proving n eck coverage. Also, th e
apy an d th e poten t ial for h em orrh agic com plicat ion s related to grow th of fibrocellu lar t issue over th e sten ted segm en t form s a

a b c

Fig. 42.2a–c (a) A 3D reconstruction of digital subtraction angiography deployed from the left P1 into the upper third of the basilar trunk followed
(DSA) demonstrating a 3-mm wide-necked basilar tip aneurysm in a patient by coil em bolization of the aneurysm . (c) Frontal view of DSA dem onstrates
with grade IV subarachnoid hem orrhage (SAH). (b) A Neuroform stent was adequate aneurysm occlusion after 15 m onths.

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498 V Cerebral and Spinal Aneurysms

n eoin t im al scaffold at th e an eur ysm n eck an d redirect s blood vessel. How ever, in a m ult icen ter Fren ch st udy th at com pared
flow along th e p aren t ar ter y, th u s prom ot ing in t ra-an eur ysm al 160 rupt ured an eur ysm s t reated w ith balloon rem odeling to 608
st asis an d th rom bosis. Accordingly, sten t-coiled an eur ysm s h ave an eur ysm s t reated w ith conven t ion al coiling, Pierot et al34 fou n d
h igh er follow -up occlusion rates th an th ose t reated w ith conven - sim ilar rates of procedural com plicat ions bet w een the t w o groups,
t ion al coiling.35 in cluding th rom boem bolic even t s an d in t raprocedural rupt ures,
Recen tly, en dolu m in al vessel recon st ru ct ion w ith th e Pipelin e along w ith h igh er occlusion rates in th e rem odeling group. In ad-
Em bolizat ion Device (PED) (ev3) h as em erged as a safe an d effi- dit ion , Sh ap iro et al44 p erform ed a literat u re review th at in clu ded
cient t reat m en t for w ide-n ecked, gian t , blister, an d fusiform in - 23 st udies an d 1,163 procedu res (273 balloon -assisted proce-
t racran ial an eu r ysm s. How ever, th e device sh ou ld be u sed ver y du res) an d fou n d th e sam e rate of th rom boem bolic com p lica-
caut iou sly in th e set t ing of SAH becau se an eu r ysm occlu sion is t ion s in balloon -assisted coiling as in u n assisted coiling. Balloon
t ypically delayed. Th is m ay exp ose th e pat ien t to a sign ifican t assist an ce is preferred over sten t assistan ce in th e acute ph ase of
risk of rebleeding, especially because strict dual antiplatelet ther- SAH by m any in ter ven t ion ists because it obviates th e n eed for
apy is also required in th e acu te set t ing. Fu r th erm ore, th e h igh an t iplatelet th erapy an d poten t ial h em orrh agic com plicat ion s.
th rom bogen icit y of th e PED p oses addit ion al risk in SAH p at ien t s Also, in th e even t of in t raoperat ive an eur ysm perforat ion during
w ho t ypically h ave n ot been pret reated w ith an t iplatelet th erapy coilin g, balloon in flat ion isolates t h e an eu r ysm from t h e circu -
to reach a th erapeut ic respon se. McAuliffe an d Wen deroth 43 lat ion an d , t h u s, m in im izes in t racerebral h em or rh age. Never-
t reated 11 p at ien ts w ith th e p ip elin e d evice in th e set t ing of SAH t h eless, th e balloon rem odeling tech n iqu e can be lim ited by th e
an d n oted t h at t w o p at ien t s d ied from rebleeding d u r in g t h e in abilit y to pack th e neck of t h e an eu r ysm an d th e possibilit y of
acu te illn ess. Th e au th ors con clu d ed t h at en d osaccu lar coiling coil p rolap se or dislocat ion w ith su bsequ en t th rom boem bolic
of th e sac is w arran ted in pat ien ts w ith acute SAH an d th at th e com plicat ion s.
pipeline device m ay be used as a coil scaffold rather than a flow - Th e Hyp erglide an d Hyp erform balloon s (ev3) are m ost com -
diver ter. m on ly u sed at our inst it u t ion . Th e lat ter is m ore com plian t an d
u t ilized in cases of tort u ou s paren t vessel or com plex an eur ysm
m or p h ology. In it ially, t h e balloon is advan ced across t h e n eck
Balloon Remodeling
of th e an eu r ysm . An at tem pt is alw ays m ade to deploy th e coils
Th e balloon rem odeling tech n iqu e involves tem p orar y balloon w ith th e balloon deflated. If th e coils com prom ise th e lum en of
in flat ion at th e n eck of th e an eu r ysm du ring coiling to protect th e p aren t vessel or th e side bran ch , th e balloon is th en in flated
th e p aren t vessel in com p lex m orp h ology. Th e tech n ique is usu- to provide assistan ce. Mult iple coils are deployed during a single
ally in dicated in w ide-n ecked an eur ysm s an d for protect ion of in flat ion . After an eur ysm coiling, th e balloon is deflated on a
bran ch ing ar teries in close p roxim it y to th e an eur ysm n eck (Fig. blan k roadm ap to determ in e th e stabilit y of th e coil m ass. If coil
42.3). Th e risk of th rom boem bolic com plicat ion s w ith th e bal- disp lacem en t occu rs, th e balloon is rein flated an d m ore coils are
loon rem odeling tech n iqu e sh ou ld be con sidered . Th ese are re- dep loyed. If th e coil m ass rem ain s u n st able despite addit ion al
lated to blood stasis or in t im al inju r y from balloon in flat ion , an d packing, a sten t is dep loyed across th e n eck of th e an eu r ysm to
sim ultaneous introduct ion of t w o m icrocatheters into the parent protect th e paren t vessel.

a b c

Fig. 42.3a–c (a) A 3D reconstruction of digital subtraction angiography rhage (SAH). (b) The aneurysm was successfully treated with balloon-
(DSA) demonstrating a 6 × 4-m m wide-necked superior cerebellar artery assisted coiling, and showed persistence of occlusion with patency of branch-
aneurysm in a patient with a Hunt and Hess grade III subarachnoid hem or- ing vessel at the 6-m onth follow-up angiogram (c).

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42 Endovascular Management of Subarachnoid Hemorrhage 499

Onyx HD-500 sel. On ce th e desired resu lt is ach ieved, th e balloon is rem oved
u n der flu oroscopic guidan ce, an d con t rol angiograp hy is per-
Onyx HD-500 (ev3) is curren tly th e on ly liquid em bolic agen t
form ed to con firm com plete vessel decon st r uct ion .
approved by th e Food an d Drug Adm in ist rat ion (FDA) for th e
Procedu ral com plicat ion s occu r in 16 to 26% of pat ien t s an d
t reat m en t of in t racran ial an eu r ysm s. Onyx em bolizat ion is in di-
are m ostly related to th e im perfect predict ive valu e of BTO in
cated in selected pat ien t s w ith an eu r ysm s th at are u n su it able for
identifying patients at risk for developing delayed ischem ic events
coil t reat m en t (t ypically w ide-n ecked an d irregu lar-sh ap ed an -
after paren t ar ter y sacrifice.46 Cer t ain ly, th is tech n ique sh ould be
eu r ysm s) or in w h om p reviou s t reat m en t h as failed to occlu de
u sed w ith caut ion in pat ien t s w ith SAH because post t reat m en t
th e an eu r ysm . Onyx HD-500 can be u sed as a m on oth erapy or in
an t iplatelet th erapy is recom m en ded for preven t ion of th rom bo-
com bin at ion w ith coils an d sten t s if n ecessar y. Th e tech n iqu e
em bolic even t s. Fu r th erm ore, th ese pat ien t s m ay be m ore pron e
involves balloon in flat ion at th e n eck of th e an eur ysm to en sure
to isch em ic injur y from su bsequen t vasospasm .
an effective seal and avoid leakage of the em bolic agent during the
cou rse of em bolizat ion . Onyx fills alm ost 100% of t h e an eu r ysm
sac, en ables opt im al an eu r ysm n eck an d p aren t vessel recon -
st r u ct ion , an d in du ces a st rong n eo-en doth elializat ion react ion
at th e an eu r ysm n eck. Th is resu lts in im proved long-term t reat- ■ Endovascular Management
m en t du rabilit y as com pared w ith conven t ion al coiling.45 Th e of Vasospasm
m ost com m on com plicat ion s in clude th rom bot ic even ts, dist al
Up to 70% of pat ien t s develop cerebral vasospasm after SAH, but
ar terial em bolizat ion , Onyx cast in stabilit y (w ith possible m igra-
only 30%becom e sym ptom atic.47 The risk of vasospasm increases
t ion in to th e p aren t vessel), an d m ass effect in n eigh boring cor t i-
bet w een 3 an d 7 days after SAH, reach es m axim al severit y in th e
cal st ru ct u res. Experien ce w ith th is agen t h as been ver y lim ited
secon d w eek, an d t yp ically resolves in th e th ird or fou r th w eek.
in pat ien t s w ith acutely ru pt u red an eur ysm s du e to th e n eed for
Delayed cerebral isch em ia du e to vasosp asm is th e secon d lead-
pre- and postoperative dual antiplatelet therapy.45 The technique,
in g cau se of deat h an d d isabilit y in p at ien t s w it h an eu r ysm al
th erefore, sh ould be u sed ver y cau t iou sly in th e set t ing of SAH.
SAH. Th e relat ion bet w een vasosp asm an d cerebral isch em ia/
in farct ion is com plex, as m any pat ien t s w ith severe spasm n ever
becom e sym ptom at ic, w h ereas oth ers w ith on ly m ild spasm de-
Parent Vessel Deconstruction
velop cerebral in farct ion s.48
Th e decon st r u ct ive app roach involves th e occlu sion of t h e p ar- Digit al subt ract ion angiography is th e gold st an dard for de-
en t vessel or several afferen t vessels to th e an eu r ysm to produ ce tect ion of vasospasm , but its use is lim ited by th e poten t ial risk
th rom bosis of th e vessel–an eu r ysm com p lex. Th is tech n iqu e is of com plicat ion s. Tran scran ial Doppler (TCD) is th e m ost w idely
in dicated in dissect ing, gian t , an d com p lex an eur ysm s w h en se- u t ilized n on invasive m eth od for m on itoring of vasospasm after
lect ive en dosaccu lar coiling is n ot feasible (Fig. 42.4) or in blister SAH. Th e sen sit ivit y an d sp ecificit y of TCD for d etect ion of va-
dissect ing p roxim al an eu r ysm s. A balloon test occlu sion (BTO) is sospasm range from 70 to 80%, an d result s correlate w ell w ith
perform ed to assess th e adequ acy of collateral flow an d th e risk angiograp h ic fin d ings.47 Th e tech n iqu e, h ow ever, is op erator
of postoperat ive st roke prior to perm an en t arterial occlusion . A d epen den t an d provides lit tle quan t itat ive data for grading th e
balloon is slow ly in flated at th e plan n ed occlusion site, an d com - severit y of th e lesion . CTA h as a good sen sit ivit y an d sp ecificit y
p lete occlu sion of th e p aren t vessel is ver ified by p roxim al con - for d etect ion of severe vasosp asm bu t it is less reliable w h en
t rast inject ion . Th e p at ien t is t h en m on itored w it h con t in u ou s vasospasm is m ild or m oderate. Perfusion st u dies appear to be
clin ical exam in at ion for a tot al of 30 m in u tes. For t h e first 15 m ore accurate for iden tificat ion of delayed cerebral isch em ia
m in utes, th e test is perform ed un der n orm oten sive param eters, th an TCD or an atom ic im aging of ar terial n arrow ing.13
an d for th e rem ain ing 15 m in utes, th e pat ien t’s blood pressure is Oral n im odipin e im proves n eurologic outcom e (bu t n ot vaso-
decreased by 30% to sim u late delayed hyp odyn am ic isch em ia. spasm ) after SAH an d sh ould be adm in istered to all pat ien ts.13
Th e BTO is “passed” by p at ien t s w h o rem ain n eu rologically in - Because th e volu m e an d clearan ce rate of blood in th e basal cis-
tact du ring th e test an d, in th e case of th e pat ien t u n der gen eral tern s an d ven t ricles are im port an t predictors of vasospasm an d
an esth esia, if all n eu rophysiological m on itoring rem ain s st able cerebral isch em ia follow ing SAH, in t rath ecal th rom bolyt ics h ave
an d angiograph ic cerebral collateral circulat ion is presen t . Such been investigated as possible prophylactic therapy for vasospasm .
pat ien ts m ay th en u n dergo paren t vessel decon st ru ct ion . How - According to a recen t m eta-an alysis of five ran dom ized con -
ever, if th e pat ien t fails th e BTO, a surgical bypass is u sually per- t rolled t rials, in t rath ecal th rom bolyt ics sign ifican tly redu ce th e
form ed prior to p aren t vessel d econ st ru ct ion . develop m en t of p oor ou tcom es, delayed n eu rologic deficits, an -
Paren t vessel decon st ru ct ion is perform ed un der p roxim al giograph ic vasospasm , an d ch ron ic hydroceph alus.49 Th ese fin d-
flow arrest to en able th e precise placem en t of th e em bolic m ate- ings, however, require confirm ation in larger, m ore rigorous trials.
rial an d reversal of collateral flow in th e dist al circu lat ion , w h ich Prop hylact ic angiop last y of th e basal cerebral ar teries, an t ip late-
vir t u ally elim in ates th e risk of distal em bolizat ion . Th e Ascen t let p rop hylaxis, en doth elin receptor an tagon ists, an d m agn e-
balloon (Micrus, San Jose, CA) is th e m ost com m on ly used t ype of siu m su lfate did n ot im p rove clin ical ou tcom es after SAH in clin i-
balloon at our in st it ut ion . It h as a coaxial dual-lum en design th at cal t rials an d sh ou ld th erefore be avoided .13 Despite prom ising
en ables con cu rren t balloon in flat ion an d coil or Onyx deliver y early results, a recen t m et a-an alysis of several sm all ran dom ized
th rough th e cen t ral lu m en . A few coils are in it ially deployed in t rials sh ow ed n o clin ical ben efit w ith st at in use after SAH.51
th e vessel p roxim al to th e an eu r ysm to create a fram ew ork for Endovascular treatm ent sh ould be considered in patients w ith
su bsequ en t Onyx inject ion . Onyx fills th e in terst ices of th e coils worsening vasospasm (new neurologic deficit/increasing velocities/
an d en ables im m ediate an d m ore effect ive occlu sion of th e ves- perfu sion deficit) w h o do n ot respon d to or can n ot tolerate (due

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500 V Cerebral and Spinal Aneurysms

a b c

d e

Fig. 42.4a–e (a) Frontal view of digital subtraction angiography (DSA) occlusion of the vertebral artery (VA) and the dissecting aneurysm . Frontal
showing a dissecting aneurysm of the right vertebral artery in a 48-year-old (d) and lateral (e) views of 6-m onth follow-up DSA showing persistence of
patient with subarachnoid hem orrhage (SAH). (b,c) Angiogram s after em - occlusion with no retrograde filling of the right VA or the aneurysm .
bolization with eight coils and 0.7 m L of Onyx 34 dem onstrates complete

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42 Endovascular Management of Subarachnoid Hemorrhage 501

to m edical com orbidit ies) hyper volem ic th erapy. A h ead CT is an d en d ovascu lar an eu r ysm coiling m ay be safer t h an su rgical
obtain ed prior to en dovascu lar in ter ven t ion to ru le out oth er clipp ing.
cau ses of n eu rologic deteriorat ion su ch as hydrocep h alu s an d Th e p roced u re is p er for m ed u n d er gen eral an est h esia an d
rebleeding. In our in st it u t ion , if p at ien t s do n ot dem on st rate fu ll h ep arin izat ion (if possible) to m ain tain an act ivated clot t ing
n eu rologic reversal w ith in 60 m in utes despite m axim al m edical t im e at t w o t im es th e pat ien t’s baselin e in t raop erat ively. Vessels
th erapy, w e proceed w ith angiograp hy an d ch em ical or m ech an - th at are am en able to angiop last y in clu de all p roxim al vessels:
ical in t ra-arterial sp asm olysis. En dovascu lar t reat m en t sh ou ld in tern al carot id ar ter y, M1, P1, A1, ver tebral, an d basilar (Fig.
n ot be delayed because angioplast y is m ost effect ive in reversing 42.5). Angioplast y sh ould be avoided in th e posterior in ferior
n eu rologic declin e an d im proving ou tcom e w h en perform ed cerebellar ar ter y (PICA), an terior in ferior cerebellar ar ter y (AICA),
w ith in 2 h ours after on set of sym ptom s, as dem on st rated by P2, A2, an d M3 du e to th e h igh risk of vessel p erforat ion . Th e
Rosenw asser et al.52 En dovascu lar t reat m en t of vasosp asm con - m ost com m on ly ut ilized balloon in our in st it ut ion is th e Hyper-
sists of balloon angioplast y, m ostly for large vessel spasm , or in - glide. Balloon angioplast y is don e to 50 to 90%of th e origin al size
fusion of in t ra-ar terial agen t s for m ore dist al bran ch vasospasm . of th e vessel; overdilat ion is avoided to reduce th e risk of vessel
Angiop last y is associated w it h greater r isk of ar ter ial r u pt u re perforat ion .
or dissect ion , esp ecially if ap plied to m ore dist al vessels, bu t it s Distal branch vasospasm is treated by infusion of intra-arterial
effect is m ore du rable th an in t ra-ar terial p h arm acological in fu - ph arm acological agen ts. Papaverin e w as th e m ost st udied in t ra-
sion s. Angiop last y provides angiograp h ic im p rovem en t in 80 to ar terial vasodilator but is curren tly n o longer used because of it s
100%of cases an d clin ical im provem en t in 30 to 80%. Vessel rup - potential neurotoxicit y.47 Recently, the efficacy of several calcium
t u re an d rebleeding from an u n secu red an eu r ysm are t w o of th e channel antagonists and other vasodilators has been investigated.
m ost com m on an d poten t ially cat ast roph ic com p licat ion s asso- In t ra-ar terial calciu m ch an n el blockers su ch as n icardip in e, vera-
ciated w ith angioplast y, an d occu r in 4% an d 5% of cases, respec- pam il, or n im odip in e w ere sh ow n to p rovide h igh rates of n eu ro-
t ively. Oth er p oten t ial com plicat ion s in clu de bran ch occlu sion , logic im provem en t an d resolu t ion of vasospasm in several sm all
h em orrh agic in farct ion , an d ar terial dissect ion . For pat ien t s w ith ret rosp ect ive series.47 Prom ising resu lt s w ere also rep or ted w ith
delayed SAH w h o h ave severe vasospasm proxim al to th e an eu - nitric oxide donors.13 However, a clinical benefit w ith these agents
r ysm site, a com bin ed en dovascu lar t reat m en t w ith angioplast y h as yet to be dem on st rated in a ran dom ized con t rolled t rial.

a b

Fig. 42.5a–f (a,b) Noncontrast computed tom ography (CT) scan showing diffuse, Fisher grade IV subarachnoid hem orrhage (SAH) centered mostly in
the posterior fossa. (continued on page 502)

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502 V Cerebral and Spinal Aneurysms

c d

e f

Fig. 42.5a–f (continued ) (c) Lateral view of digital subtraction angiogra- (e) Lateral view of DSA showing severe spasm of the basilar artery 3 days
phy (DSA) demonstrating a sm all fusiform aneurysm of the left posterior after SAH. (f) Lateral view of DSA after balloon angioplast y showing signifi-
inferior cerebellar artery. (d) Lateral view of DSA after aneurysm treatm ent. cant improvem ent in arterial diam eter.

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42 Endovascular Management of Subarachnoid Hemorrhage 503

im prove procedural safet y, patient outcom e, and long-term treat-


■ Conclusion m en t durabilit y. Fin ally, even in th e era of m in im ally invasive
En d ovascu lar t h erapy h as becom e a m ain st ay t reat m en t m o - th erapies, w e are con st an tly rem in ded t h at su rgical clipp ing re-
dalit y for p at ien t s w it h r u pt u red cerebral an eu r ysm s. Fu t u re m ain s an invaluable t reat m en t opt ion for m any pat ien t s w ith
advan ces in en dovascu lar tech n iques an d devices w ill fur th er an eur ysm al SAH.

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sociat ion St roke Coun cil; Coun cil on Cardiovascular Radiology an d In ter- by evacuat ion of h em atom a. World Neurosurg 2010;74:626–631
ven t ion ; Coun cil on Cardiovascu lar Nursing; Coun cil on Cardiovascular 29. Mitch ell P, Kerr R, Men delow AD, Molyn eu x A. Could late rebleeding over-
Surger y an d An esth esia; Coun cil on Clin ical Cardiology. Guidelin es for th e t urn th e superiorit y of cran ial an eur ysm coil em bolizat ion over clip liga-
m an agem en t of aneur ysm al subarach noid h em orrh age: a guidelin e for t ion seen in th e In tern at ion al Subarach n oid An eur ysm Trial? J Neurosurg
h ealth care profession als from th e Am erican Hear t Associat ion /Am erican 2008;108:437–442
St roke Associat ion . St roke 2012;43:1711–1737 30. Ch alouh i N, Teufack S, Ch an dela S, et al. An eur ysm al subarach noid h em -
14. Kow alski RG, Claassen J, Kreiter KT, et al. In it ial m isdiagn osis and ou tcom e orrh age in pat ien t s un der 35-years-old: a single-cen ter experien ce. Clin
after subarach n oid h em orrh age. JAMA 2004;291:866–869 Neurol Neurosurg 2013;115:665–668
15. van der Wee N, Rin kel GJ, Hasan D, van Gijn J. Detect ion of subarach n oid 31. Lu sseveld E, Br ilst ra EH, Nijssen PC, et al. En dovascu lar coiling versu s
h aem orrh age on early CT: is lum bar pun ct ure st ill n eeded after a n egat ive n eu rosu rgical clip ping in p at ien t s w ith a ru pt u red basilar t ip an eu r ysm .
scan? J Neu rol Neurosurg Psych iat r y 1995;58:357–359 J Neu rol Neu rosu rg Psych iat r y 2002;73:591–593
16. Fiebach JB, Sch ellinger PD, Gass A, et al; Kom peten znet zw erk Sch lagan fall 32. Chalouhi N, Jabbour P, Gon zalez LF, et al. Safet y and efficacy of endovascu-
B5. St roke m agn et ic reson an ce im aging is accurate in hyperacute in t race- lar t reat m en t of basilar tip an eu r ysm s by coiling w ith an d w ith ou t sten t
rebral h em orrh age: a m u lt icen ter st u dy on th e validit y of st roke im aging. assistan ce: a review of 235 cases. Neu rosu rger y 2012;71:785–794
St roke 2004;35:502–506 33. Ch alouh i N, Tjoum akaris S, Dum on t AS, et al. Superior hypophyseal ar ter y
17. Willin sky RA, Taylor SM, TerBrugge K, Farb RI, Tom lin son G, Mon t an era an eur ysm s h ave th e low est recurrence rate w ith en dovascular th erapy.
W. Neurologic com plicat ion s of cerebral angiography: prospect ive an aly- AJNR Am J Neuroradiol 2012;33:1502–1506

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34. Pierot L, Cogn ard C, An xion n at R, Ricolfi F; CLARITY Invest igators. Re- 44. Sh apiro M, Babb J, Becske T, Nelson PK. Safet y an d efficacy of adjun ct ive
m od eling tech n iqu e for en dovascu lar t reat m en t of r u pt u red in t racran ial balloon rem od eling du ring en d ovascu lar t reat m en t of in t racran ial an eu -
an eu r ysm s h ad a h igh er rate of ad equ ate p ostop erat ive occlu sion th an did r ysm s: a literat ure review. AJNR Am J Neuroradiol 2008;29:1777–1781
conven t ion al coil em bolizat ion w ith com parable safet y. Radiology 2011; 45. Molyn eu x AJ, Cekirge S, Saatci I, Gál G. Cerebral An eur ysm Mult icen ter
258:546–553 European Onyx (CAMEO) trial: results of a prospective obser vational st udy
35. Piot in M, Blan c R, Spelle L, et al. Sten t-assisted coiling of in t racran ial an - in 20 European cen ters. AJNR Am J Neuroradiol 2004;25:39–51
eur ysm s: clin ical an d angiograph ic result s in 216 con secut ive an eur ysm s. 46. Graves VB, Perl J II, St roth er CM, Wallace RC, Kesava PP, Masar yk TJ. En do-
St roke 2010;41:110–115 vascu lar occlu sion of th e carot id or ver tebral ar ter y w ith tem porar y p rox-
36. Molyn eu x AJ, Clarke A, Sn eade M, et al. Cerecyte coil t rial: angiograph ic im al flow arrest and m icrocoils: clinical result s. AJNR Am J Neuroradiol
outcom es of a prospect ive ran dom ized t rial com paring en dovascular coil- 1997;18:1201–1206
ing of cerebral an eur ysm s w ith eith er cerecyte or bare plat in um coils. 47. Jabbour PM, Tjoum akaris SI, Rosenw asser RH. Neuroen dovascular m an -
St roke 2012;43:2544–2550 agem ent of vasospasm follow ing an eur ysm al su barach n oid h em orrh age.
37. Rordorf G, Bellon RJ, Budzik RE Jr, et al. Silen t th rom boem bolic even t s as- Neurosurg Clin N Am 2009;20:441–446
sociated w ith th e t reat m en t of un r upt ured cerebral an eur ysm s by use of 48. Et m inan N, Vergouw en MD, Ilodigw e D, Macdon ald RL. Effect of ph arm a-
Guglielm i detach able coils: prospective st udy applying diffusion -weighted ceut ical t reat m en t on vasospasm , delayed cerebral ischem ia, and clin ical
im aging. AJNR Am J Neu roradiol 2001;22:5–10 outcom e in pat ien t s w ith an eu r ysm al subarachn oid h em orrh age: a sys-
38. Ch alouh i N, Jabbou r P, Kung D, Hasan D. Safet y and efficacy of t irofiban in tem at ic review an d m et a-an alysis. J Cereb Blood Flow Met ab 2011;31:
sten t-assisted coil em bolizat ion of in t racran ial an eu r ysm s. Neu rosu rger y 1443–1451
2012;71:710–714, discu ssion 714 49. Kram er AH, Fletch er JJ. Locally-adm inistered in t rath ecal th rom bolyt ics
39. Jabbour PM, Tjoum akaris SI, Rosenw asser RH. En dovascular m an agem en t follow ing an eur ysm al subarach n oid h em orrh age: a system at ic review
of int racranial aneur ysm s. Neurosurg Clin N Am 2009;20:383–398 and m et a-an alysis. Neu rocrit Care 2011;14:489–499
40. Am ent a PS, Dalyai RT, Kung D, et al. Sten t-assisted coiling of w ide-n ecked 50. Kirkpat rick PJ, Turn er CL, Sm ith C, Hu tch in son PJ, Mu rray GD; STASH Col-
an eu r ysm s in th e set t ing of acu te su barach n oid h em orrh age: exp erien ce laborators. Sim vastatin in aneur ysm al subarachnoid haem orrhage (STASH):
in 65 patients. Neurosurgery 2012;70:1415–1429, discussion 1429 a m u lt icen t re ran d om ised p h ase 3 t r ial. Lan cet Neu rol 2014;13(7):666–
41. Bodily KD, Cloft HJ, Lan zin o G, Fiorella DJ, W h ite PM, Kallm es DF. Sten t- 675
assisted coiling in acu tely ru pt u red in t racran ial an eu r ysm s: a qu alit at ive, 51. Vergouw en MD, Meijers JC, Geskus RB, et al. Biologic effect s of sim vas-
system at ic review of th e literat ure. AJNR Am J Neuroradiol 2011;32: t at in in p at ien t s w it h an eu r ysm al su barach n oid h em or rh age: a double-
1232–1236 blin d, placebo-con t rolled ran dom ized t r ial. J Cereb Blood Flow Met ab
42. Mocco J, Snyd er KV, Albu qu erqu e FC, et al. Treat m en t of in t racran ial an - 2009;29:1444–1453
eu r ysm s w ith th e En terprise sten t: a m ult icen ter regist r y. J Neu rosurg 52. Rosenw asser RH, Arm on da RA, Th om as JE, Ben itez RP, Gan non PM, Har-
2009;110:35–39 rop J. Th erapeut ic m odalit ies for th e m an agem en t of cerebral vasospasm :
43. McAuliffe W, Wen deroth JD. Im m ediate an d m idterm result s follow ing t im ing of en dovascular opt ion s. Neurosurger y 1999;44:975–979, discus-
t reat m en t of recen tly rupt ured in t racran ial aneur ysm s w ith th e Pipeline sion 979–980
em bolizat ion device. AJNR Am J Neuroradiol 2012;33:487–493

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43 Surgical Therapies for Saccular
Aneurysms of the Internal
Carotid Artery
Leonardo Rangel-Cast illa and Robert F. Spetzler

An eur ysm s of th e in tern al carot id ar ter y (ICA) t run k, in cluding


t h e p oster ior com m u n icat in g ar ter y (PCoA) segm en t , accou n t
■ Surgical Orientation and Anatomy of
for 35 to 50% of all in t racran ial an eur ysm s.1–5 Before th e en do the Internal Carotid Artery
vascu lar era, th ese an eur ysm s w ere relat ively easy to approach
Th e ICA is divided in to fou r segm en t s: C1, cer vical; C2, p et rou s;
an d clip; n ow, m ost of th em are t reated w ith en dovascular coil
C3, cavern ous; an d C4, su praclin oid. Th e supraclin oid segm en t
em bolizat ion tech n iqu es.6–10 Th e rem ain ing an eu r ysm s th at are
begin s w h ere th e ar ter y en ters th e subarach n oid space an d ter
referred to vascular n eu rosu rgeon are m ore com plex, large or
m in ates at th e bifurcat ion in to th e ACA an d th e MCA. Th e C4 seg
gian t , in corporate an arter y in to th e n eck, or are recurren t an eu
m en t em erges from th e dura m ater an d passes along th e m edial
r ysm s previously coiled. Th eir in t im ate relat ion sh ip w ith th e
side of th e an terior clin oid p rocess an d below th e opt ic n er ve. It
skull base an d cran ial n er ves h as to be w ell un derstood before
reach es th e lateral side of th e opt ic ch iasm an d bifurcates below
th ey are ap proach ed su rgically.5,11–13 An eur ysm s of th e ICA gen
th e an terior perforated su bst an ce at th e m edial en d of th e syl
erally form a fam ily; h ow ever, each specific su bt ype of ICA an eu
vian fissu re. Th e C4 segm en t is fu rth er divided in to th ree m ore
r ysm h as a differen t in ciden ce, clin ical presen tat ion , an atom ic
segm en t s 16,17 : th e op h th alm ic segm en t is th e longest an d goes
feat ures, operat ive n uan ces, com plicat ion s, an d progn osis. About
from th e roof of th e cavern ou s sin u s an d th e origin of t h e op h
25% of all in t racran ial an eu r ysm s are PCoA an eur ysm s, m aking
th alm ic ar ter y to th e origin of th e PCoA; th e com m u n icat ing seg
th em t h e secon d m ost com m on after an terior com m u n icat ing
m en t exten ds from th e origin of th e PCoA to th e origin of th e
ar ter y an eur ysm s (ACoA). ICA bifurcat ion an eu r ysm s accoun t for
ACh A; an d the ch oroidal segm en t is th e sh or test an d goes from
n o m ore th an 15% in adults, but in ch ildren th ey are th e m ost
th e origin of th e ACh A to th e bifu rcat ion . Op h th alm ic ar ter y seg
com m on locat ion . An terior ch oroidal ar ter y (ACh A) an eu r ysm s
m en t an d an eu r ysm s are review ed in Ch apters 46 an d 47. Each
are uncom m on and account for less than 5%of all aneurysm s. This
segm en t h as a con stan t n u m ber of p erforators. Th e com m u n i
ch apter review s th e m icrosu rgical t reat m en t of an eu r ysm s aris
cat ing segm en t h as on e to th ree p erforators, bu t in m ore th an
ing from th e term in al ICA, ACh A, an d PCoA.
50% of th e h em isph eres th ere are n o perforators com ing off th is
segm en t. The oph thalm ic perforators arise from the posterior half
of th e paren t vessel an d go to th e opt ic apparat us, in fun dibulum ,
an d prem am illar y m em bran e. Th e ch oroidal segm en t h as four or
■ Embryology of the Internal five perforators th at arise from th e posterior h alf an d term in ate
Carotid Artery on th e opt ic tract , u n cu s, an d an terior p erforat ing substan ce.

Th e in t racran ial p or t ion of th e ICA arises from th e em br yon ic


dorsal aor ta. With in 4 w eeks of gest at ion , th e ICA h as cau dal an d Superior Hypophyseal and Infundibular Arteries
cran ial por t ion s. Th e caudal port ion of th e ICA an astom oses at
Th is is a grou p of th ree to fou r ar teries th at arise from th e p os
m u lt ip le sites w ith t h e ar ter y located on t h e h in d brain , w h ich
terom edial aspect of th e ICA. Th ey term in ate at th e pit uit ar y
is th e precursor of th e basilar ar ter y an d regresses to form th e
glan d, opt ic apparat us, an d floor of th e th ird ven t ricle. Th e larg
PCoA. Ot h er an astom ot ic sites (hyp oglossal, ot ic, t r igem in al)
est of th ese is th e superior hypophyseal ar ter y. Th e in fun dibu lar
regress before bir th .14 At days 45 to 48, th e ACh A, th e an terior
ar teries arise from PCoA an d go to th e in fun dibulum . Th e supe
cerebral ar ter y (ACA), an d m iddle cerebral ar ter y (MCA) develop
rior hyp op hyseal an d in fu n dibu lar ar teries go below th e ch iasm
from th e cran ial por t ion s of a p aren t em br yon ic vessel th at arise
in to th e t uber cin ereum to form th e an astom ot ic plexus aroun d
from th e th ird aor t ic arch . By w eek 8 th e ICA con t in u es to grow
th e pit u it ar y st alk. Th ey povid e blood su p ply to th e an terior p i
in to th e p osterior cerebral ar ter y (PCA), an d th e PCoA regresses
t u itar y lobe.
as th e ver tebral an d basilar ar teries develop. Du ring th e sam e
w eek, both PCAs can be iden t ified as th e posterior com m un ica
t ion of th e PCoAs. If th e em br yon ic PCoA fails to regress, th e Terminal Internal Carotid Artery and A1
dom in an t su p ply to th e occip ital lobe arises from th e ICA via th e
Segment of the Anterior Cerebral Artery
fet al PCA in stead of the ver tebrobasilar system . A fetal PCA is
seen in arou n d 30% of cases. It is a varian t of th e PCoA w ith th e Th e bifu rcat ion of th e ICA is located ben eath th e an terior p erfo
sam e caliber as th e P2 segm en t an d is associated w ith a hypo rated su bst an ce. Th e ACA p asses over th e opt ic n er ve to reach th e
plast ic P1 segm en t .15 ACoA. Th e first segm en t of th e ACA or A1 ar ter y h as perforators

505

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506 V Cerebral and Spinal Aneurysms

to t h e basal forebrain . It gives r ise to t h e recu r ren t ar ter y of m m (range, 5 to 25 m m ). Th e ACh A is divided in to cisternal an d
Heu bn er. Th e MCA divides u n der th e fron t al an d parietal oper plexal segm en t s. Th e cister n al segm en t goes to t h e ch oroidal
cula.5,16,17 ACA an d MCA an eur ysm s are review ed in Ch apters 48, fissu re an d bran ch es off in to a p roxim al an d d ist al p or t ion at
49, 52, and 53. t h e lateral gen icu late body. Th e plexal segm en t p asses th rough
th e ch oroidal fissu re to en ter th e ch oroidal p lexu s an d tem poral
h orn . Th e ACh A gives blood supply to th e globu s pallidu s, poste
Posterior Communicating Artery rior lim b of t h e in tern al cap su le, opt ic t ract , an d lateral gen icu
late body.4,5 There is interchangeabilit y of field bet w een the AChA
Th e PCoA arises from th e p osterom edial asp ect of th e ICA h alf
an d th e PCoA or PCA. If th e ACh A is sm all, th e PCoA takes over
w ay bet w een th e op h th alm ic ar ter y an d th e bifu rcat ion . It t rav
t h e p oster ior lim b of t h e in ter n al cap su le.24 More t h an h alf of
els m edially an d p osteriorly above an d m edial to th e ocu lom otor
t h e h em isph eres h ave ACh A an d PCA an astom oses. Th ese an as
n er ve to join th e PCA. Th e PCoA con t in ues as th e PCA during em
tom oses are foun d at th e lateral surface of th e lateral gen icu late
br yon ic developm en t , bu t in th e adult it is an n exed by th e basilar
body, at th e tem poral lobe n ear th e u n cu s, an d th e rich est on e at
ar ter y.16,17 As described above, a fetal PCA m ean s th at th e PCoA
th e su rface of th e ch oroid plexu s w ith th e lateral p osterior ch o
rem ain s th e m ain origin of th e PCA an d its course is sligh tly dif
roidal bran ch es of th e PCA. Th ese an astom oses explain th e in
feren t; it goes fu r th er laterally above or lateral to th e oculom otor
con sisten t clin ical resu lts of ACh A occlu sion .
n er ve.5,18–20 In n orm al circum stan ces, th e PCoA provides blood
su p ply to th e hyp oth alam u s, ven t ral th alam u s, opt ic t ract , poste
rior lim b of th e in tern al cap su le, p osterior p erforated substan ce, Veins Related to Terminal ICA/A1, PCoA,
an d su bt h alam ic n u cleu s. Dilat ion s of th e PCoA or igin , kn ow n
and AChA Aneurysms
as th e fu n ction al dilat ion or in fu n dibu lar w iden ing, are fou n d in
6 to 10% of cerebral angiogram s. Th ese dilat ion s are defin ed as Th e an terior cerebral an d su perficial m id dle cerebral vein s ru n
con ic, t riangu lar, or in fu n dibu lar sh aped, an d are less th an 3 m m u n der or over th e ICA bifurcat ion to reach th e cavern ous sin us or
w ide. They can be difficult to differentiate from aneur ysm s. There th e sph en opariet al sin us. Deep ly, th e an terior an d deep m iddle
are repor t s of saccular an eur ysm s arising from a previously doc cerebral vein an d th e basal vein of Rosen th al are in t im ally re
um en ted in fun dibu lu m .21,22 Th e PCoA h as an average of eigh t lated w ith th e PCoA an d th e ACh A. Th ese vein s m erit par t icu lar
perforators arising from th e su p erior an d lateral su rfaces th at go care d u ring th e d issect ion of an an eu r ysm to avoid vein r u pt u re
to th e t u ber cin ereum , m am m illar y bodies, posterior perforated an d p ossibly causing n eurologic deficit s.25
su bstan ce, opt ic ap parat u s, th alam u s, hypoth alam u s, su bth ala
m us, an d in tern al capsule. The prem am illar y arter y is th e largest
bran ch an d com m on ly origin ates at th e m iddle of th e PCoA. It
en ters th e floor of th e th ird ven t ricle bet w een th e m am m illar y ■ Clinical Relevance of the Terminal
bodies an d th e opt ic t ract and supplies th e posterior hypoth ala ICA/A1, PCoA, and AChA Aneurysms
m us, ven t ral th alam us, an d posterior lim b of th e in tern al cap
su le. In som e cases, th e PCoA is sm all an d th e ACh A t akes over it s Epidemiology
n orm al dist ribut ion of supply to th e gen u an d an terior th ird of
Term in al ICA/A1 an eur ysm s accoun t for 5 to 15% of all in t racra
th e in tern al cap sule.
n ial an eu r ysm s. Th e result s of ph ase 1 of th e In tern at ion al St udy
of Un rupt ured In t racran ial An eur ysm s (ISUIA) sh ow ed th at ICA
an eur ysm s accoun t for 24.8% an d 17.8% of th e un r upt ured an d
Anterior Choroidal Artery rupt u red an eu r ysm group , respect ively.26,27 In 2003, th e ISUIA
Th e su rgeon sees th e ACh A before th e PCoA, even th ough th e grou p pu blish ed a secon d an alysis; an ICA aneur ysm w as iden t i
ACh A arises dist ally to th e PCoA. Th is is because th e ICA passes in fied in 22.9% an d 34.8% of th e un t reated an d t reated groups, re
a posterolateral direct ion , placing th e origin of th e ACh A fur th er sp ect ively.26,27 In th e Fam ilial In t racran ial An eu r ysm (FIA) st u dy,
lateral to th e origin of th e PCoA. Th e ACh A arises m ore laterally ICA an eu r ysm s cou n ted for 40.1% of all an eu r ysm s.28,29 In th e
on th e posterior w all of th e ICA th an of th e PCoA in m ost cases. In tern at ion al Subarach n oid An eur ysm Trial (ISAT), 32.5% of th e
Th e ACh A h as a m ore lateral cou rse (arou n d th e cerebellar pe an eu r ysm s w ere ICA an eu r ysm s.3,30 Recen t ly, t h e Jap an ese Un
du n cle in to th e tem p oral h orn ) th an th e PCoA (m edial direct ion rupt ured Cerebral An eur ysm St udy (UCAS) dem on st rated th at
above th e oculom otor n er ve in to th e in terpedun cular fossa).12,16,23 18.6% of 6,697 an eur ysm s w ere located at th e ICA.31 In t h e Bar-
Com m on ly th e ACh A arises as a single ar ter y from th e ICA. Less row Rupt u re An eu r ysm s Trial (BRAT), on ly 2.9%of th e an eur ysm s
frequen tly, th e ACh A can arise as t w o differen t bran ch es. It can w ere located at th e ICA term in us.2,32 PCoA an eu r ysm s are con
also aberran tly arise from th e PCoA or th e MCA. Th e ACh A is ver y sidered th e m ost com m on t ype of ICA an eu r ysm s (50%), an d are
sim ilar in size to th e oph th alm ic ar ter y an d sm aller th an th e m ore com m on ly seen in fem ales. In th e ISUIA, PCoA an eur ysm s
PCoA. At it s origin , th e ACh A h as a posterom edial direct ion be counted for 13.9%and 17%of the unruptured and ruptured group,
h in d th e ICA, an d th en it passes below or along th e m edial side of respect ively.26,27 In th e FIA st u dy, PCoA an eu r ysm s w ere seen in
th e opt ic t ract to reach th e cerebral p edu n cle. It en ters th e cru ral 10.4% of cases.28,29 In th e ISAT, PCoA an eur ysm s accoun ted for
cistern (bet w een th e cerebral pedun cle an d un cu s), an d th en it 25% of th e an eur ysm s.3,30 Th e UCAS iden t ified PCoA an eur ysm s
passes th rough th e ch oroidal fissu re in to th e ch oroid p lexu s in 15.5% of cases.31 In th e BRAT, 20.6% of all an eur ysm s w ere
w ith in th e tem poral h orn . Th e average length of th e ACh A is 12 PCoA an eur ysm s.2,32 ACh A an eur ysm s are rath er rare an d con st i

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43 Surgical Therapies for Saccular Aneurysm s of the Internal Carotid Artery 507

t u te 2 to 5% of all in t racran ial an eu r ysm s. Th ere w as n o ACh A PCoA Aneurysms


an eur ysm subgroup in any of th e largest series, in clu ding th e
Pat ien ts w ith PCoA an eur ysm s com m on ly p resen t w ith a supra
ISUIA, FIA, ISAT, or UCAS.3,26–31 In th e BRAT st u dy, on ly 2.2%of all
sellar an d am bien t cistern SAH, bu t th ey also can p resen t w ith
an eur ysm s w ere ACh A an eur ysm s.2,32
in t raparen chym al h em orrh age (IPH) in to th e tem poral lobe or
in t raven t ricu lar h em orrh age (IVH) in to th e tem poral h or n in
9% or 21% of r u pt u re an eu r ysm s, resp ect ively. An ot h er clin ical
Clinical Presentation p resen t at ion is a su bd u ral h em atom a (SDH) along t h e ten to
Terminal ICA/A1 Aneurysms riu m w ith brain stem m ass effect , w h ich m ay w arran t im m ediate
cran iotom y an d SDH evacu at ion (Fig. 43.1).5,34 Th ese an eu r ysm s
Pat ien t s w ith ru pt u red ICA bifurcat ion an eu r ysm s p resen t w ith can exp an d an d com p ress th e ocu lom otor n er ve. Som e au t h ors
in t racran ial h em orrh age (ICH) (basal ganglia h em orrh age) an d con sider PCoA an eu r ysm s to h ave a r u pt u re h istor y akin to an eu
su barach n oid h em orrh age (SAH). If th e an eu r ysm s grow en ough , r ysm s in th e p osterior circu lat ion .
t h ey can com p ress t h e opt ic n er ve.5 Morbid it y of ICA bifu r
cat ion an eu r ysm s is u su ally h igh er t h an ot h er ICA (PCoA an d
AChA Aneurysms
ACh A) an eu r ysm s d u e to t h e ten d en cy to h ave calcificat ion
w ith in th e an eur ysm s w all. ICA bifurcat ion an eu r ysm s are good Pat ien ts w ith ACh A an eu r ysm s also presen t w ith a suprasellar
can didates for th e con t ralateral ap proach in p at ien t s w ith m u l an d am bien t cistern SAH, an d th ese an eur ysm s can be difficult
t iple an eur ysm s.33 to differen t iate from a PCoA an eur ysm . Th ese an eur ysm s rarely

a b c

d e f

Fig. 43.1a–f Patient presented with severe headache. (a,b) Axial com - axial CT angiography (CTA) (d) dem onstrated a posterior com m unicating
puted tom ography (CT) scan of the brain showed intraventricular hem or- artery (PCoA) aneurysm . (e) Axial CTA after surgery dem onstrate complete
rhage (IVH) in the temporal horn and subdural hem atom a (SDH) over the aneurysm obliteration. The patient recovered well with no neurologic defi-
tentorium and frontotemporal area with m ass effect and m ild m idline shift. cits. (f) The follow-up CT scan is unrem arkable. (Courtesy of Barrow Neuro-
Angiogram with a lateral view of the internal carotid artery (ICA) (c) and logical Institute.)

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508 V Cerebral and Spinal Aneurysms

cau se IPH, IVH, SDH, or ocu lom otor n er ve com p ression . Oc MCA, recu rren t ar ter y of Heu bn er, len t icu lost riate ar teries, tem
casion ally, t h ese an eu r ysm s can be h id d en or bu r ied in t h e poral bran ch es of th e MCA, th e ACh A an d its bran ch es, an d th e
un cu s.35,36 PCoA an d it s bran ch es. Th e m ost crit ical perforators are th e m e
dial len t icu lost riate ar teries from th e p osterior asp ect of A1 an d
M1 segm en t s an d th e ICA t h at cou rse th rough th e an terior p er
forated su bst an ce to t h e basal gan glia. At t h is area, im p or t an t
■ Preoperative Evaluation of a Terminal vein s converge, in cluding th e m iddle an d an terior cerebral vein
th at cou ld r u n u n der or over th e an eu r ysm to reach th e cavern
ICA/A1 Aneurysm, and PCoA and ous or th e sph en opariet al sin us. Th e deep m iddle cerebral vein
AChA Aneurysms an d vein of Rosen th al can r un on th e in ferior side of large ICA
bifurcat ion an eu r ysm s.
Th e su rgical ch allenge for ICA term in u s, PCoA, an d ACh A an eu
r ysm s is th e ver y lim ited an d n arrow space w h ere th ese an eu
r ysm s arise, an d th e lim ited m obilit y of th e surrou n ding st ruc
t u res in clu ding th e ICA itself. In cer tain cases, th e an terior clin oid Anatomic Configuration of PCoA Aneurysms
process can be p rom in en t , an d it h as to be drilled aw ay in order Posterior com m u n icat ing arter y an eur ysm s are th e m ost com
to h ave a com plete view of th e an eur ysm . Com puted tom ogra m on of all th e ICA an eur ysm s. Th e direct ion of th e an eur ysm
phy angiogram (CTA) is a u sefu l st u dy to see th e an atom ic ch ar fu n du s can poin t su p raten torial posterolaterally adjacen t to th e
acterist ics an d th e relat ion of th e an terior clin oid process an d tem poral lobe (pat ien t s w ith th ese an eur ysm s can presen t w ith
ot h er bon e st r u ct u res to t h e an eu r ysm . PCoA an eu r ysm s can tem poral ICH or IVH); in fraten torial posterolaterally tow ard th e
be at t ach ed to th e m esial tem poral lobe or ten torium , an d pre in terp edu n cular cistern an d th e oculom otor n er ve; an terolater
op erat ive m agn et ic reson an ce im aging (MRI) can p rovid e clu es ally (if large, they can hide the origin of the PCoA); superolaterally
of t h is ad h eren ce. Large ICA bifu rcat ion an eu r ysm s can com bet w een th e ten torial edge an d th e sph en oid ridge; an d postero
press th e opt ic n er ve, in w h ich case a preoperat ive MRI w ill also laterally sim ilar to in ferior w all an eu r ysm s. Pat ien t s w ith PCoA
in for m t h e su rgeon abou t t h e relat ion of t h e opt ic ap p arat u s an eur ysm s w ith posterolateral project ion m ay presen t w ith a
an d th e an eur ysm s. ICA bifurcat ion an eu r ysm s w ith calcified dilated pu pil an d ocu lom otor p aresis. An an eu r ysm fu n du s can
w alls or a p osterior p roject ion are relat ively m ore favorable be at tach ed an d fixed to cer tain poin ts of arach n oid th icken ing:
for en d ovascu lar t h erapy; again , com p u ted tom ograp hy (CT) or w h ere th e oculom otor n er ve exit s in to th e cavern ou s sin us; at
CTA m ay be useful in t reat m en t plan n ing of th ese cases. Clipping th e ju n ct ion of th e ocu lom otor n er ve, ten toriu m , an d u n cu s; an d
of th ick w alled an d calcified an eur ysm s w ith severe ath eroscle w h ere th e arach n oid is covering th e PCoA an d th e oculom otor
rosis m ay be ch allenging. Clip p lacem en t can con st rict th e ori n er ve is adjacen t to Liliequist’s m em bran e. Th e term t rue PCoA
gin s of A1 an d M1 segm en ts. In t raoperat ive elect rophysiology aneurysm refers to th e an atom ic con figu rat ion in w h ich th e an
m on itoring is useful in en suring th e pat ien t’s toleran ce of tem eur ysm neck originates entirely from the PCoA.37,38 Rarely, a PCoA
porar y flow arrest . Motor an d som atosen sor y evoked poten t ials an eur ysm is par t ially obscured by a large an terior clin oid pro
are u sed in ou r daily p ract ice, an d w e h ave fou n d t h em ver y cess, in w h ich adequate proxim al con t rol an d visualizat ion re
u sefu l w h en p aren t ar teries h ave to be tem porar y occlu ded for quires rem oval of the anterior clinoid process or petroclinoid fold
an eu r ysm d issect ion , esp ecially for ICA bifu rcat ion an d ACh A or even exposure of th e cer vical ICA.39,40
an eur ysm s.

PCoA Aneurysms Relationship to the Oculomotor Nerve,


Anatomic Configuration of Terminal Tentorium, and Temporal Lobe
ICA/A1 Aneurysms Th e PCoA an d th e ocu lom otor n er ve r u n togeth er u n t il th ey leave
In tern al carot id ar ter y bifurcat ion an eur ysm s var y in size from th e in terp ed u n cu lar cistern t h rough th e Liliequ ist’s m em bran e,
2 to 3 m m to gian t an eur ysm s. Som e ICA bifurcat ion an eur ysm s w h ere th ey t ake differen t courses. A large an eu r ysm can com
ar ise p referen t ially from th e A1 or t h e M1 p or t ion of t h e ICA press th e ocu lom otor n er ve or ru pt u re in to it . App roxim ately
ter m in us. Th is asym m et r y an d dom e project ion sh ould be rec 20% of pat ien ts w ith PCoA an eur ysm s presen t w ith oculom otor
ogn ized an d t aken in to con siderat ion w h en plan n ing to clip re n er ve palsy, an d of pat ien ts p resen t ing w ith th ird n er ve palsy,
con st r u ct th e an eu r ysm . Dissect ion an d clip recon st r u ct ion of an 80% h ave an eur ysm s located at th e PCoA region . Th e an eu r ysm
ICA bifurcat ion can be difficult due to th e vessel’s h igh posit ion fu n du s can den sely at tach to th e ocu lom otor n er ve. It can p roject
relat ive to th e sku ll base an d its being em bedded in to th e brain above, below, or be firm ly at t ach ed to th e ten tor iu m . At t im es
paren chym a. It can p roject in th ree direct ion s: su periorly in to it m ay be n ecessar y to rem ove par t of th e ten torium to expose
th e olfactor y t ract s or fron to orbit al gyru s; p osteriorly tow ard th e an eu r ysm . An eu r ysm s can p roject in to an d be bu ried by th e
th e an terior perforated su bst an ce, sylvian , or lam in a term in alis parah ip p ocam p al gyr u s or u n cu s. A su bp ial resect ion of th e tem
cistern s; or in fer iorly in to t h e in ter p ed u n cu lar, cr u ral, or am bi poral lobe m ay be n ecessar y to fu lly expose an eu r ysm s w h en
en t cister n s. Large an eu r ysm s en croach in to t h e sylvian an d th ey are den sely adh eren t to tem p oral lobe st ru ct u res or in th e
lam in a term in alis cistern s, com pressing th e ACA an d MCA an d set t ing of h em orrh age. Th e m ost com m on cau ses of in t raopera
their perforators. Th ese an eur ysm s are intim ately related to other t ive ru pt u re are ret ract ion of th e tem poral lobe w h ile th e dom e
ar teries th at sh ould be iden t ified prior to clipping. Th ese ar teries rem ain s adh eren t to th e m esial tem poral lobe, an d prem at ure
in clu d e t h e ICA, ACA, MCA, p er forat in g ar ter ies from ACA an d m edial ret ract ion of th e supraclin oid ICA.

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43 Surgical Therapies for Saccular Aneurysm s of the Internal Carotid Artery 509

PCoA Aneurysms’ Relationship to PCoA, AChA, and rologic deficit , an d six (3.5%) of th ese cases en t ailed st rokes re
Anterior Thalamoperforating Arteries lated to th e su rgical procedu re. Large PCoA an eu r ysm s are rare
an d h ave a h igh er perioperat ive m ort alit y (18.2%). In long term
A PCoA an eu r ysm can p roject in m u lt ip le d irect ion s in relat ion
follow u p , 83% of p at ien t s w it h large PCoA an eu r ysm s h ave a
to t h e ar ter y. Th e PCoA m ay be rad iograp h ically “absen t ,” bu t in
m odified Ran kin scale (m RS) score of < 2.34
realit y th e PCoA is hypoplast ic or com pressed by th e an eur ysm ,
Th e ou tcom e for ACh A an eu r ysm s is differen t . Th e ACh A h as a
especially as it crosses th e p osterior clin oid p rocess. Th e origin of
ver y im por t an t paren chym al territor y, an d acciden tal sacrifice
th e ar ter y is frequ en tly covered by th e an eu r ysm s, an d a p lan e
of th e ar ter y can cau se h igh ly m orbid postoperat ive isch em ic
bet w een th em sh ould be developed. Th e PCoA courses in to th e
com plicat ion s. Th e an terior ch oroidal syn drom e con sists of con
in terp edu n cu lar fossa an d w ill be on th e in ferior proxim al side
t ralateral h em iplegia, h em ian esth esia, an d h em ian op sia. Most
of th e an eur ysm . Th e ACh A is usually displaced posteriorly an d
of th e t im e, p at ien t s w ith ACh A occlu sion h ave a posterior lim b
m edially by large an eur ysm s an d can be m istaken for a m edial
in tern al capsule in farct ion on im aging (Fig. 43.2). Sym ptom s m ay
st riate ar ter y. Th e th alam op erforat ing bran ch es of th e PCoA are
n ot presen t im m ediately after ACh A clipping due to possible col
d isp laced m ed ially an d p oster iorly by t h e an eu r ysm . Som e of
lateralizat ion th at preven t s an im m ediate deficit .35,36 Oth er ex-
t h ese ar ter ies (p rem am m illar y ar ter y) are w ell d evelop ed an d
plan at ion s of delayed deficit s after clip ping of an ACh A an eu r ysm
n eed to be w ell visualized before clipping.
in clude clip torsion over t im e, clip torsion secon dar y to fron t al
set tling after th e ret ractor is rem oved , or delayed th rom bosis. In
Anatomic Configuration of AChA Aneurysms a series of 51 ACh A an eur ysm s, Friedm an et al43 reported a m or-
talit y of 4% an d m ajor m orbidit y (Glasgow Outcom e Scale [GOS]
In m ost cases, th e ACh A arises as a single t run k th at bran ch es score < 3) of 10%. Sixteen p ercen t of p at ien t s in th is series h ad a
in to a grou p of ar teries. Bran ch ing can occu r early or late as th e docum en ted ACh A in farct ion .
ar ter y en ters th e cr ural cistern . In 30% of cases, th ere are t w o to
fou r ACh A bran ch es com ing d irect ly off of t h e ICA, bu t t h ere is
alw ays a m ain bran ch th at goes in to th e cru ral cistern an d th e
ch oroidal fissu re.41 Th e size of th e ar ter y can be variable, ranging ■ Approaches to the Terminal ICA/A1,
from 0.5 to 2 m m . An eu r ysm s m ay arise in conju n ct ion w ith any
of th ese bran ch es. If th e an eur ysm projects in fero , postero , an d
PCoA, and AChA Aneurysms
su perolaterally, it is in close relat ion w ith th e m esial tem poral Th ree t yp es of cran iotom y ap proach es are com m on ly u sed to
lobe; an d, sim ilar to PCoA an eu r ysm s, it can be buried in th e p a m an age ICA an eur ysm s: pterion al, orbitozygom at ic, an d lateral
ren chym a.4,5 Th ese an eu r ysm s rarely com e in to con t act w ith th e su p raorbit al. Det ails of th e m acro an d m icrosu rgical tech n iqu es
oculom otor n er ve an d com m on ly reside above th e ten torium . are described in th e follow ing su bsect ion s, as w ell as th e advan
Widely opening an d adequ ately dissect ing th e sylvian fissu re fa tages an d disadvan t ages of each approach .
cilitates ident ificat ion of th e ACh A. Th e arter y m ay t ravel m edial
to th e an eu r ysm an d adh ere to th e dom e at it s cistern al segm en t .
Th e ACh A sh ou ld be p reser ved at all cost s, an d th e ar ter y m u st Pterional Approach
be dissected off of th e an eu r ysm dom e. Th e pat ien t is p osit ion ed su p in e w ith t h e h ead placed in a th ree
poin t fixat ion , exten ded an d t ilted to th e op posite side (abou t
20 degree t ilt). If th e h ead is t ilted m ore th an 30 degrees, th e
tem poral lobe “falls” on to th e surgeon’s corridor w h en th e syl
■ Possible Surgical Complications of vian fissu re is being open ed. Th e n eck is flexed to allow gravit y
Terminal ICA/A1, PCoA, and AChA to ret ract t h e fron t al lobe aw ay from t h e an ter ior sku ll base,
m in im izing th e n eed of ret ract ion . A cu r vilin ear in cision is m ade
Aneurysms beh in d th e h airlin e st ar t ing from w ith in 1 cm of th e t ragus at th e
In gen eral, th e surgical ou tcom e of ICA bifu rcat ion an d PCoA an level of th e zygom at ic root to m id lin e. Th e skin flap is reflected
eu r ysm s is relat ively good. In a series of 55 ICA term in u s an eu an ter iorly an d t h e p er icran iu m is reflected as a vascu lar flap
r ysm s t reated su rgically, 49 (89.1%) h ad a good ou tcom e an d did based fron t ally. To p reser ve th e fron t alis bran ch of t h e facial
n ot en tail any n eurologic deficit s.4 Leh ecka et al42 repor ted a n er ve, t h e tem p oralis m u scle is d issected u sing an in ter fascial
large series of ICA bifu rcat ion an eu r ysm s in w h ich th e m orbidit y dissect ion an d reflected in feriorly, leaving a m uscle cu ff along
of th e su rgical m an agem en t w as related to th e preser vat ion of th e su perior tem p oralis lin e to su t u re th e m u scle to at closu re.
th e perforators arou n d th e an eu r ysm , especially th ose p erfora Tw o burr h oles are m ade at th e keyh ole an d just above th e zygo
tors com ing off th e posterior w all of th e ICA bifurcat ion . In t ra m at ic root . Th e cran iotom y is perform ed w ith a foot plated cra
operat ive rupt ure is n ot un com m on an d is related to lift ing th e n iotom e. Th e m edial supraorbit al cut of th e cran iotom y exten ds
fron t al lobe an d dislocat ion of th e ICA w h ile th e an eu r ysm ’s to t h e lateral bord er of t h e su p raorbit al n otch an d is exten d ed
dom e is st ill adh eren t to th e fron t al lobe. Th e risk of ru pt u re is as low as possible dow n to th e cran ial base. Th e bon e flap is ele
h igh er for th e an teriorly project ing ICA bifurcat ion an eur ysm s. vated, and hem ostasis of the m iddle m eningeal arter y branches is
For PCoA an eu r ysm s, th e overall su rgical ou tcom e is gen erally done w ith a bipolar elect rocauter y. The sphenoid ridge is drilled
good . In Yaşargil’s 4 ser ies of 173 p at ien t s w it h r u pt u red PCoA flat un t il th e superior orbit al fissu re is exposed. Th e m en ingo
an eur ysm s w h o u n der w en t su rger y, 144 (83.2%) h ad a good to orbit al ban d is coagu lated an d divid ed . Th e d u ra is t acked u p
excellen t recover y.4 Nin eteen (16.8%) rem ain ed w ith som e n eu to th e bon e edge. Th e du ra is open ed w ith a cur vilin ear in cision

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510 V Cerebral and Spinal Aneurysms

a b c

d e

Fig. 43.2a–e (a) A patient presented with Hunt and Hess grade III sub- tion. (c) Despite these m aneuvers, a follow-up angiography showed com -
arachnoid hem orrhage (SAH). (b) Angiogram of the lateral view of the plete obliteration of the aneurysm s and absence of the AChA. (d,e) Axial
internal carotid artery (ICA) dem onstrates a PCoA aneurysm . The patient m agnetic resonance imaging (MRI) 24 hours after surgery dem onstrates
underwent a left craniotomy and aneurysm clipping. During surgery, the acute infarction in the AChA distribution. (Courtesy of Barrow Neurological
anterior choroidal artery (AChA) was dissected off of the aneurysm dom e, Institute.)
and the aneurysm was clipped, leaving the AChA out of the clip reconstruc-

an d reflected an teriorly. Th e du ra is covered on both sides w ith an eu r ysm s (Fig. 43.3). Th e p at ien t is p osit ion ed su p in e w it h
w et Telfa or cot ton oids to preven t dehydrat ion an d sh rin kage. t h e h ead placed in a th ree poin t fixat ion fram e. Th e h ead is po
Th e m icroscop e is brough t in to th e field. As in all vascu lar cases, sit ion ed u p righ t in a n eu t ral posit ion . Th e skin in cision is m ade
our preferen ce is to use th e m outh piece an d th e focus pedal, as directly th rough th e eyebrow or sligh tly above it , an d ru n s m edi
th ey facilit ate m an ip u lat ing th e m icroscope w ith ou t t aking th e ally from th e orbital n otch follow ing th e eyebrow an d cur ving
h an ds off th e in st r u m en ts. dow n laterally tow ard th e zygom at ic p rocess of th e orbit .47 Th is
in cision avoids th e fron t al bran ch of th e facial n er ve. Th e in cision
is taken dow n to th e pericran ium , w h ich is cut in a h orsesh oe
Orbitozygomatic Approach sh ap ed fash ion an d reflected in fer iorly. Th e tem p oralis m u scle
Th e orbitozygom at ic (OZ) ap proach is ver y u sefu l for large an eu is rem oved to expose th e keyh ole. A bu rr h ole is placed at th e
r ysm located h igh relat ive to th e cran ial base. Th is approach im keyh ole an d th e cran iotom y is fash ion ed w ith a cran iotom e foot
proves th e angle of at tack to ICA aneur ysm s w ith m in im al need of plate. Th e orbital bar is in clu ded in th e bon e flap . A h igh speed
ret ract ion on th e fron t al or tem poral lobes. It h as been dem on bu rr sh ou ld be u sed to p olish dow n th e orbit al roof to h ave a
st rated th at t h e angle of at t ack obt ain ed w as sign ifican tly greater st raigh t view in to th e basal cistern s. Th e dura is open ed w ith a
w ith t h e OZ ap p roach t h an w it h t h e pterion al ap p roach .44–46 cur vilin ear in cision w ith th e base dow n an d reflected in feriorly.
Ou r preferen ce is to p er for m an OZ cran iotom y for ICA an eu Th e m icroscope is brough t in to th e field . Th e fron tal lobe is gen
r ysm s. Th e tech n iqu e of th is su rgical ap p roach is d escr ibed in tly an d slow ly elevated from th e an terior skull base. Th e opt ic
Ch apter 88. an d carot id cister n s are reach ed an d op en ed to d rain cerebro
sp in al flu id (CSF) an d relax th e fron t al lobe. Th e p roxim al sylvian
fissure, th e ch iasm at ic cistern , an d th e ICA cistern s are open ed,
Lateral Supraorbital Approach an d m ore CSF is drain ed ou t . At th is p oin t , an ICA bifu rcat ion
Th e lateral su p raorbit al app roach p rovides access to cer t ain an an eu r ysm is visu alized an d dissected. Both th e ACA an d MCA are
terior circulat ion an eur ysm s in clu ding ACoA an d ICA bifurcat ion visualized an d dissected off of th e an eu r ysm , if n ecessar y. A

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43 Surgical Therapies for Saccular Aneurysm s of the Internal Carotid Artery 511

a b c

d e f

Fig. 43.3a–f A patient with an unruptured internal carotid artery (ICA) ping. Note the calcified atherosclerotic aneurysm (asterisk). (f) Follow-up
bifurcation aneurysm underwent elective surgical clipping via a right lateral coronal CTA dem onstrating complete obliteration of the aneurysm . ON,
supraorbital craniotomy. (a–c) Computed tom ography angiogram s (CTAs) optic nerve; ACA, anterior cerebral artery; MCA, middle cerebral artery.
dem onstrate a right 5-m m ICA bifurcation aneurysm (arrow). Intraopera- (Courtesy of Barrow Neurological Institute.)
tive im ages of the ICA bifurcation aneurysm before (d) and after (e) clip-

st raigh t clip is ap plied to occlu de th e an eu r ysm . Th e paten cy of a su bfron tal approach , to establish early proxim al con t rol over
th e ICA, ACA, an d MCA are revised after th e clipp ing. Du ra h as to th e sup raclin oid ICA. Th e surgeon sh ou ld m ain tain aw aren ess of
be closed in a w ater t igh t fash ion , an d th e fron tal sin us m ust be fron t al lobe ret ract ion an d th e possibilit y of an eu r ysm r u pt u re.
sealed . Th e pericran iu m is closed as a separate layer to m in im ize Iden t ificat ion of both A1 an d M1 segm en t s origin at ing from th e
th e likelih ood of CSF leak or in fect ion . Th e galea an d skin are base of t h e an eu r ysm is essen t ial. To visu alize t h ese vessels,
closed sep arately. exten sive arach n oid dissect ion of th e carot id, opt ic, an d sylvian
cistern s is n eed ed . Th e su p er ficial arach n oid of t h e sylvian fis
su re is d ivid ed an d t h e sylvian cister n is en tered . At t h is p oin t
Microsurgical Technique th e d issect ion p roceeds p roxim ally by spreading th e fissu re from
Su rger y is p erform ed w ith th e su rgeon seated. Th e sylvian fis in side out . Cau t ious ret ract ion of th e fron t al lobe is pr uden t .
sure is w idely op en ed to m in im ize brain ret ract ion . Th e surgeon After th e M1 h as been iden t ified, th e dissect ion con t in ues
can u se m icrosu ct ion an d m icrodissector/bip olar forcep s to keep along th e lateral surface to fin d th e an terolateral w all of th e ICA.
th e sylvian fissu re op en du ring th e en t ire procedu re. We rarely Medial dissect ion w ill reveal th e A1 segm en t . Som et im es th e A1
u se ret ractors for ICA an eu r ysm s. Our preferen ce is to do sh arp segm en t can be h idden beh in d an eu r ysm s th at p roject an teri
dissect ion w ith m icroscissors or an arach n oid kn ife. Th e sylvian orly. Th e goal is to iden t ify an d preser ve all bran ch es an d perfo
fissure is open ed on its fron t al side from dist al to proxim al an d rators in th e region of th e carot id bifu rcat ion so th at th eir cou rse
from in side out. Th e ICA and optic cistern s are opened. Dissection an d locat ion are clearly seen before clips are applied. For ICA/A1
of th e ICA sh ould be don e on th e an terosuperior surface un t il an eur ysm s, it is im por tan t to op en th e lam in a term in alis cistern
dist al an d proxim al con t rol is ach ieved. Th e opt icocarot id an d an d dissect A1 to avoid ret ract ion on ACA th at can poten t ially
oculocarot id t riangles are open ed. Th e dissect ion is con t in ued t ran sm it ten sion on th e an eu r ysm ’s fu n d u s, to iden t ify p erforat
on th e m edial aspect of th e ICA. ing arteries (arter y of Heu bn er), an d to assess ACoA an d con t ra
lateral circulat ion in case th e ipsilateral A1 n eeds to be p ar t ially
in cluded w ith in th e an eur ysm clip. If dealing w ith a r upt ured
Surgical Clipping of ICA/A1 Aneurysms an eur ysm , th e lam in a term in alis is open ed for CSF drain age. Th e
After th e sylvian fissure h as been w idely open ed in a dist al to PCoA an d ACh A are id en t ified an d t h eir cou rses are n oted in
proxim al d irect ion in u n r u pt u red cases, a sm all ar ter y from th e relat ion to th e an eu r ysm . Dissect ion u n dern eat h th e bifu rcat ion
ICA to th e dura (ar ter y of th e dura of th e an terior clin oid process) is im p ortan t to iden t ify perforators from th e PCoA an d ACh A as
is coagu lated an d divided. Th is sm all arter y origin ates from th e w ell as th e vein of Rosen th al before th e clip is applied.
an ter ior w all of t h e ICA, 3 to 5 m m p roxim al to t h e bifu rcat ion . Th e an eu r ysm can be bu ried in p aren chym a of th e basal fore
In th e presen ce of SAH, it is w ise to begin th e m icrodissect ion via brain , an d a sm all cor t ical open ing m ay be n ecessar y. Th e an eu

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512 V Cerebral and Spinal Aneurysms

r ysm is d issected from t h e ACA an d t h e MCA an d t h e ar ter y p roblem . W ith large PCoA an eu r ysm s, t h e ACh A is u su ally cov
of Heu bner is iden t ified. A tem porar y clip facilitates dissect ion ered an d adh eren t to th e fun dus. Perforat ing ar teries arising di
aroun d the n eck an d fun dus. Th e tem porar y clip is applied distal rectly ben eath th e bifurcat ion are bran ch es of th e ACh A th at can
to th e ACh A in a perforator free zon e. Som et im es tem porar y be follow ed proxim ally to iden t ify th e ACh A. If th e an eur ysm is
clips on A1 and M1 are necessary. Usually, a straight clip is applied buried in th e tem poral lobe an d th e ACh A is n ot visualized, sub
perpen dicu lar to th e ACA an d MCA, slow ly w iggling bet w een th e pial resect ion of th e m esial tem p oral lobe an d adh esion s releases
an eur ysm an d th e ACA/MCA. Som et im es it is n ecessar y to sh ape th e an eu r ysm fu n d u s an d exp oses th e ACh A. After th e p roxim al
th e an eur ysm n eck w ith bipolar coagu lat ion , esp ecially in cases an d dist al en d of th e an eur ysm h as been visualized, a st raigh t or
w ith broad n ecks. Th e clip’s length sh ould be on e an d a h alf a righ t angle fen est rated clip m ay be used to occlu de th e an eu
t im es th e w idth of th e an eu r ysm . An in it ial pilot clip can be ex r ysm . A sm all p or t ion of t h e n eck is left to m ain t ain t h e caliber
ch anged for a fin al clip after bip olar resh ap ing of th e dom e an d of th e ICA. Tips of th e clip are in spected to verify paten cy of th e
n eck. Clip applicat ion is along th e a xis of M1, placing th e clip PCoA, PCoA perforators, an d ACh A.
bet w een th e ACA an d MCA to avoid ICA bifu rcat ion sten osis.
Mu lt ip le clips are requ ired for t h ick w alled or w ide n ecked an
Intradural Anterior Clinoidectomy
eur ysm s. Th e clip m ay slide dow n tow ard th e ICA term in at ion
w h ere the origin s of A1 an d M1 are, an d m ay lim it th e flow in to Preop erat ive evalu at ion of th e ICA in relat ion to th e bon e st ru c
the ACA an d MCA. In docyan ine green injection is especially help t u res is n ecessar y to an t icip ate th e n eed of cer vical carot id con
ful in en su ring paten cy of t h e ACA an d MCA. In cases of ru pt u red t rol or an terior clin oid process resect ion . Th e clin oidal du ra is
an eur ysm s w ith a large ICH an d lack of space, a sm all cort ical separated laterally an d is drilled w ith a 2 m m diam on d bit from
in cision is m ade accordingly, avoiding Broca’s area, to evacu ate a m edial to lateral direction (aw ay from the optic nerve to the su
t h e h em atom a. In t racerebral h em atom a in t h e im m ed iate vi perior orbital fissu re) u n t il th e opt ic st ru t is reach ed an d d rilled.
cin it y of th e an eur ysm sh ould be left in place un t il proxim al an d In select cases, it m ay be n ecessar y to open th e dist al dural ring
distal con t rol is obtain ed. an d th e falciform ligam en t .

Surgical Clipping of PCoA Aneurysms Surgical Clipping of AChA Aneurysms


After th e sylvian fissure h as been w idely open ed, th e opt icoca After the sylvian fissure has been w idely opened, the interpedun
rot id t riangle is also op en ed an d dissect ion of t h e m edial aspect cular, carot id, opt ic, an d lam in a term in alis cistern s are open ed
of ICA is con t in ued. Th e origin s of th e PCoA, th e PCoA perfora w ith th e sam e tech n ique as for PCoA an eu r ysm s. Th e PCoA an d a
tors, an d th e ACh A are iden t ified. As previously m en t ion ed, our sect ion of th e ICA sh ou ld be dissected free an d h ave sp ace for a
preferen ce is to avoid brain ret ractors. A PCoA an eu r ysm can be tem porar y clip in case of prem at ure ru pt u re. Next , th e ACh A an d
at tach ed to p arah ip pocam pal gyr u s or u n cu s an d a ret ractor on its bran ch es sh ould be iden t ified an d dissected free as w ell. Th e
th e tem poral lobe cou ld poten t ially avu lse th e dom e of th e an eu an eur ysm ’s n eck is dissected an d th e ACh A is m obilized from th e
r ysm . On th e oth er h an d, an terom edial ret ract ion on th e ICA can an eur ysm fun du s. Th e clip is gen tly applied on th e an eur ysm ’s
p u ll on t h e an eu r ysm if it is at t ach ed to t h e tem p oral lobe, ten n eck. Som et im es a piece of Gelfoam (Pfizer, New York, NY) is in
torium , or oculom otor n er ve. Dissect ion of th e an eu r ysm dom e ser ted bet w een th e an eu r ysm an d th e ACh A to keep th e ar ter y
from th e ocu lom otor n er ve sh ou ld be avoided becau se t ract ion separated from th e an eu r ysm . W h ile th e clip is applied , th e sur
can result in irreversible ner ve dam age. A decrease in arterial pul geon sh ou ld obser ve th e ICA for possible kin king. Th e ACh A an d
sat ion after an eu r ysm clip p ing is adequ ate for ocu lom otor n er ve its bran ch es are in spected for in tegrit y. Th e t ip of th e an eur ysm
palsy resolu t ion . Placem en t of a tem porar y clip on th e p roxim al clip is also in sp ected.
su p raclin oid ICA facilit ates n eck d issect ion an d clip p lacem en t .
If available, in t raop erat ive m on itor in g is u sefu l in evalu at ing
toleran ce to flow arrest . If m on itoring is n ot available, usually Surgical Clipping of Blood Blister–Like and
altern at ing 3 an d 5 m in utes of occlusion an d reperfusion , re Ventral ICA Trunk Aneurysms
spect ively, is gen erally w ell tolerated. It is im por tan t to open th e
Blood Blister–Like (BBL) Aneurysms
lam in a term in alis cistern above both opt ic n er ves an d ACAs to
fu r th er m obilize th e fron t al lobe w ith ou t t ran sm it t ing th e force Th ese an eu r ysm s are broad based an d t h in w alled , w it h n o
of th e ret ract ion to th e an eur ysm . Open ing of th e lam in a term i an atom ic n eck. Th ey are m ore fragile th an saccular an eur ysm s.
n alis cistern en ables th e su rgeon to evaluate cross circulat ion Usu ally t h ey are sm all an d d ifficu lt to d iagn ose. Th ey accou n t
from th e ACoA an d ACAs. Th e origin of th e PCoA is u su ally ju st for 0.3 to 1% of in t racran ial an eur ysm s an d 0.9 to 6.5% of an eu
proxim al to th e an eu r ysm on th e p osterolateral w all of th e ICA. r ysm s of th e ICA. Th ese lesion s are a h em isph eric prot uberan ce
Th e m edial side of t h e ICA is explored by gen tly elevat ing an d arising from a nonbranching segm ent in the supraclinoid portion
pu sh ing th e ICA laterally w ith a su ct ion t ip can n u la. Th is exp oses of th e ICA (Fig. 43.4). Th e n at u ral h istor y an d p ath ophysiology of
th e real d im en sion s of th e PCoA, p erforators, an d an eur ysm . th ese lesion s are u n clear, bu t th ey can resu lt as a con sequ en ce of
ar ter ial d issect ion . Th ey h ave a focal w all d efect w it h absen ce
of in tern al elast ic lam in a an d m edia. Th e gap is covered w ith
Identification of the AChA
th in adven t it ia an d fibrin ou s t issu e. In ou r op in ion , en d ovascu lar
Som e of th e m orbidit y of PCoA an eu r ysm su rger y resu lt s from em bolizat ion is n ot an ad equ ate an d d u rable opt ion for t h ese
ACh A occlu sion ; th erefore, its early iden t ificat ion is im perat ive. an eur ysm s. Collateral flow sh ou ld be st u died preoperat ively be
With sm all PCoA an eur ysm s, iden t ificat ion of th e ACh A is n ot a cau se an eu r ysm lacerat ion d u ring exp lorat ion is n ot u n com m on

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43 Surgical Therapies for Saccular Aneurysm s of the Internal Carotid Artery 513

a b c d

e f g

Fig. 43.4a–g A 26-year-old wom an who presented with a Hunt and Hess anterior cerebral artery (ACA) to isolate the diseased segm ent of the ICA
grade III subarachnoid hem orrhage (SAH). (a) Axial computed tom ography (asterisk) from the cerebral circulation. Note the oculom otor nerve (CN III)
(CT) of the head dem onstrates diffuse SAH and bifrontal intracranial lateral to the ICA. (f) After rem oving the blood clot over the blister aneu-
hem orrhage (ICH). (b,c) Anteroposterior (AP) and lateral views of the inter- rysm , the inside of the ICA was visualized. An aneurysm clip could not be
nal carotid artery (ICA) injection dem onstrate a dorsal ICA aneurysm . applied. The rem ainder of the diseased ICA was transected (asterisks). Som e
(d) Three-dim ensional (3D) reconstruction demonstrating a blood blister– ICA perforators can be visualized (arrowheads). The surgical procedure was
like dorsal ICA aneurysm . Note the narrowing (arrow) of the ICA proxim al to completed with a superficial temporal artery (STA)-MCA bypass. (g) Post-
the aneurysm , suggesting ICA dissection and associated blister-like aneu- operative magnetic resonance angiography (MRA) demonstrates patency of
rysm s. (e,f) Intraoperative im ages of the aneurysm . (e) Three vascular clips the bypass (arrow) filling the MCA territory. Note the absence of the supra-
have been applied to the proxim al ICA, m iddle cerebral artery (MCA), and clinoid segm ent of the ICA.(Courtesy of Barrow Neurological Institute.)

an d th e ICA m ay h ave to be sacrificed. Proxim al con t rol is m an


datory, usually at the cer vical carotid level. Direct clipping or clip
■ Clinical Outcome After ICA/A1, PCoA,
w rapping is usually th e m ost secure an d durable tech n ique.48 An and AChA Aneurysm Surgery
en circling clip is an oth er opt ion .49 Direct clip ping h as been re
Sim ilar to ot h er in t racran ial an eu r ysm s, t h e ou tcom e after su r
pu ted to be h azardou s becau se of th e h igh er rep or ted in ciden ce
gical m an agem en t of ICA an eu r ysm s h as dram at ically im proved
of in t raop erat ive r u pt u re as w ell as p aren t vessel n ar row in g,
sin ce th e in t roduct ion of m icrosurgical tech n iqu es. In Yaşargil’s 4
alth ough th is h as n ot been our experien ce. Oth er surgeon s h ave
series of 51 p at ien t s w ith ru pt u red ICA bifu rcat ion an eu r ysm s,
prop osed app lying th e clip parallel to th e carot id, taking p ar t of
49 (89%) h ad good ou tcom es w ith ou t focal n eurologic deficits.
th e n orm al ar ter y w all an d produ cing a sm all sten osis of th e ICA.
Th is grou p of p at ien t s h ad a Hu n t an d Hess SAH grade of 0b to
Th e m ost im p or t an t asp ect s of m an aging th is kin d of an eu r ysm
IVb. On e pat ien t w ith a grade V SAH died. In th e sam e series, for
are aneur ysm diagnosis and proxim al control planning.50,51 W hen
t h e PCoA an eu r ysm grou p of 131 p at ien t s, Yaşargil rep or ted
approach ing th ese an eur ysm s it is pr uden t to n ot m an ipulate
good outcom es in all pat ien ts w ith a grade of 0a to Ia, 88.3%good
th e clot associated w ith th e site of h em orrh age u n t il vascu lar
outcom es for grades IIa to IIIa, 37.5% for grade IIIb, an d 20% for
con t rol is obt ain ed.
grade IV. Oculom otor n er ve palsy resolut ion is an im por t an t
variable in PCoA an eur ysm outcom e. Gü resir et al52 repor ted re-
su lts from a m eta an alysis from p at ien ts w ith PCoA an eu r ysm
Ventral ICA Trunk Aneurysms
oculom otor n er ve palsy an d fou n d a sign ifican tly high er rate of
Th ese an eu r ysm s p roject in fer iorly in to t h e in ter p ed u n cu lar com p lete ocu lom otor n er ve p alsy resolu t ion for pat ien t s w h o
cistern . Th ey are usually large an d lack a w ell defin ed n eck, an d u n der w en t m icrosu rgical clip ping com pared w ith en dovascu lar
are often fusiform , par t ially th rom bosed, an d h ave calcificat ion s. coiling an d sp on t an eou s cou rse. Wir th et al53 foun d th at PCoA
Th e origin s of t h e PCoA an d ACh A m igh t be in clu ded w ith in th e an eur ysm s h ad th e low est operat ive m orbidit y (5%) com pared
an eur ysm . Given th e rarit y of th ese lesion s, th ere is lit tle con w ith oth er locat ion s. Friedm an et al43 pu blish ed th eir resu lt s on
sen su s on th e best t reat m en t regim en for t h ese lesion s. Opt ion s th e su rgical m an agem en t of 51 ACh A an eu r ysm s in w h ich 82%
for t reat m en t of t h ese an eu r ysm s in clu d e creat ion of a n eck for ach ieved a GOS score of 4 or 5. Eigh t (16%) p at ien t s h ad ACh A
clipping, endovascular em bolization w ith or w ith out a sten t , and ter r itor y in farct ion s. Five of t h ose in farct ion s m an ifested in a
ICA ligat ion or ICA t rap ping w ith or w ith ou t revascularizat ion . d elayed fash ion , 6 to 36 h ours after th e operat ion . Th is series

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514 V Cerebral and Spinal Aneurysms

in clu ded p at ien ts from as far back as 1968, w h en m odern m icro eu r ysm s.4 Large an eu r ysm s are also com m on ly seen at th e ICA
n eu rosu rger y tech n iqu es w ere n ot w ell d evelop ed . In a large bifurcat ion an d less frequ en tly at th e PCoA.34 Also, PCoA an d
series of 99 ACh A an eu r ysm s, Leh ecka et al36 described th e m ain ACh A an eu r ysm s frequ en tly presen t w ith an int raparen chym al
difficu lt y du ring su rger y to be preser vat ion of flow in th e ACh A h em atom a (tem poral lobe) an d subdural h em atom a requ iring
origin at ing at th e base of th e an eu r ysm an d of th ose at tach ed to surgical evacuation. Wide neck aneurysm s are seen at th e ICA bi
th e an eu r ysm ’s dom e. Preser vat ion of th e ACh A w ill u lt im ately furcat ion w here part of th e w ide n eck involves th e ACA or MCA.
determ in e th e ou tcom e for ACh A an eu r ysm s. En d ovascu lar coiling h as becom e m ore com m on for PCoA an eu
r ysm s. Th e angiograp h ic view of th e n eck an d m icrocath eter ac
cess are t ypically m uch sim pler than w ith other aneur ysm s.54 The
m ajor draw back of en dovascu lar coiling is th e h igh recu rren ce
rate. Raym on d et al55 fou n d an overall recu rren ce in 33.6%, an d
■ Treatment Decision for ICA/A1, PCoA, m ajor recurren ce requiring ret reat m en t in 20.7% of coiled an eu
and AChA Aneurysms: Clip or Coil? r ysm s. PCoA an eu r ysm s h ad th e secon d h igh est recurren ce rate
(37.2%) of all in t racran ial an eur ysm s. A st udy looking at m ajor
Th e t w o m ost recen t prosp ect ive, ran dom ized con t rolled t rials
recu rren ce of an eur ysm s t reated d uring th e ISAT t rial foun d th at
com p aring su rgical clipp ing an d en dovascu lar coiling of ru p
coiled an eu r ysm s in th e PCoA locat ion h ad a sign ifican tly h igh er
t u red in t racran ial an eu r ysm s, th e ISAT an d BRAT, h ave sh ow n
risk of recu rren ce requ iring re em bolizat ion .56
th at p at ien t s in t h e clip grou p h ad a sign ifican tly h igh er degree
of an eur ysm obliterat ion an d a sign ifican tly low er rate of recur
ren ce an d ret reat m en t . In th e BRAT t rial, based on m RS scores at
3 years, th e outcom e of all pat ien t s assign ed to coil em bolizat ion
sh ow ed a favorable absolu te differen ce com p ared w ith th e ou t
■ Conclusion
com e of th ose assign ed to clip occlu sion , bu t th is differen ce w as An eur ysm s arising from th e ICA are com m on lesion s. An eur ysm s
n ot stat ist ically sign ifican t .32 As w ith any oth er in t racran ial an arising from each sp ecific dom ain of th e ICA h ave a dist in ct pro
eu r ysm s, th e ideal tech n iqu e for ICA/A1, PCoA, an d ACh A an eu file of in ciden ce, clin ical presen tat ion , an atom ic ch aracterist ics,
r ysm treatm ent should offer the best sh ort and long term results. operat ive n uan ces, com plicat ion s, ou tcom e, an d progn osis. Th e
Factors t h at favor su rgical clip p in g are you n g p at ien t age, t h e operat ive field to access th ese lesion s is n arrow, an d surroun ding
sm all size of t h e an eu r ysm , th e p resen ce of in t racran ial h em a st r u ct u res h ave lim ited m obilit y (ICA itself, an terior clin oid pro
tom a, an d a n eck to d om e rat io greater t h an 0.5. Du rabilit y of cess, opt ic an d oculom otor n er ves, pet roclival ligam en t). Precise
t reat m en t is essen t ial in you ng pat ien ts; it is in terest ing to n ote and m eticulous m icrosurgical techniques are necessary to ensure
th at you ng p at ien t s are m ore likely to h arbor ICA bifu rcat ion an favorable ou tcom es.

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24. Abbie AA. Th e blood supply of th e lateral gen iculate body, w ith a n ote on in tern al carot id arter y bifurcat ion an eur ysm s. Surg Neurol 2009;71:649–
th e m orp h ology of th e ch oroidal ar teries. J An at 1933;67(Pt 4):491–521 667
25. Rh oton A. Th e cerebral vein s. In : Rhoton A, ed. Cran ial An atom y an d Sur 43. Friedm an JA, Pich elm an n MA, Piepgras DG, et al. Ischem ic com plicat ion s
gical Approaches. Ph iladelphia: Lippin cot t William s & Wilkin s, Sch aum of surger y for an terior choroidal ar ter y an eur ysm s. J Neurosurg 2001;
burg; 2003, p. 187–234 94:565–572
26. In tern at ion al St udy of Un rupt ured In t racran ial An eur ysm s Invest igators. 44. Figueiredo EG, Desh m ukh P, Zabram ski JM, et al. Quan t it at ive an atom ic
Un ru pt u red in t racran ial an eu r ysm s—risk of ru pt u re an d risks of su rgical st u dy of th ree su rgical ap p roach es to th e an terior com m u n icat ing ar ter y
in ter ven t ion . N Engl J Med 1998;339:1725–1733 com plex. Neurosurger y 2005;56(2, Suppl):397–405, discu ssion 397–405
27. W iebers DO, W h isn an t JP, Hu ston J III, et al; In ter n at ion al St u dy of Un 45. Gon zalez LF, Craw ford NR, Horgan MA, Desh m u kh P, Zabram ski JM,
r u pt ured Int racranial An eur ysm s Invest igators. Un rupt ured int racran ial Sp et zler RF. Working area an d angle of at t ack in th ree cran ial base ap
an eur ysm s: n at ural h istor y, clin ical outcom e, an d risks of surgical an d p roach es: pter ion al, orbitozygom at ic, an d m a xillar y exten sion of t h e
endovascular t reat m en t . Lan cet 2003;362:103–110 orbitozygom at ic ap p roach . Neu rosu rger y 2002;50:550–555, discu ssion
28. Broderick JP, Sauerbeck LR, Forou d T, et al. The Fam ilial In t racran ial Aneu 555–557
r ysm (FIA) st udy protocol. BMC Med Gen et 2005;6:17 46. Figueiredo EG, Desh m ukh P, Nakaji P, et al. An an atom ical an alysis of the
29. Mackey J, Brow n RD Jr, Moom aw CJ, et al; FIA an d ISUIA Invest igators. m in i m odified orbitozygom at ic an d supra orbit al approach es. J Clin Neu
Un ru pt u red in t racran ial an eu r ysm s in th e Fam ilial In t racran ial An eu r ysm rosci 2012;19:1545–1550
an d In tern at ion al St u dy of Un r u pt u red In t racran ial An eu r ysm s coh or t s: 47. Kang HJ, Lee YS, Suh SJ, Lee JH, Ryu KY, Kang DG. Com parat ive an alysis of
differen ces in m u lt ip licit y an d locat ion . J Neu rosu rg 2012;117:60–64 th e m in i pterion al an d su p raorbit al keyh ole cran iotom ies for u n r u pt u red
30. Molyn eu x A, Kerr R, St rat ton I, et al; In tern at ion al Subarach n oid An eu an eu r ysm s w ith n um eric m easurem en t s of their geom et ric con figura
r ysm Trial (ISAT) Collaborat ive Group. In tern at ion al Su barach n oid An eu t ion s. J Cerebrovasc En dovasc Neurosurg 2013;15:5–12
r ysm Trial (ISAT) of n eurosurgical clipping versu s en dovascular coiling in 48. Kalan i MY, Zabram ski JM, Kim LJ, et al. Long ter m follow u p of blister
2143 pat ien t s w ith rupt u red in t racran ial an eur ysm s: a ran dom ised t rial. an eur ysm s of th e in tern al carot id ar ter y. Neurosurger y 2013;73:1026–
Lan cet 2002;360:1267–1274 1033, discussion 1033
31. Morit a A, Kirin o T, Hash i K, et al; UCAS Japan Invest igators. Th e n at ural 49. Park PJ, Meyer FB. Th e Su n dt clip graft . Neu rosu rger y 2010;66(6, Su p p l
cou rse of un rupt ured cerebral aneu r ysm s in a Japan ese coh ort . N Engl J Op erat ive):300–305, discu ssion 305
Med 2012;366:2474–2482 50. Regelsberger J, Mat sch ke J, Grzyska U, et al. Blister like an eu r ysm s—a
32. Spet zler RF, McDougall CG, Albuquerque FC, et al. Th e Barrow Rupt ured diagn ost ic an d th erapeut ic ch allenge. Neurosu rg Rev 2011;34:409–416
An eu r ysm Trial: 3 year resu lt s. J Neurosu rg 2013;119:146–157 51. McLaugh lin N, Laroch e M, Bojan ow ski MW. Surgical m an agem ent of
33. van Rooij W J, Slu zew ski M, Beute GN. In tern al carot id bifurcat ion an eu blood blister like an eur ysm s of th e in tern al carot id ar ter y. World Neuro
r ysm s: frequen cy, angiograph ic an atom y an d resu lt s of coiling in 50 an su rg 2010;74:483–493
eur ysm s. Neu roradiology 2008;50:583–587 52. Gü resir E, Sch uss P, Seifer t V, Vat ter H. Oculom otor n er ve palsy by poste
34. Velat GJ, Zabram ski JM, Nakaji P, Spet zler RF. Surgical m an agem en t of rior com m un icat ing ar ter y an eur ysm s: in fluen ce of su rgical st rategy on
giant posterior com m un icat ing arter y an eur ysm s. Neurosurger y 2012; recover y. J Neurosurg 2012;117:904–910
71(1, Suppl Operat ive):43–50, discu ssion 51 53. Wir th FP, Law s ER Jr, Piepgras D, Scot t RM. Surgical t reat m en t of in ciden
35. Heros RC. Micron eurosurgical m anagem en t of an terior ch oroidal ar ter y t al in t racran ial an eur ysm s. Neurosurger y 1983;12:507–511
an eu r ysm s. World Neu rosu rg 2010;73:459–460 54. Golshan i K, Ferrell A, Zom orodi A, Sm ith TP, Brit z GW. A review of th e
36. Leh ecka M, Dash t i R, Laakso A, et al. Micron eurosu rgical m an agem ent of m an agem en t of posterior com m u nicat ing ar ter y an eur ysm s in th e m od
an terior ch oroid ar ter y an eu r ysm s. World Neu rosu rg 2010;73:486–499 ern era. Surg Neurol In t 2010;1:88
37. Ku zm ik GA, Bulsara KR. Microsurgical clipping of t r ue posterior com m u 55. Raym ond J, Guilber t F, Weill A, et al. Long term angiograph ic recurren ces
n icat ing ar ter y an eur ysm s. Act a Neuroch ir (Wien ) 2012;154:1707–1710 after select ive en dovascular t reat m en t of an eur ysm s w ith det ach able
38. Nakan o Y, Saito T, Yam am oto J, et al. Surgical t reat m en t for a r upt ured coils. St roke 2003;34:1398–1403
t rue posterior com m un icat ing arter y an eur ysm arising on th e fet al t ype 56. Cam pi A, Ram zi N, Molyn eu x AJ, et al. Ret reat m en t of r upt ured cerebral
posterior com m u n icat ing ar ter y—t w o case repor t s an d review of th e lit an eu r ysm s in p at ien t s ran d om ized by coiling or clip p ing in t h e In ter
erat ure. J UOEH 2011;33:303–312 nat ional Subarach noid Aneur ysm Trial (ISAT). Stroke 2007;38:1538–1544
39. Ch ang DJ. Th e “n o drill” tech n ique of an terior clin oidectom y: a cran ial
base approach to th e paraclin oid an d parasellar region . Neu rosurger y
2009;64(3, Suppl):on s96–on s105, discussion on s105–on s106

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44 Endovascular Therapies for Aneurysms
of the Internal Carotid Artery
Tarek Y. El Ahm adieh, Najib E. El Tecle, Salah G. Aoun, Allan Douglas Nanney III,
Joseph G. Adel, and Bernard R. Bendok

Over the past t w o decades, advances in endovascular technology, In a st udy by Beck et al,9 an eur ysm s of th e ICA w ere foun d to
tech n iques, an d st rategies h ave expan ded th e toolbox available rep resen t 14.7% of all rupt u red an eu r ysm s greater th an or equ al
to th e n eurovascular specialist . It is curren tly feasible to perform to 7 m m in diam eter, an d 4.1% of all rupt ured an eur ysm s less
en d ovascu lar p rocedu res on com plex vascu lar lesion s th at w ere th an 7 m m in diam eter.
previou sly con sid ered u n t reatable or w ere associated w ith h igh
t reat m en t-related m orbid it y.1 Th e n ew ch allenge, h ow ever, h as
becom e t h e ju d iciou s m atch ing of t h e p at h ology to t h e cor re-
sp on d ing st rategies an d tech n iqu es t h at carr y t h e best sh or t -
an d long-term ou tcom e w ith th e least am ou n t of com p licat ion s.
■ Embryology
An eur ysm s of th e in tern al carot id ar ter y (ICA) represen t 30 to Th e cer vical segm en t of th e ICA is derived from em br yological
50% of all in t racran ial an eur ysm s.2,3 Th ese lesion s can presen t th ird aor t ic arch es, w h ereas in t racran ial segm en t s of th e ICA are
sign ifican t en dovascu lar as w ell as su rgical ch allenges. Pet rou s form ed from th e dorsal aor t a.10 Alterat ion s in early em br yologi-
an d cavern ous segm en t an eu r ysm s, for exam ple, are em bedded cal develop m en t of th e cerebral vascu lat u re m ay lead to d iverse
in com plex su rroun ding an atom y, w h ich com p licates op en su r- an atom ic var iat ion s an d abn or m alit ies. For exam p le, d evelop -
gical approach es. Th ese lesion s, h ow ever, can be m an aged u sing m en t al failu re of t h e t h ird aor t ic arch m ay lead to agen esis or
various decon st r uct ive an d recon st r uct ive en dovascular st rate- hypoplasia of th e ICA. An oth er exam ple is th e fen est rat ion or
gies.4 Paraclin oid an eu r ysm s can be ap p roach ed su rgically or par t ial du p licat ion of a specific segm en t of th e ICA. Th is is often
en d ovascu larly u sin g var iou s tech n iqu es t h at sh ou ld be in d i- associated w ith saccu lar an eur ysm form at ion at th e fen est rated
vid u alized . Hybr id tech n iqu es can be h elp fu l for select lesion s segm en t an d can p resen t an en dovascu lar ch allenge to th e t reat-
in th is locat ion .5 En dovascular th erapy carries th e ch allenge of in g p hysician . Sim ilarly, t h e p resen ce of a fet al-t yp e PCoA can
ach ieving com plete occlusion of th e an eur ysm w ith preser vat ion pose both su rgical an d en dovascu lar ch allenges.
of th e oph th alm ic ar ter y an d avoidan ce of opt ic n er ve m ass ef-
fect.6 Issues involving the posterior com m un icat ing artery (PCoA)
segm en t in clu de p aren t ar ter y preser vat ion (an terior ch oroidal
an d fetal-t ype PCoAs in par t icular), as w ell as m ass effect issues
related to th e th ird n er ve. Carot id term in u s an eu r ysm s can u su-
■ Anatomic Considerations
ally be t reated w ith stan dard en dovascular tech n iques w h erein A w idely accepted n om en clat ure of th e ICA segm en ts is th e on e
preser vat ion of an terior cerebral ar ter y (ACA) an d m iddle cere- p rop osed by Bou t h illier et al 11 d escr ibin g seven segm en t s of
bral ar ter y (MCA) an atom y is a prim ar y con cern . En dovascu lar t h e ICA, n u m bered from C1 to C7. Th ese segm en t s are n am ed th e
th erap ies in clu de decon st ru ct ive an d recon st ru ct ive ap proach es. cer vical, p et rou s, lacer u m , caver n ou s, clin oid , op h t h alm ic, an d
Deconst ruct ive approaches usually require balloon test occlusion com m u n icat in g, m ovin g con secu t ively from cau dal to rost ral.
to d eter m in e t h e p oten t ial n eed for byp ass. Recon st r u ct ive Th e cou rse of th e cer vical (C1) segm en t of t h e ICA, as it app ears
st rategies in clu d e coilin g w it h assist d evices, balloon rem od el- on digital su bt ract ion angiography, is st raigh t in up to 70% of
in g, sten t -assisted coiling, flow diversion , an d p ar t ial coiling cases.12 W it h in t h e carot id can al, t h e len gt h an d sh ap e of t h e
w it h d elayed clip p ing. Th is ch apter discu sses th e epidem iology p et rous (C2) segm en t of th e ICA is determ in ed by th e con figura-
of an eu r ysm s ar isin g from t h e ICA, t h eir related su rgical an d t ion of th e p et rou s an d sp h en oidal bon es. Th e p et rou s segm en t
rad iological an atom y, classificat ion , n at u ral h istor y, an d clin ical h as a 1-cm upw ard course th rough th e th ickn ess of th e cran iu m ,
presentation, as well as current endovascular treatm ent strategies. follow ed by a sh arp an terior ben d to form th e h orizon tal pet rous
segm en t .11 From th e p et rou s apex, th e ICA exten ds su periorly
an d m edially tow ard th e sella t u rcica defin ing th e laceru m (C3)
segm en t . It t h en ascen d s ver t ically an d en ters t h e caver n ou s
sin u s.
■ Epidemiology Th e cavern ou s (C4) segm en t of th e ICA is d ivided in to five
An eur ysm s of th e pet rous segm en t of th e ICA are relat ively rare. par t s: (1) th e posterior ver t ical segm en t, (2) th e p osterior ben d,
Cavern ou s segm en t an eu r ysm s an d carot id term in u s an eu r ysm s (3) th e h orizon tal segm en t , (4) th e an terior ben d, an d (5) th e
each represen t 2 to 9%of all in t racran ial an eur ysm s,7,8 an d an eu - anterior vertical segm ent.13 On lateral projection, those five parts
r ysm s of th e clin oid, oph th alm ic, an d com m u n icat ing segm en ts h ave an S-sh aped con figu rat ion defin ing th e carot id siph on . On
represen t 20 to 25%. Su barach n oid h em orrh age is by far th e m ost an terop oster ior p roject ion , t h e p oster ior an d an ter ior ver t ical
seriou s acu te presen tat ion of pat ien ts w ith saccu lar an eu r ysm s. segm en t s are su p er im p osed .11 Th e p oster ior-ben d bran ch es of

516

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th e cavern ou s ICA m ay arise as a com m on t ru n k, m en ingohy- 2. Superior hypophyseal artery aneurysm s: Usually h ave an in -
pop hyseal t ru n k, or as separate vessels. Th ese m ay in clu de th e ferom edial direct ion . Th ey t yp ically project below t h e an te-
in ferior hypophyseal ar ter y, m argin al an d basal ten torial, as w ell rior clin oid process an d m ay be con fused w ith in t racavern ous
as dorsal an d m en ingeal bran ch es.14 an eur ysm s on lateral angiogram s.
Tw o m ajor groups of ar teries arise from th e h orizon t al seg- 3. Posterior com m un icat ing artery aneurysm s: Typ ically ar ise
m en t . An teriorly, th e cap su lar ar teries of McCon n ell su pp ly th e from th e posterior w all of th e ICA an d project laterally. As
periph er y of th e an terior p it u itar y an d adjacen t du ra. Th ese are th ey grow, th ey m ay com press th e occulom otor n er ve.
m icroscop ic vessels th at are u su ally too sm all to appear on angi- 4. Anterior choroidal artery aneurysm s: Gen erally poin t p osteri-
ography; h ow ever, th ey m ay represen t a possible site for cavern - orly or posterolaterally far from th e occu lom otor n er ve.
ous (C4) aneurysm form ation. The clinoid (C5) section is the short- 5. Carot id term inus aneurysm s: Usu ally p roject lon git u d in ally
est segm en t of t h e ICA. Th is segm en t gives n o n am ed bran ch es. from t h e vessel w all in th e d irect ion of blood flow . As n oted
Th e p roxim al an d dist al du ral rings defin ing th is segm en t are by Rh oton , perforators arising from th e dist al ICA m ay be as-
difficu lt to iden t ify on angiograp hy an d on oth er n on invasive sociated w ith th e an eu r ysm an d sh ou ld be carefu lly iden t ified
im aging m odalit ies. Th e oph th alm ic (C6) segm en t cou rses pos- an d spared du ring in ter ven t ion .
teriorly an d gives rise to th e oph th alm ic an d superior hypophy-
seal ar ter ies. Th e op h t h alm ic ar ter y is u su ally t h e first bran ch
to origin ate from th e ICA after it exits th e cavern ous sin us.12 It
arises from th e an terom edial or su perior surface of th e ICA im -
m ediately after it pen et rates th e dural ring. Th is m akes th e prox-
■ Natural History
im al stem of th e op h th alm ic ar ter y a usefu l angiograph ic lan d- Man agem en t of ICA an eu r ysm s requ ires a th orough u n derst an d-
m ark for th e posit ion of th e dura. Th e oph th alm ic arter y courses in g of t h e com p lex an d often con flict ing dat a obt ain ed from
an terolaterally an d pierces th e dura again to en ter th e opt ic canal natural histor y studies. Any decision involving conser vative m an-
w h ere it occupies a posit ion in ferior or in ferolateral to th e optic agem en t or in ter ven t ion sh ou ld balan ce th e risk of th e plan n ed
n er ve. Th e superior hypophyseal ar ter y arises m edially or in fer- procedu re again st risks carried by th e n at u ral cou rse of th e dis-
om edially bet w een th e oph th alm ic an d PCoA. Th e su praclin oid ease. In 1998, th e In tern at ion al St udy of Un ru pt ured In t racran ial
por t ion of th e ICA in it ially cou rses p osteriorly an d th en cu r ves An eur ysm s-I (ISUIA-I) ret rospect ively repor ted on th e risk of
upw ard tow ard th e an terior p erforated su bst an ce. Th e com m u - rupt ure of 1,937 un r upt ured in t racran ial an eur ysm s.16 Th e cu -
n icat ing (C7) segm en t st ar ts at th e level of th is cur ve, w h ere the m u lat ive ru pt u re rate of an eu r ysm s less th an 10 m m in diam eter
PCoA arises.15 Angiograp h ically, th e com m u n icat ing segm en t is w as fou n d to be less th an 0.05% p er year in pat ien ts w h o h ad n o
iden t ified as th e p ort ion of th e ICA exten ding from th e origin of previou s an eu r ysm al r u pt u re. High er r u pt u re risk w as rep or ted
th e PCoA to th e carot id term in u s.14 Th e C7 segm en t also gives in p at ien ts w ith larger an eur ysm s. An eur ysm s of th e posterior
rise to th e an terior ch oroidal ar ter y as w ell as oth er sm all perfo- circulat ion w ere fou n d to carr y sign ifican tly h igh er risks of r up -
rators. Th e carot id term in u s r un s u pw ard an d laterally. On th e t u re com p ared w ith an terior circu lat ion an eu r ysm s. Th e ISUIA-II
lateral view, the carotid bifurcation cann ot be precisely identified t rial, p u blish ed in 2003, involved a p rosp ect ive an alysis of 1,692
because bran ch es from th e MCA often obscu re it . In th e an tero- pat ien ts w ith 2,686 u n ru pt u red in t racran ial an eu r ysm s m an -
posterior view, th e bifu rcat ion is sit uated above th e distal en d of aged con ser vat ively.3 Th e 5-year cum ulat ive risk of r upt ure for
th e pet rous (C2) segm en t . an ter ior circu lat ion an eu r ysm s less t h an 7 m m in diam eter in
p at ien t s w ith ou t h istor y of su barach n oid h em or rh age w as re-
p or ted to be 0%. Th is fin d in g rem ain s a p oin t of sign ifican t con -
t roversy. An eur ysm s of th e ICA w ith sizes ranging bet w een 7 to
12 m m , 13 to 24 m m , an d 25 m m or m ore w ere foun d to h ave
■ Classification of Internal Carotid rupt u re rates of 2.6%, 14.5%, an d 40%, resp ect ively.3 Th e Sm all
Artery Aneurysms Un rupt u red In t racran ial An eur ysm Verificat ion (SUAVe) st udy,
An eur ysm s of th e ICA can be classified according to several ch ar- pu blish ed in 2010, rep or ted on th e an n u al ru pt u re rate in 448
acterist ics: t ype (t rue an eur ysm s or pseu doan eur ysm s); sh ape unruptured intracranial aneur ysm s less than 5 m m in diam eter.17
(fu siform , saccu lar, or com plex); size (sm all, < 10 m m ; large, 10 Th e average an n u al risk of ru pt u re of single u n ru pt u red an eu -
to 24 m m ; or gian t ≥ 25 m m ); an d locat ion (C1 to C7). Th e m ost r ysm s less th an 5 m m in diam eter w as est im ated to be 0.34%.
com m on ly u sed classificat ion , h ow ever, is t h e on e described by Alth ough th ese dat a suggest low ru pt u re risk for sm all asym p -
Rhoton,15 w ho system ically divided subarachnoid ICA aneurysm s tom at ic u n rupt u red an eur ysm s, th e issu e rem ain s con t roversial.
in to t h e follow ing five categories based on th e origin s of m ajor Rupt u red an eu r ysm s less th an 7 m m in diam eter are frequ en tly
bran ch es: en cou n tered in clin ical p ract ice.9,18,19 Moreover, th e m edian size
of r u pt ured an eu r ysm s w as foun d to be 6.28 m m in on e st u dy,
1. Ophthalm ic artery aneurysm s: Can be fu r t h er su bclassified w it h 71.8% of t h e cases h aving an eu r ysm s less t h an 7 m m in
based on t h eir site of origin , t h eir or ien t at ion in sp ace, an d diam eter.20
th eir relat ion sh ip to su rrou n ding st ru ct u res. Th ree differen t Recen tly, th e Un rupt u red Cerebral An eur ysm St udy (UCAS) of
t yp es of op h th alm ic arter y an eu r ysm s are id en t ified: an eu- Jap an p rosp ect ively follow ed u p 697 u n r u pt u red in t racran ial
r ysm s arising from th e clin oid segm en t of th e ICA, an eur ysm s an eur ysm s w ith a m ean size of 5.7 ± 3.6 m m .21 Th e an n ual r up -
ar ising from t h e carot id cave, an d an eu r ysm s ar ising from t ure rate of in t racran ial an eur ysm s w as est im ated to be 0.95%.
th e upper surface of th e ICA an d project ing superiorly tow ard An eur ysm al size (> 7 m m ), locat ion (an terior and posterior com -
th e opt ic n er ve. m u n icat in g ar ter ies), an d m or p h ology (p resen ce of a daugh ter

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518 V Cerebral and Spinal Aneurysms

sac) w ere fou n d to be in dep en den t predictors of ru pt u re. An eu - an terior ch oroidal ar ter y, arisin g from C7, rarely p resen t w it h
r ysm s of th e ICA represen ted 34% of th e total coh ort . ICA/PCoA cran ial n er ve d eficit becau se t h ey com m on ly p roject above t h e
jun ct ion an eur ysm s w ere foun d to carr y a h igh risk of ru pt ure. ten torium . An eur ysm s of th e carot id term in us usually presen t
Th e an n u al r u pt u re rates at t h is locat ion var ied accord in g to w ith subarach n oid h em orrh age, or w ith in t raparen chym al h em -
an eur ysm al size an d w ere rep or ted to be 0.41%, 1.0%, 3.19%, an d orrh age in to th e basal ganglia. Th ey m ay en large en ough to com -
6.12%per an eur ysm per year in an eur ysm s 3 to 4 m m , 5 to 6 m m , press th e opt ic fibers leading to visual deficits.
7 to 9 m m , an d 10 to 24 m m in diam eter, resp ect ively. Ru pt u re
rates of gian t an eu r ysm s (≥ 25 m m ) of th e ICA/PCoA jun ct ion
w ere ext rem ely h igh . An eu r ysm s of t h e p araclin oid segm en t ,
ICA bifu rcat ion , an d ICA/an terior ch oroidal ar ter y jun ct ion w ere ■ Endovascular Therapy
fou n d to car r y low er r isks of r u pt u re w it h a r u pt u re rate of 0
to 0.14% for an eur ysm s less th an 7 m m in diam eter, an d 1.19%, Endovascular strategies, options, and tools to treat ICA aneurysm s
1.07%, and 10.1% per an eu r ysm per year for an eur ysm s 7 to sh ou ld be w eigh ed carefu lly again st op en su rgical st rategies,
9 m m , 10 to 24 m m , an d ≥ 25 m m in diam eter, resp ect ively. opt ion s, an d tools as w ell as n at ural h istor y. Occasion ally, it is
An in terest in r isk factors of an eu r ysm al r u pt u re h as grow n advan t ageous to com bin e op en an d en d ovascular tech n iques.5,30
in t h e literat u re.3,16,21–23 On e su ch factor t h at m ay be obser ved En d ovascu lar st rategies can be d ivid ed in to t h ree categor ies:
is grow th over t im e. In a recen t an alysis of 64 u n r u pt u red an eu - (1) paren t ar ter y recon st ruct ive tech n iques w ith coil deposit ion
r ysm s ≤ 7 m m in diam eter reported in th e literat ure, Ch m ayssan i in t h e an eu r ysm , (2) recon st r u ct ion w it h flow d iversion , an d
et al19 fou n d th e absolu te diam eter grow th to be sign ifican tly (3) decon st ruct ive tech n iques involving paren t ar ter y sacrifice
larger in an eu r ysm s t h at even t u ally r u pt u red , com p ared w it h w ith or w ith out bypass.31,32 A case-by-case approach is advised
t h ose t h at rem ain ed u n r u pt u red over t im e. Ot h er r isk factors to avoid errors in decision m aking. Factors to con sider in clude
discu ssed in th e literat u re in clu de older age, fem ale sex, sm ok- pat ient age, clin ical presentation, cardiovascular risk factors, ren al
ing, an d hyper ten sion .24,25 Fam ilial an eu r ysm s h ave also been st at u s, an eu r ysm size, m or p h ology in clu d in g relat ion sh ip of
sh ow n to carr y h igh er risks of r u pt u re com pared w ith sporad ic t h e an eu r ysm to th e p aren t ar teries, an d m ass effect issu es.33,34
lesion s.26 In th eir st u dy of 113 p at ien t s w ith fam ilial an eu r ysm s, Ot h er im p or t an t factors in clu d e t h e p at ien t ’s toleran ce of an t i-
Broderick et al26 rep or ted an an n u al ru pt u re rate of 1.2%, w h ich coagu lan t or an t ip latelet adm in ist rat ion an d in dividu al prefer-
is 17 t im es h igh er th an th e rate of r u pt u re of sporadic an eur ysm s en ces. Th e follow ing sect ion discu sses differen t en dovascu lar
repor ted in ISUIA-II. tech n iques an d st rategies used to address saccular an eur ysm s of
the ICA, their indications, th eir poten tial com plicat ions, and th eir
clin ical ou tcom es.

■ Clinical Presentation
Th e clin ical p resen t at ion of pat ien t s w ith ICA an eu r ysm s is ■ Parent Artery Reconstructive
largely depen den t on th e an eu r ysm locat ion , size, an d direct ion .
Pat ien t s w ith pet rou s (C2) segm en t an eu r ysm s m ay presen t
Techniques w ith Coil Deposition
w ith th rom boem bolic st roke, ver t igo or dizzin ess, h earing loss, in the Aneurysm
pu lsat ile t in n it u s, or eigh th cran ial n er ve deficit .4 Horn er’s syn -
Coiling Technique
drom e h as also been rep or ted in associat ion w ith such lesion s.27
Pat ien t s w ith an eu r ysm s of th e caver n ou s (C4) segm en t of th e An eur ysm s of th e ICA approach ed using th is tech n iqu e are t ypi-
ICA are u su ally asym ptom at ic. Th e m ost com m on m ass effect cally sm all to in term ediate in size, saccu lar in sh ape, an d h ave a
sym ptom s of these aneur ysm s are headache an d diplopia.28 Other favorable dom e-to-n eck rat io.35 Pet rou s, cavern ous, an d paracli-
com m on m an ifest at ion s of cavern ou s (C4) an eu r ysm s in clu de n oid an eu r ysm s are often w ide-n ecked . As w ith any coiling pro-
th e form at ion of a carot id-cavern ou s fist u la an d ep ist axis, w h ich cedu re, th ough tfu l select ion of access cath eters is crucial. Recen t
can be fat al.29 An eur ysm s w ith carot id-cavern ous fist ulas m ay advan ces in guide cath eter tech nology en able greater stabilit y of
cau se ch em osis, pu lsat ile exop h th alm os, or an orbital bruit . th e access system in th e ext racran ial carot id, w ith poten t ial for
Th e clin ical p resen t at ion of th ose w ith p araclin oid (C5 an d intracranial advancem ent of certain guide catheters w hen deem ed
C6) an eu r ysm s is largely dep en den t on an eu r ysm al locat ion rel- advan t ageous.36 Th ree-dim en sion al app reciat ion of th e an eu r ys-
at ive to the dural rings. Aneurysm s that arise proxim al to the dis- m al an d paren t arter y an atom y is param oun t for procedural
tal du ral ring are usu ally con tain ed in a lim ited ext radural space plan n ing. Th e operator can u se each p lan e to keep an eye on d if-
an d do n ot cause subarach n oid h em orrh age. An eur ysm s th at feren t aspects of th e an atom y during coiling. Careful at ten t ion
arise distal to th e distal du ral ring are in close proxim it y w ith th e sh ou ld be given to sizing an d d ist r ibu t ion of t h e coils in t h e
opt ic n er ve and th u s can cause visual sym ptom s. Su barach n oid an eur ysm . Ach ieving a h om ogen eou s dist ribut ion of coils w ith in
h em orrh age can be seen w h en th ese an eur ysm s are in t radural. t h e an eu r ysm al sac m ay d ecrease t h e recan alizat ion rate d u e to
Pat ien t s w ith an eu r ysm s of th e com m u n icat ing (C7) segm en t of com pact ion .37 Th erefore, th e coil u n iform it y in dex, along w ith
th e ICA u su ally p resen t w ith su barach n oid h em orrh age or th ird th e packing den sit y an d th e angiograph ic occlu sion , can be an
n er ve com p ression sym ptom s. Typ ically, blood from t h ese an - im por t an t param eter in predict ing t reat m en t stabilit y. Cau t ion
eu r ysm s is seen in th e lateral su p rasellar an d am bien t cister n s. sh ou ld be exercised w h en p lacing sm all coils tow ard th e en d of
Com p ression of th e th ird cran ial n er ve u su ally lead s to p ain fu l, th e procedu re. Negat ive road m aps can be u t ilized to en su re th at
n on –p u p il-sp ar ing ocu lom otor n er ve p alsy. An eu r ysm s of th e th ese coils are w ell p laced an d at m in im al risk of h ern iat ion an d

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44 Endovascular Therapies for Aneurysm s of the Internal Carotid Artery 519

dist al em bolizat ion . Gel-coated coils m ay resu lt in greater occlu - w ere pat ien t age greater th an 50 years an d in it ial presen tat ion
sion rates an d decreased recan alizat ion rates.38,39 w ith m RS score > 2.43 The 3-year follow -up results from the BRAT
w ere recen tly published.44 Based on th e m RS scores at 3 years,
th e ou tcom es of p at ien t s assign ed to coil em bolizat ion sh ow ed
Balloon-Assisted Coiling Technique a favorable 5.8% absolute differen ce com pared w ith outcom es of
Th is tech n iqu e can be qu ite effect ive for w ide-n ecked an eu r ysm s th ose assign ed to clip occlu sion . Th is differen ce did n ot reach sig-
but it requires frequen t in flat ion an d deflat ion of a balloon . It is n ifican ce (p = 0.25). Pat ien t s in t h e clip grou p h ad a h igh er rate
n ot w ell suited for u lt ra-w ide-n ecked an eur ysm s. Th e exact cu t- of an eu r ysm obliterat ion an d a low er rate of recu rren ce an d re-
off for th e dom e-to-n eck rat io th at w ould m ake th is tech n ique t reat m en t . Th e Cerebral An eu r ysm Reru pt u re After Treat m en t
less effect ive rem ain s con t roversial.40 We t ypically favor placing (CARAT) st udy dem on st rated th at r upt ured an eur ysm s, t reated
th e balloon across th e n eck of th e an eu r ysm follow ed by an eu - eith er en dovascu larly or surgically, carr y low risk of reru pt u re.45
r ysm m icrocath eterizat ion . In som e cases, th e balloon can be left Ret reat m en t rates, h ow ever, w ere sign ifican tly h igh er in en do-
in flated u n t il several coils are p laced. Carefu l at ten t ion sh ou ld be vascu larly t reated an eur ysm s com pared w ith th ose t reated sur-
paid to tem p orar y occlu sion t im es. A sten t can be p laced at th e gically in th e first year of follow -up (p < 0.0001). An eu r ysm s of
en d if n ecessar y. th e ICA represen ted 31% of th e st udied an eu r ysm s.
Th e An alysis of Treat m en t by En dovascu lar ap p roach of Non -
rupt ured An eur ysm s (ATENA) st udy prospect ively invest igated
Stent-Assisted Coiling Technique the sh ort-term outcom es of endovascular therapy in 649 patien ts
presen t ing w ith u n r u pt u red in t racran ial an eu r ysm s. An eu r ysm s
Th is tech n iqu e can be u sed to t reat side-w all an eu r ysm s of th e w ere t reated using coiling alon e in 54.5% of th e cases, balloon -
ICA an d an eur ysm s of th e carot id term in u s. A sten t can be de- assisted coiling in 37.3%, an d sten t ing in 7.8% of cases.46 Over a
ployed before or after a cath eter is p laced in th e an eu r ysm . We 1-m on th follow -up period, th e m orbidit y an d m or talit y rates
t ypically prefer to “jail” th e cath eter in th e an eu r ysm follow ed by w ere repor ted to be 1.7% an d 1.4%, respect ively. Th e rate of fail-
sten t d ep loym en t . Th e m icrocat h eter u sed to dep loy th e sten t u re of en dovascu lar th erapy, defin ed as th e in terrupt ion of t reat-
is t ypically posit ion ed before th e an eur ysm is cath eterized. It m en t d u e to an atom ic or tech n ical reason s, w as rep or ted as 2.2%
can be advan t ageou s to dep loy t w o to th ree coil loop s before in an eur ysm s of th e ICA. Th rom boem bolic even t s w ere th e lead-
sten t dep loym en t . Th is m ay st abilize th e m icrocath eter in th e ing cau se of m orbidit y an d m or talit y. Th ese com m on ly occurred
an eu r ysm before an d d u r ing sten t d ep loym en t . If t h e sten t is in association w ith large aneurysm s and aneurysm s treated using
d eployed first , a m icrocath eter can th en be in ser ted th rough th e sten t-assisted coiling. In th eir review of 1,137 con secu t ive pa-
side-w all st r u t s in to t h e an eu r ysm al sac. Coil d ep loym en t is tients presenting w ith either ruptured or un ruptured aneur ysm s,
t yp ically st raigh tfor w ard th ereafter. Piot in et al47 also n oted sign ifican t ly h igh er m or t alit y rates in
associat ion w it h sten t -assisted coiling com p ared w ith coiling
alon e. How ever, th e st udy sh ow ed sign ifican tly low er recurren ce
Outcomes of Assisted and Nonassisted Coiling rates in pat ien ts t reated w ith sten t-assisted coiling (14.9% vs
Th e In tern at ion al Su barach n oid An eu r ysm Trial (ISAT) w as th e 33.5% in pat ien ts t reated w ith coiling alon e; p < 0.0001).
first ran dom ized st udy to describe favorable ou tcom es for en do- Th e HydroCoil En dovascu lar An eu r ysm Occlu sion an d Pack-
vascu lar coiling of r upt ured in t racran ial an eur ysm s com pared ing St udy (HELPS) exam in ed th e safet y an d efficacy of hydrogel-
w ith surgical clipping.41 Th e st u dy repor ted on 2,143 p at ien t s coated coils com p ared w ith bare p lat in u m coils.48 Coiling w as
w h o w ere deem ed appropriate to receive eith er of th e t w o t reat- su ccessfu l in 98.6% of th e 499 rep or ted p at ien ts w h o p resen ted
m en t m odalit ies. An eu r ysm s of t h e ICA rep resen ted 32.5% of w ith eith er r upt ured or un ru pt u red an eur ysm s. Assisted tech -
t h e total ru pt ured an eu r ysm s rep or ted in th e st udy. At 1-year n iques w ere allow ed for both t reat m en t arm s. Mor t alit y rates
follow -up, th e m orbidit y an d m or t alit y rates (m odified Ran kin over a 3-m on th follow -u p p er iod w ere n ot sign ifican tly d iffer-
scale [m RS] score of 3 to 6) w ere fou n d to be sign ifican tly low er en t bet w een t h e t w o t reat m en t arm s (3.6% for pat ien t s t reated
in pat ien t s t reated w ith en dovascular coiling (23.7% vs 30.6% w it h Hyd roCoils (MicroVen t ion , Aliso Viejo, CA) vs 2.0%for t h ose
w ith surgical clipping; p = 0.0019). Long-term follow -u p , h ow - t reated w ith bare plat in u m ). Adverse even ts, p ar t icularly th rom -
ever, h as sh ow n an in creased risk of recurren ce in an eur ysm s boem bolic com plicat ion s, w ere m ore com m on w ith balloon - an d
t reated en dovascu larly com pared w ith th ose ap p roach ed su rgi- sten t-assisted tech n iqu es.
cally. Th e 5-year risk of death w as sign ifican tly low er in th e en -
dovascu lar t reat m en t arm .42 It sh ould be n oted th at 80%of an eu-
r ysm s screen ed for th is st udy w ere n ot in cluded, th us lim it ing
gen eralizabilit y.
More recen tly, th e Barrow Ru pt u red An eu r ysm Trial (BRAT)
■ Reconstruction w ith Flow Diversion
repor ted on 500 pat ien t s w h o p resen ted w ith ru pt u red in t racra- Flow diver ters are self-expan ding, cylin drical m esh sten t s u sed
n ial an eur ysm s an d w ere eligible for both en dovascu lar an d su r- to recon st ru ct th e paren t ar ter y an d redirect blood flow aw ay
gical th erapies. Abou t 75% of rupt ured an eur ysm s st udied in th e from t h e an eu r ysm . Th ese d evices, n am ely th e Pipelin e Em boli-
BRAT w ere located in th e an terior circu lat ion . Th e 1-year follow - zat ion Device (PED; Ch est n u t Medical Tech n ologies, Men lo Park,
up period favored en dovascular coiling over su rgical clipp ing in CA) an d th e SILK Flow Diver ter (SFD; Balt Ext rusion , Mon t m o-
term s of clin ical ou tcom es (m RS score > 2 w as rep or ted in 23.2% ren cy, Fran ce), seem to offer an oth er valuable tool in th e en do-
of en dovascularly t reated pat ien ts vs 33.7% of th ose w h o u n der- vascular treatm ent of otherw ise difficult-to-treat ICA aneur ysm s.
w en t su rgical clip p ing; p = 0.02).43 Pred ictors of p oor ou tcom e Th e PED received U.S. Food an d Dr ug Adm in ist rat ion (FDA) ap -

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520 V Cerebral and Spinal Aneurysms

p roval in 2011 for t h e t reat m en t of large or gian t w id e-n ecked th e risk of isch em ic com p licat ion s from in adequ ate collateral ce-
an eur ysm s of th e pet rous (C2), cavern ous (C4), an d paraclin oid rebral blood flow.32 Revascularizat ion using a surgical bypass is
segm en ts of th e ICA.49 Th e SFD, h ow ever, h as been approved on ly som et im es n ecessar y to en h an ce toleran ce of th is p roced u re.
in Eu rope an d a few cou n t ries elsew h ere. Flow diverters are de- To d eter m in e w h ich grou p of p at ien t s n eed s a su rgical byp ass,
ployed along th e longit u din al axis of th e p aren t ar ter y an d across a balloon test occlu sion (BTO) is p er for m ed p r ior to sacr ifice
th e an eu r ysm al n eck. Th is leads to th e disr u pt ion of an eu r ysm al of t h e ICA (Fig. 44.1).66 A balloon is in flated for 30 m in u tes in
in flow an d outflow jets an d cau ses st asis an d th rom bosis in side th e region w h ere t h e en dovascu lar ICA occlu sion is plan n ed .
th e an eu r ysm al sac. Fur th er, flow diver ters are th ough t to in du ce Meanw h ile, a digit al subt ract ion angiograp hy of th e con t ralat-
n eoin t im al proliferat ion in th e ar terial w all overlaying th e sten t eral carot id an d ver tebral circu lat ion s is perform ed to st u dy th e
st r u t s, p oten t ially leading to com p lete in tegrat ion of th e device collateral blood flow. Addit ion ally, w h ile th e p at ien t is aw ake, a
w ith in th e in t im a.50 Recon st ru ct ion w ith flow diversion can be serial assessm en t of th e pat ien t’s n eu rologic st at u s is don e to de-
tech n ically ch allenging in term s of sten t deploym en t an d avoid- tect any clin ical deficit s cau sed by th e BTO.32 To detect any hypo-
ance of perforator occlusion; how ever, increased experience w ith ten sion -in duced n eurologic deficits, a hypoten sive ch allenge test
th ose devices h as led to tech n ical su ccess rates of 95 to 100% ch aracter ized by low er in g t h e p at ien t ’s blood p ressu re to t w o -
w ith th e PED an d 90 to 96% w ith th e SFD.51–55 th irds of baselin e du ring BTO is also perform ed. Con t in u ou s elec-
Several st u d ies rep or t ing on th e efficacy an d safet y of flow t roen cep h alogram (EEG) m on itoring is u n der taken th rough ou t
diver ters in th e t reat m en t of in t racran ial an eu r ysm s h ave been th e procedu re to ch eck for any ch anges during BTO. Fin ally, a
pu blish ed.52–57 Im m ediate p ost p rocedu ral com p lete obliterat ion single p h oton em ission com pu ted tom ography (SPECT) scan is
rates associated w ith th e PED range bet w een 8% an d 21%; h ow - com p leted to evalu ate cerebral p erfu sion . Su rgical bypass sh ou ld
ever, overall com plete obliterat ion rates on follow -up angiogra- be con sidered in pat ien t s w h o dem on st rate in adequate collat-
phy can in crease u p to > 50%at 3 m on th s, 85 to 95%at 6 m on th s, eral cerebral blood flow. Th e t yp e of su rgical byp ass requ ired for
an d > 95% at 12 m on th s.51,53,55–57 Th e delay in th rom bu s form a- each case depen ds on several factors. Th ese in clude th e am oun t
t ion n oted w ith th ese d evices can be du e to aggressive an d pro- of blood flow n eeded, th e availabilit y of a don or vessel, an d th e
longed dual an t iplatelet th erapy. Morbidit y an d m or talit y rates size of th e recipien t vessel, as w ell as th e region of th e byp ass.
associated w ith th e PED range bet w een 0% an d 16.6%.51,52 Com - Com plete en dovascu lar ICA occlu sion sh ou ld be perform ed im -
m on causes of m ortalit y an d m orbidit y are in -sten t th rom bosis m ediately after a h igh -flow byp ass graft procedu re to avoid graft
or sten osis, perforator occlusion , an d in t racran ial h em orrhage.51 t h rom bosis cau sed by com p eten t blood flow from th e p aren t
It ap pears th at th e SFD m ay be associated w ith low er com p lete ar ter y. In cases w h ere a low -flow bypass graft is used, com plete
occlusion rates an d an in creased risk of th rom bosis. Im m ediate ICA occlusion can be perform ed 2 to 3 days after th e bypass pro-
post p rocedu ral com p lete occlu sion rates associated w ith th e SFD cedu re. Table 44.1 su m m arizes th e in d icat ion s an d th e p rotocol
range bet w een 10%an d 11.8%; h ow ever, th ese rates can in crease for revascu larizat ion at ou r in st it u t ion .
u p to 49 to 70% at 12-m on t h follow -u p .54,55,58 Morbid it y an d Th e risk of isch em ic com p licat ion s associated w ith com plete
m or t alit y rates associated w it h t h e SFD ran ge bet w een 3% an d ICA occlu sion ranges bet w een 2% an d 22% d esp ite t h e u se of
15%.55,58,59 BTO.4 In th eir literat u re review on th e outcom es of en dovascular
Qu est ion s regarding long-term du rabilit y an d safet y of flow paren t vessel occlu sion w ith or w ith ou t byp ass in th e t reat m en t
diver ters, as w ell as th eir feasibilit y for u se in ru pt u red in t racra- of gian t in t racran ial an eu r ysm s, Parkin son et al66 repor ted m or-
n ial an eu r ysm s, rem ain to be an sw ered . Addit ion ally, th e n eeded talit y an d m orbidit y rates of 7%an d 17%, respect ively (n ot exclu -
d u rat ion of d u al an t ip latelet t h erapy rem ain s u n kn ow n . Klisch sive to ICA an eu r ysm s). Th e overall in it ial com plete occlu sion
et al60 reported on t w o cases w h o presen ted w ith acute sten t rate w as est im ated to be 81%. Th e recurren ce rate w as foun d to
t h rom bosis w ith in 2 w eeks of d iscon t in u at ion of an t ip latelet be 1.1% at a m ean follow -up du rat ion of 14 m on th s. Recen tly,
t h erapy, 1 year after th e p roced u re. Fu r t h er m ore, con cer n s re- Gobble et al67 st u died th e efficacy an d safet y of su rgical bypass
gard ing d elayed an eu r ysm al r u pt u re cau sed by t h e for m at ion in p at ien ts w ith gian t in t racran ial an eu r ysm s. Of th e 36 p at ien t s
of a biologically act ive red th rom bus in side th e an eur ysm al sac st u died, 30 p at ien t s h ad gian t an eu r ysm s located on th e ICA. Th e
h ave been raised.61 Also, tech n ical ch allenges such as difficult 36 pat ien ts un der w en t 37 su rgical bypasses w ith 34 saph en ou s
dep loym en t of flow diver ters in th e set t ing of vasosp asm , as w ell vein an d t h ree rad ial ar ter y graft s. Overall graft p aten cy w as
as delayed device m igrat ion , h ave been recen tly repor ted in th e rep or ted in 89.2% of cases at a m ean follow -u p du rat ion of 53
literat u re.62,63 m on th s. Th e m ort alit y an d m orbidit y rates w ere 5.6% each .

Deconstructive Techniques Involving Parent


Artery Sacrifice w ith or Without Bypass ■ Site -Specific Considerations
En dovascu lar h u n terian ligat ion of th e p roxim al ICA aim s to p er-
Petrous (C2) Segment Aneurysms
m an en tly obst ru ct flow to th e paren t arter y an d th e an eur ysm ,
su bsequ en tly leading to an eu r ysm al sh rin kage an d th rom bosis. An eur ysm s of th e pet rous (C2) segm en t of th e ICA are m ost com -
Th is tech n iqu e is com m on ly u sed to address gian t an eu r ysm s of m on ly of th e fusiform t ype.68 Saccu lar an eu r ysm s of th is seg-
th e p et rou s (C2) an d cavern ou s (C4) segm en t s of th e ICA th at are m en t are relat ively rare.69 Th ese lesion s, h ow ever, can becom e
oth er w ise con sidered difficu lt to t reat u sing conven t ion al surgi- large an d p at ien t s p resen t w ith r u pt u re, d ist al th rom boem bolic
cal or en dovascu lar tech n iqu es.64,65 Alth ough 80%of pat ien t s can m an ifest at ion s, or local m an ifestat ion s (e.g., t in n it us).4 In dica-
clin ically tolerate com p lete ICA occlu sion , th is tech n iqu e carries t ion s for t reat m en t of p et rou s (C2) segm en t an eu r ysm s in clu de

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44 Endovascular Therapies for Aneurysm s of the Internal Carotid Artery 521

a b c

d e

Fig . 44.1a– e A 50-year-old wom an presented with a sudden onset of patient experienced progressive decline in her third nerve function on the
severe headache. (a) Com puted tom ography angiography (CTA) scan left side. (d) Follow-up m agnetic resonance angiography (MRA) detected a
dem onstrated a 14-m m narrow-necked aneurysm arising from the lateral 6 m m × 4 m m filling at the aneurysm al base (arrow). The patient under-
aspect of the left cavernous internal carotid artery (ICA) with intradural ex- went a balloon test occlusion (BTO), which showed m ild asym m etry of
tension. (b) An angiogram showed an additional 2- to 3-mm m ore proxi- flow. (e) Left superficial temporal artery (STA) to m iddle cerebral artery
m al aneurysm . (c) The patient underwent coiling of the larger aneurysm (MCA) bypass was perform ed followed by carotid occlusion. Her third nerve
with final angiography showing complete occlusion. Five years later, the function partially recovered at follow-up.

Table 44.1 Indications and Protocol for Revascularization

Clinical Assessment Hypotensive


(Normotensive) Challenge Test EEG SPECT Scan Procedure

Pass Pass Pass Pass Complete ICA occlusion


Pass Fail Fail Fail Complete ICA occlusion with low-flow bypass (STA-MCA)
Fail Fail Fail Fail Complete ICA occlusion with high-flow bypass (SV or RA)
Pass Fail Pass Fail Complete ICA occlusion with low-flow bypass (STA-MCA)
Abbreviations: EEG, electroencephalogram ; SPECT, single photon em ission computed tom ography; ICA, internal carotid artery; STA, superficial temporal artery; MCA,
middle cerebral artery; SV, saphenous vein; RA, radial artery.

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522 V Cerebral and Spinal Aneurysms

recurrent transient ischem ic at tacks, ischem ic stroke, cranial neu- or in delayed m ass effect sym ptom s in cases of an eur ysm al re-
ropath ies, pulsat ile t in n it u s, or rupt ure.4 Rapid grow th m ay also curren ce.32,75 In th eir rep or t on th ree p at ien ts w ith cavern ou s
be an indication for inter vention. Treatm ent options include con- (C4) segm en t an eur ysm s t reated w ith en dovascular coiling, Xu
ser vat ive m an agem en t w ith follow -u p im aging, en d ovascu lar et al75 described th e developm en t of delayed cran ial n er ve palsy,
coiling, balloon- or stent-assisted coiling, flow diverter placem ent, in associat ion w ith an eu r ysm al recurren ce, for all pat ien t s. Th e
an d p aren t ar ter y occlu sion w it h or w ith ou t h igh -flow byp ass. au th ors hyp ot h esized t h at recu r ren t flow in sid e a p reviou sly
In cases w h ere C2 an eu r ysm s h ave a w ell-d efin ed n eck, en d o - coiled an eu r ysm m ay lead to p ersisten t h em odyn am ic an d m ass
vascular occlusion of th e an eu r ysm w ith coils can be an opt ion . effect s th at could cause com p ression of n earby st r uct u res. An eu-
Balloon - or sten t-assisted tech n iques m ay be n eeded for w ider r ysm s of th e cavern ous (C4) segm en t of th e ICA presen t ing w ith
n ecked an eu r ysm s. Cu r ren t sten t s are su fficien t ly flexible to m ass effect can th erefore be t reated u sing en d ovascu lar ICA oc-
p er m it easy d eliver y in to t h e tor t u ou s p et rou s (C2) segm en t of clu sion w ith or w ith ou t su rgical byp ass. As p reviou sly discu ssed,
t h e ICA.70 Placem en t of a PED can be ap p rop r iate for gian t or a BTO is recom m en ded prior to th is procedure.32,66 Th is tech -
m ore com plex an eu r ysm s.49,52 En dovascu lar com p lete ICA occlu - n iqu e is associated w ith a m or talit y rate of 0 to 1.7% an d a m or-
sion u sing det ach able coils is an oth er valid t reat m en t opt ion of bidit y rate of 2.7 to 6.6%.28 An oth er available t reat m en t opt ion
com p lex p et rou s (C2) segm en t an eu r ysm s.4,64 All pat ien ts sh ould for th ese an eur ysm s is flow diversion w ith a PED.49,52
un dergo a BTO before ICA occlu sion to assess th eir toleran ce of
the procedure.66 Revascularization procedures are associated w ith
Ophthalmic (C6) Segment Aneurysms
good clin ical ou tcom es at long-term follow -u p .66,71
An eur ysm s of th e oph th alm ic (C6) segm en t of th e ICA are com -
m on ly en coun tered in clin ical pract ice. Th ey accoun t for arou n d
Cavernous (C4) Segment Aneurysms 11% of all in t racran ial an eu r ysm s.76 Com m on ly, oph th alm ic (C6)
An eur ysm s of th e cavern ous (C4) segm en t of th e ICA are kn ow n segm en t an eu r ysm s arise from th e ICA p or t ion adjacen t to th e
to h ave a ben ign n at ural course.3 Th ese lesion s, esp ecially sm all origin of on e of th e t w o m ain ar terial bran ch es: th e oph th alm ic
on es, can be obser ved con ser vatively w ith follow -up im aging. ar ter y or t h e su p er ior hyp op hyseal ar ter y. An eu r ysm s ar ising
Rarely, cavern ou s (C4) segm en t an eu r ysm s grow in to large sizes d ist al to t h e or igin of t h e op h t h alm ic ar ter y u su ally p roject su -
an d com press n earby st ruct ures (cavern ous sin us an d cran ial p er iorly or su p erom ed ially tow ard t h e opt ic n er ve.77 On t h e
n er ves), or ru pt ure spon tan eou sly leading to carot id-cavern ous other hand, aneurysm s related to the superior hypophyseal artery
fist ula form at ion . In dicat ion s for t reat m en t of th ese lesion s in - u sually p roject m edially tow ard th e opt ic ch iasm . In dicat ion s for
clu de acu te ru pt u re (carot id-cavern ou s fist u la), p rogressive op h - t reat m en t in both locat ion s in clu de an eu r ysm al r u pt ure (su b -
th alm op legia, severe ret ro-orbit al p ain , erosion of th e sph en oid arach n oid h em orrh age), focal n eurologic deficit (visual dist ur-
sin u s (risk of life-th reaten ing ep istaxis), an d p rogressive an eu - ban ces), large size, irregular m orp h ology, an d/or rapid grow th .6
r ysm al en largem en t .28,32 Treat m en t of large or rapidly grow ing An eu r ysm s of t h e op h t h alm ic (C6) segm en t of th e ICA can be
asym ptom at ic cavern ous (C4) segm en t an eur ysm s m ay also be ap p roach ed u sing su rgical, en dovascu lar, or com bin ed tech -
considered. How ever, clearly defined aneurysm al size and grow th n iques.78 Th e m ost feared com plicat ion of both en dovascular an d
rate in dicat ing t reat m en t are yet to be determ in ed. Cavern ou s su rgical th erap ies is visu al d ist u rban ces, w h ich can be cau sed
(C4) segm en t an eur ysm s can be t reated using coiling tech n iques by direct com pression or injur y to th e opt ic n er ve, or by distal
w ith or w ith ou t sten t assistan ce depen ding on th eir m orph ology oph th alm ic ar ter y th rom boem bolic even ts.77
an d n eck size.28,65 Com plete occlusion of any associated carot id- Appreciat ing th e an atom ic relat ion sh ip bet w een th e targeted
cavern ou s fist u la is cru cial w h en dealing w ith su ch lesion s. In an eur ysm an d th e origin of th e oph th alm ic or superior hypophy-
th eir review of 113 pat ien ts w ith cavern ou s (C4) segm en t an eu - seal ar ter y is by far th e m ost im p or tan t step p rior to dep loym en t
r ysm s, Ch oulakian et al72 reported favorable results for en dovas- of d et ach able coils. Any su sp ected com p rom ise of im p or t an t
cular coiling w ith or w ithout stent assistance. Com plete occlusion ar terial bran ch es during th e procedure m ay w arran t th e con sid-
w as rep or ted in 75% of cases. Th e recu rren ce rate w as fou n d to erat ion of altern at ive en dovascu lar or m icrosu rgical app roach es.
be aroun d 12% at a m ean follow -up of 6.2 m on th s. Clin ical out- Endovascular coiling of narrow -necked aneurysm s can be straight-
com es of sym ptom at ic cavern ou s an eu r ysm s w ere n ot discu ssed for w ard in cases w h ere n o ar terial bran ch es em an ate from th e
in th is st udy; h ow ever, several oth er st u dies h ave reported im - an eur ysm . On th e oth er h an d, balloon - or sten t-assisted coiling
p rovem en t of sym ptom s follow ing en d ovascu lar t h erapy.7,73,74 can be u sed for w id e-n ecked op h t h alm ic (C6) segm en t an eu -
In on e st u dy, 64 of 67 p at ien t s w h o presen ted w ith p ain m an ifes- r ysm s. Carefu l stabilizat ion of th e balloon -cath eter across th e
tat ion s h ad resolut ion or im provem en t of sym ptom s follow ing an eur ysm al n eck requires m et icu lous tech n iqu e to preven t dis-
endovascular treatm ent, w hereas only 39 of 64 patients w ho pre- tal p rop agat ion of th e balloon . Sim ilarly, an accurate deploym en t
sen ted w ith diplop ia sh ow ed im provem en t .7 On th e oth er h an d, of th e sten t can be tech n ically d em an d ing, bu t can be safely
a system at ic literat ure review by van der Schaaf et al74 repor ted achieved in experien ced h an ds.
im provem en t of diplopia in 27 of 28 pat ien t s w h o originally p re- In an at tem pt to com pare outcom es of en dovascular versus
sen ted w ith th is sym ptom . su rgical m an agem en t of op h th alm ic (C6) segm en t an eu r ysm s,
Decon st r u ct ive tech n iqu es w ith or w ith ou t su rgical byp ass Hoh et al79 ret rosp ect ively rep or ted on 238 p at ien t s w h o p re-
for pat ien t s presen t ing w ith m ass effect m ay h ave bet ter decom - sen ted w ith p araclin oid an eu r ysm s an d w ere t reated u sing
pressive resu lts com p ared w ith en dovascu lar coiling.32 In fact , en d ovascu lar coilin g or su rgical clip p in g. Of t h e 180 su rgically
den sely p acking an eu r ysm s w ith det ach able coils m ay resu lt in t reated p atien t s, a com p lete occlu sion rate of arou n d 94% w as
acute w orsening of clinical sym ptom s directly after the procedure, ach ieved. On th e oth er h an d, a com plete occlusion rate of 44%

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44 Endovascular Therapies for Aneurysm s of the Internal Carotid Artery 523

w as rep or ted in t h e 57 en d ovascu larly t reated p at ien t s. Th e be con sidered an in dicat ion for m icrosu rger y, par t icularly if th e
m or t alit y an d m orbid it y rates w ere rep or ted to be 2% an d 3% PCoA is fetal. In su ch cases, com plete occlusion of th e an eur ysm
for en dovascularly t reated p at ien ts, respect ively, versus 0% an d w it h p reser vat ion of t h e PCoA sh ou ld be th e p r im ar y aim of
6% for surgically t reated pat ien ts. Sim ilar result s w ere repor ted t h e in ter ven t ion .85 Balloon -assisted coiling is an alter n at ive en -
by Boet et al,80 w h o also n oted h igh er rates of recurren ce associ- d ovascu lar tech n ique com m on ly used in t reat ing ICA/PCoA an -
ated w ith en dovascu lar th erapy com p ared w ith su rger y. More eu r ysm s. In cases w h ere th e PCoA arises from th e n eck of th e
recen t st u dies, h ow ever, report h igh er com p lete occlu sion rates an eur ysm , a balloon can be used to protect th e origin of th e PCoA
for en dovascular t reat m en t of oph th alm ic (C6) segm en t an eu - du ring coil packing. How ever, com plete preser vat ion of th e PCoA
r ysm s, especially w ith th e adven t of balloon - an d sten t-assisted can n ot alw ays be ach ieved , an d th e overall tolerabilit y for su ch
coiling tech n iqu es.81,82 In t h eir review of 147 p at ien t s presen t ing tech n iques rem ains con t roversial.86 Con t in u ou s elect rop hysio-
w ith un r upt ured oph thalm ic ar ter y an eu r ysm s, Yadla et al81 re- logical m on itoring can be con sidered du ring balloon - assisted
por ted a m ore th an 95% occlu sion rate in 81.6% of cases t reated coiling an d in term it ten t balloon deflat ion s are advised in cases
en dovascu larly. Th e overall recu rren ce rate w as 17.8% at a m ean w h ere isch em ia is suspected. Sten t-assisted coiling is an oth er
follow -up period of 28.3 m on th s. Major com plicat ion s occu rred com m on ly u sed tech n iqu e for t reat in g com m u n icat in g (C7)
in 1.4% of th e cases, an d w ere m ain ly associated w ith gian t oph - segm en t an eur ysm s. A Y-con figu rat ion sten t ing of th e ICA an d
thalm ic arter y aneur ysm s. Additionally, Chalouhi et al82 reported PCoA h as been repor ted in th e literat ure.87 Th is tech n iqu e m ay
on 87 p at ien t s w h o p resen ted w it h su p er ior hyp op hyseal ar- allow diversion of blood flow aw ay from th e an eur ysm , th us re-
ter y an eu r ysm s. A com p lete or n ear-com p lete occlu sion rate of du cing th e “w ater-h am m er” effect of flow an d th e risk of recu r-
97.6% w as ach ieved at th e t im e of th e procedu re. Aneur ysm s ren ce. Poten t ial com p licat ion s of t h e sten t-assisted tech n iqu e
w ere t reated using coiling alon e, balloon - or sten t-assisted coil- in clu d e m isp lacem en t of t h e sten t , in -sten t t h rom bosis, an d in -
in g, or flow -d iver t ing tech n iqu es. Recu r ren ce occu r red in 3.9% sten t sten osis.
of pat ien t s at a m ean follow -u p period of 10.4 m on th s. Of n ote, En dovascu lar t reat m en t of ICA/PCoA an eu r ysm s is associated
th e st u dy fou n d a low er recu rren ce rate in p at ien t s t reated w ith w it h h igh recu r ren ce rates.86 In t h eir ret rosp ect ive review of
sten t-assisted coiling com pared w ith th ose t reated w ith coiling p rosp ect ively collected dat abase, Raym on d et al88 st u d ied t h e
alon e. recu rren ce rates of 501 en dovascu larly t reated in t racran ial an -
Gian t an eur ysm s of th e oph th alm ic (C6) segm en t of th e ICA eu r ysm s. An eu r ysm s of th e ICA/PCoA ju n ct ion w ere fou n d to
can p resen t a sign ifican t ch allenge w h en app roach ed en dovas- h ave a recu rren ce rate of 37.2%, w h ich w as th e secon d m ost
cularly.66 In ter ven t ion is recom m en ded in th e m ajorit y of cases, com m on recu rren ce rate after basilar bifu rcat ion an eu r ysm s.
given th eir kn ow n h igh risk of rupt ure. Reduct ion of th e m ass An eu r ysm al size an d in it ial occlu sion rate are p oten t ial risk fac-
effect caused by th e an eu r ysm , alth ough sim ultan eously en sur- tors for an eu r ysm al recurren ce an d reh em orrh age.89,90 An oth er
ing com plete occlu sion , can be difficult to ach ieve u sing conven - m ajor con cern in th e m an agem en t of ICA/PCoA an eu r ysm s is th e
t ion al en dovascu lar coiling w ith or w ith ou t sten t assist an ce.83 n eu rologic ou tcom e of p at ien t s p resen t in g w it h occu lom otor
Th e m ain d isadvan t ages of t h ese tech n iqu es are in com p lete n er ve palsy. Th e effect of su rgical clipping versus en dovascu lar
an eu r ysm al occlu sion an d persisten t com pression sym ptom s. coiling on th e ou tcom es of com p ressive sym ptom s cau sed by
Altern at ive th erap ies for gian t op h th alm ic (C6) segm en t an eu - rupt ured an d u n rupt ured ICA/PCoA an eur ysm s rem ains a sub -
r ysm s in clude surgical clipping, as w ell as com bin ed en dovascular ject of con t roversy.86 Several st u dies suggest sign ifican t ly bet ter
an d surgical tech n iques such as suct ion decom pression .5,78 Th e n eu rologic outcom es in associat ion w ith surgical clipping com -
overall long-term occlusion rates an d visual outcom es appear to pared w ith en dovascular th erapy.91,92 Th is h as been exp lain ed by
be su perior w ith su rgical clipping com pared w ith en dovascular th e fact th at su rgical clip ping can com pletely elim in ate th e m ass
th erapy.84 En dovascu lar sacrifice of th e ICA w ith or w ith out su r- effect of th e an eu r ysm an d lead to sym ptom resolu t ion . On th e
gical bypass is an altern at ive th erapeut ic opt ion for select gian t other hand, endovascular coiling, w hich is characterized by pack-
oph th alm ic (C6) segm en t an eu r ysm s.32,66 ing th e an eu r ysm w ith coils, can result in p ersisten t com pression
of th e n er ve an d th us persisten t or w orsen ed sym ptom s. Oth er
st u dies h ave rep or ted excellen t resu lt s for en dovascu lar coiling,
Communicating (C7) Segment Aneurysms w ith part ial an d com plete resolut ion of sym ptom s occu rring in
An eur ysm s of th e com m un icat ing (C7) segm en t of th e ICA usu- 86.4% of cases.93,94
ally arise n ear th e ICA jun ct ion an d on e of its m ain ar terial Gian t an eur ysm s of th e com m u n icat ing (C7) segm en t of th e
branches: the PCoA or the anterior choroidal artery. Patients w ith ICA are relat ively rare.95 Th ese lesion s im p ose sign ifican t en do-
com m u n icat ing (C7) segm en t an eu r ysm s u su ally p resen t w ith vascular as w ell as surgical challenges to the treating physician.1,96
rupt ure (subarach n oid h em orrh age), th rom boem bolic m an ifes- High p acking den sit ies are t yp ically d ifficu lt to ach ieve u sing
tat ion s, or th ird n er ve palsy. Several en dovascu lar tech n iqu es en dovascu lar coiling tech n iqu es w ith or w ith ou t balloon or sten t
can be con sidered in th e m an agem en t of th ese lesion s. Ch oosing assist an ce.1 Th e recu rren ce rates associated w ith th is tech n iqu e
th e righ t app roach often depen ds on th e size of th e an eu r ysm , it s are ver y h igh , an d repeated coiling procedures are often n eeded
m orph ology, as w ell as its relat ion sh ip w ith th e PCoA an d an te- d u r ing t h e follow -u p cou rse.1 ICA occlu sion w it h or w it h ou t
rior ch oroidal ar teries. Mass effect issu es sh ou ld also factor in to bypass is n ot com m on ly u sed for ICA/PCoA gian t an eur ysm s.
th e decision . Prior to en dovascu lar coiling, a carefu l exam in at ion How ever, th is tech n iqu e can be u sed in pat ien ts w ith an absen t
of th e th ree-dim en sion al (3D) angiograph ic orien tat ion of th e ipsilateral PCoA.1 Su rgical m an agem en t of gian t ICA/PCoA an eu -
an eu r ysm relat ive to t h e ICA an d t h e PCoA is cr u cial (Fig. 44.2). r ysm s can h ave favorable clin ical an d angiograph ic outcom es in
A PCoA arising from th e dom e of th e ICA/PCoA an eur ysm m ay exp erien ced h an ds.95

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524 V Cerebral and Spinal Aneurysms

a b

c d e

Fig. 44.2a–e A 65-year-old woman presented to the em ergency room nents, a larger component projecting laterally, posteriorly, and inferiorly
with a hypertensive crisis and severe headache. (a,b) Cerebral angiography (c), and a sm aller component projecting m edially. (d,e) The patient under-
dem onstrated a 4.2 m m × 4.2 m m × 2.7 m m irregular-shaped aneurysm went coiling of her internal carotid artery (ICA)/PCoA aneurysm with final
arising at the origin of the right posterior com m unicating artery (PCoA). angiography showing near-complete occlusion of the aneurysm with pres-
The aneurysm had a neck size of 3.3 mm and was m ade of t wo compo- ervation of the fetal PCoA.

Carotid Terminus Aneurysms du ce th e risk of recan alizat ion . In th eir review of 46 p at ien ts
w ith 50 en dovascularly t reated carot id term in us an eu r ysm s, van
An eur ysm s of th e carot id term in us represen t 2 to 9%of all in t ra- Rooij et al97 repor ted a com plete or n ear-com plete occlu sion rate
cran ial an eu r ysm s (Fig. 44.3).8 Balloon - or sten t-assisted coiling of 94% directly after em bolizat ion . Procedure-related m or t alit y
techn iques, as well as the advanced Y-configuration stenting tech - an d m orbidit y w as repor ted in 4.4% of th e pat ien ts. At a m ean
n iqu es, can be used to address large an d w ide-n ecked lesion s. follow -up of 16.2 m on th s, th e ret reat m en t rate w as 14% an d all
Carefu l exam in at ion of th e relat ion sh ip bet w een th e an eu r ysm ret reated aneur ysm s w ere larger th an 10 m m in diam eter. Oish i
an d th e an terior an d m iddle cerebral ar teries is crucial in plan - et al8 also st udied th e efficacy an d safet y of en dovascular th er-
n ing t reat m en t . Placem en t of a sten t across th e an eur ysm al n eck apy in 25 pat ien ts h arboring 25 carot id term in us an eur ysm s.
can h elp diver t th e blood flow aw ay from th e an eu r ysm an d re- Com plete occlu sion rate w as ach ieved in 76% of p at ien ts at th e

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44 Endovascular Therapies for Aneurysm s of the Internal Carotid Artery 525

a b c

d e f

Fig . 44.3a–f (a) A 74-year-old wom an, with a previous history of sm ok- callosal artery aneurysm (2 m m × 1.8 m m). The patient underwent stent-
ing, was found to have a large right supraclinoid aneurysm on brain m ag- assisted coiling of her large paraclinoid aneurysm . (e ) Near-com plete
netic resonance im aging (MRI). (b–d) Cerebral angiography showed a obliteration of the aneurysm was achieved. The patient was discharged on
20 m m × 20 m m right paraclinoid aneurysm with a 6-m m neck, in addition postprocedural day-2 neurologically intact. (f) Follow-up MRA at 9 m onths
to a right m iddle cerebral artery aneurysm (6 m m × 6 mm ) and right peri- showed recurrent filling in the aneurysm al sac (arrow).

t im e of th e p rocedu re. A recu rren ce rate of 13.6%w as repor ted at cor resp on d in g tech n iqu e an d st rategy t h at car r y t h e opt im al
a m ean follow -u p of 24.4 m on th s. Th rom boem bolic even t s w ere sh or t- an d long-term ou tcom es. An eu r ysm s of variou s segm en t s
rep or ted in t w o p at ien t s. of th e ICA can n ot be exclu sively t reated by surgical clipping or
en dovascu lar th erapy. In stead, a m ult idisciplin ar y approach to
ever y lesion rem ain s th e key to su ccessful m an agem en t of th ese
an eur ysm s. A case-by-case approach en ables th e t reat ing physi-
cian to con sider all th e opt ion s an d to form ulate a com preh en -
■ Conclusion sive p lan th at can be th orough ly discu ssed w ith th e p at ien t . To
An eur ysm s of th e ICA are ch allenging lesion s th at can be ap - ach ieve th is, it is im por tan t to h ave all th e tools available in h an d.
proach ed eith er m icrosu rgically or en dovascularly. Th e greatest It is also im p or t an t to be able to u se th ese tools an d p erform all
ch allenge, h ow ever, is th e abilit y to m atch th e p ath ology to th e tech n iques w ith m axim al proficien cy an d a focus of excellen ce.

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526 V Cerebral and Spinal Aneurysms

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18. Weir B, Disney L, Karrison T. Sizes of ruptured and unruptured aneurysm s in Packing St u dy (HELPS t rial): p rocedu ral safet y an d operator-assessed ef-
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20. Joo SW, Lee SI, Noh SJ, Jeong YG, Kim MS, Jeong YT. W h at is th e sign ifi- r ysm Trial (ISAT) Collaborat ive Group. In tern at ion al Su barach n oid An eu-
can ce of a large n um ber of ru pt ured an eur ysm s sm aller th an 7 m m in r ysm Trial (ISAT) of n eurosurgical clipping versu s en dovascular coiling in
diam eter? J Korean Neu rosu rg Soc 2009;45:85–89 2143 pat ien t s w ith rupt ured in t racran ial an eur ysm s: a ran dom ised t rial.
21. Morit a A, Kirin o T, Hash i K, et al; UCAS Japan Invest igators. Th e n at ural Lan cet 2002;360:1267–1274
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Med 2012;366:2474–2482 subarach n oid h aem orrh age, death , or depen den ce an d st an dardised m or-
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an eu r ysm s: p robabilit y of an d risk factors for an eu r ysm ru pt u re. J Neu ro- In tern at ion al Subarach n oid An eur ysm Trial (ISAT): long-term follow -up.
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eur ysm s: inciden ce of r upt u re an d risk factors. St roke 2009;40:313–316 An eur ysm Trial. J Neurosurg 2012;116:135–144

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44 Endovascular Therapies for Aneurysm s of the Internal Carotid Artery 527

44. Spet zler RF, McDougall CG, Albuquerqu e FC, et al. Th e Barrow Rupt ured 63. Ch alouh i N, Sat t i SR, Tjoum akaris S, et al. Delayed m igrat ion of a pipelin e
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45. CARAT Invest igators. Rates of delayed rebleeding from int racran ial an eu- on s234, discussion on s234
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37:1437–1442 ar ter y t r u n k an eu r ysm s: feasibilit y of en d ovascu lar t rap p ing or proxim al
46. Pierot L, Spelle L, Vit r y F; ATENA Invest igators. Im m ediate clinical out- obliteration of th e ICA. Clin Neurol Neurosurg 2011;113:285–288
com e of pat ien t s h arboring un rupt ured in t racran ial an eur ysm s t reated 65. van Rooij W J. En dovascular t reat m en t of cavernous sin us an eur ysm s.
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zat ion device in th e t reat m en t of in t racran ial an eur ysm s: a review. World an eu r ysm su rger y: cu rren t tech n iqu es, in dicat ion s, an d ou tcom e. Neu ro-
Neurosu rg 2013;80:829–835 surger y 1996;38:83–92, discussion 92–94
52. Ch it ale R, Gon zalez LF, Randazzo C, et al. Single cen ter experien ce w ith 72. Ch oulakian A, Drazin D, Alexan der MJ. En dosaccular t reat m en t of 113
pipelin e stent: feasibilit y, tech n ique, and com plicat ion s. Neurosurger y cavernous carotid arter y aneur ysm s. J Neurointer v Surg 2010;2:359–362
2012;71:679–691, discussion 691 73. Vascon cellos LP, Flores JA, Veiga JC, Cont i ML, Shiozaw a P. Present at ion
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by fun ct ion al recon st ruct ion of th e paren t arter y: th e Budapest experi- m ic an eur ysm : en dovascular t reat m en t an d review of th e literat ure. AJNR
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57. Lylyk P, Miran da C, Cerat to R, et al. Curat ive en dovascular recon st r uct ion sten t-assisted en dovascu lar em bolizat ion of p araop h th alm ic an d su pra-
of cerebral an eur ysm s w ith th e pipelin e em bolizat ion device: th e Buen os sellar varian t superior hypophyseal an eur ysm s: th e Duke Cerebrovascu-
Aires experien ce. Neurosurger y 2009;64:632–642, discussion 642–643, lar Center experien ce in 57 pat ien t s. World Neurosu rg 2012;78:289–294
quiz N6 78. Fulkerson DH, Horn er TG, Payner TD, et al. Result s, outcom es, an d follow -
58. Täh t in en OI, Man n in en HI, Van n in en RL, et al. Th e silk flow -diver t ing u p of rem n an t s in th e t reat m en t of oph th alm ic an eur ysm s: a 16-year ex-
sten t in th e en dovascu lar t reat m en t of com p lex in t racran ial an eu r ysm s: perien ce of a com bin ed n eurosu rgical and en dovascular team . Neurosur-
tech n ical aspect s an d m idterm result s in 24 con secut ive pat ien t s. Neuro- ger y 2009;64:218–229, discu ssion 229–230
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59. Berge J, Bion di A, Mach i P, et al. Flow -diver ter silk sten t for the t reat m en t cal an d en dovascular t reat m en t of paraclin oid aneu r ysm s by a com bin ed
of in t racran ial an eur ysm s: 1-year follow -up in a m ult icen ter st udy. AJNR n eu rovascu lar team . Neu rosu rger y 2001;48:78–89, d iscu ssion 89–90
Am J Neuroradiol 2012;33:1150–1155 80. Boet R, Wong GK, Poon WS, Lam JM, Yu SC. An eu r ysm recu rren ce after
60. Klisch J, Turk A, Turn er R, Woo HH, Fiorella D. Ver y late th rom bosis of t reat m en t of paraclin oid/oph th alm ic segm en t an eur ysm s—a t reat m en t-
flow -diver t ing con st r uct s after th e t reat m en t of large fusiform posterior m odalit y assessm en t . Act a Neuroch ir (Wien ) 2005;147:611–616, discus-
circulat ion an eur ysm s. AJNR Am J Neuroradiol 2011;32:627–632 sion 616
61. Turow ski B, Mach t S, Kulcsár Z, Hänggi D, St u m m er W. Early fat al h em or- 81. Yadla S, Cam pbell PG, Grobelny B, et al. Open an d en dovascular t reat m en t
rhage after en dovascular cerebral an eur ysm t reat m en t w ith a flow di- of un rupt ured carot id-oph thalm ic an eur ysm s: clin ical an d radiograph ic
ver ter (SILK-Sten t): do w e n eed to reth in k ou r con cept s? Neu roradiology ou tcom es. Neurosu rger y 2011;68:1434–1443, discussion 1443
2011;53:37–41 82. Ch alou h i N, Tjou m akaris S, Du m on t AS, et al. Su perior hyp ophyseal ar ter y
62. McTaggar t RA, San t arelli JG, Marcellus ML, et al. Delayed ret ract ion of th e an eur ysm s h ave th e low est recurren ce rate w ith en dovascu lar th erapy.
p ip elin e em bolizat ion d evice an d corking failu re: p it falls of p ip elin e AJNR Am J Neuroradiol 2012;33:1502–1506
em bolizat ion d evice p lacem en t in t h e set t ing of a r u pt u red an eu r ysm . 83. Hauck EF, Welch BG, W h ite JA, et al. Sten t/coil t reat m en t of ver y large an d
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E250–E251 2009;71:19–24, discussion 24

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528 V Cerebral and Spinal Aneurysms

84. Deh dash t i AR, Le Rou x A, Bacigaluppi S, Wallace MC. Long-term visual 91. Gü resir E, Schuss P, Setzer M, Platz J, Seifert V, Vat ter H. Posterior com m uni-
outcom e an d an eur ysm obliterat ion rate for ver y large an d giant oph th al- cating arter y aneurysm -related oculom otor n er ve palsy: influence of surgi-
m ic segm en t an eur ysm s: assessm en t of surgical t reat m en t . Act a Neuro- cal and endovascular treatm en t on recovery: single-center series an d sys-
ch ir (Wien ) 2012;154:43–52 tem atic review. Neurosurger y 2011;68:1527–1533, discussion 1533–1534
85. Zada G, Breault J, Liu CY, et al. In ternal carot id ar ter y an eur ysm s occurring 92. Ch en PR, Am in -Hanjan i S, Albuquerque FC, McDougall C, Zabram ski JM,
at th e origin of fet al varian t posterior cerebral ar teries: surgical an d en do- Spet zler RF. Outcom e of oculom otor n er ve palsy from posterior com m u -
vascular experience. Neu rosurger y 2008;63(1, Su ppl 1):ONS55–ONS61, n icat ing ar ter y an eur ysm s: com parison of clipping an d coiling. Neurosur-
discu ssion ONS61–ONS62 ger y 2006;58:1040–1046, discu ssion 1040–1046
86. Golsh an i K, Ferrell A, Zom orodi A, Sm ith TP, Brit z GW. A review of th e 93. Ch alou h i N, Th eofan is T, Jabbou r P, et al. En dovascu lar t reat m en t of p os-
m an agem en t of posterior com m un icat ing ar ter y an eur ysm s in th e m od- terior com m u n icat ing ar ter y an eu r ysm s w ith ocu lom otor n er ve p alsy:
ern era. Surg Neu rol Int 2010;1:88 clin ical ou tcom es an d predictors of n er ve recover y. AJNR Am J Neurora-
87. Kim TG, Kim SH, Ch o KG, Ch ung SS. En dovascular t reat m en t of in tern al diol 2013;34:828–832
carot id-posterior com m un icat ing ar ter y w ide-necked an eu r ysm u sing 2 94. Han se MC, Gerrit s MC, van Rooij W J, Houben MP, Nijssen PC, Slu zew ski M.
En terprise sten t s in Y-con figu rat ion. Clin Neurol Neurosu rg 2013;115: Recover y of posterior com m u n icat ing arter y an eur ysm -in duced ocu lo-
1117–1120 m otor palsy after coiling. AJNR Am J Neuroradiol 2008;29:988–990
88. Raym on d J, Guilbert F, Weill A, et al. Long-term angiograph ic recurren ces 95. Velat GJ, Zabram ski JM, Nakaji P, Spet zler RF. Surgical m an agem en t of
after selective endovascular treatm ent of aneur ysm s w ith detachable coils. gian t posterior com m un icat ing arter y an eur ysm s. Neurosurger y 2012;71
St roke 2003;34:1398–1403 (1, Su ppl Operat ive):43–50, discussion 51
89. Cam pi A, Ram zi N, Molyn eu x AJ, et al. Ret reat m en t of ru pt ured cerebral 96. San ai N, Caldw ell N, Englot DJ, Law ton MT. Advan ced tech n ical skills are
an eur ysm s in pat ien t s ran dom ized by coiling or clipping in th e In tern a- required for m icrosurgical clipping of posterior com m un icat ing ar ter y
t ion al Subarach n oid An eur ysm Trial (ISAT). St roke 2007;38:1538–1544 an eur ysm s in th e en dovascu lar era. Neurosurger y 2012;71:285–294, dis-
90. Joh n ston SC, Dow d CF, Higash ida RT, Law ton MT, Du ckw iler GR, Gress DR; cu ssion 294–295
CARAT Invest igators. Predictors of reh em orrh age after t reat m en t of rup - 97. van Rooij W J, Sluzew ski M, Beute GN. In tern al carot id bifurcat ion an eu-
t u red in t racran ial an eur ysm s: th e Cerebral An eur ysm Rerupt ure After r ysm s: frequ en cy, an giograp h ic an atom y an d resu lt s of coilin g in 50
Treat m en t (CARAT) st udy. St roke 2008;39:120–125 an eur ysm s. Neuroradiology 2008;50:583–587

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45 Management Strategies for
Intracavernous Aneurysms
Babu G. W elch, Christopher S. Eddlem an, Aw ais Z. Vance, and Duke S. Sam son

An eur ysm s of th e cavern ou s carot id segm en t h ave long been m en t , a longer h orizon tal segm en t , an d a sh ort an terior vert ical
touted as h aving an overall low risk of rupt ure an d a low risk of segm en t . Th e cavern ou s ICA segm en t is th e m ost m edial st r u c-
life-altering com p licat ion s. Alth ough m any case series an d sm all t u re w ith in th e cavern ou s sin u s. Laterally, cran ial n er ves (CNs) III
prosp ect ive st u dies are rep or ted in th e literat u re, th e m ain dif- an d IV course w ith in th e sin us w all, w h ile CN VI cou rses w ith in
ficult y w ith cavern ous carot id an eur ysm s (CCAs) is th eir vir t u- th e cavern ou s sin u s close to th e ar ter y it self. Th e oph th alm ic an d
ally u n kn ow n n at u ral h istor y. Ret rosp ect ive grou ping of th ese m axillar y division s of th e t rigem in al n er ve also course w ith in
lesion s by locat ion an d n ot by et iology ser ves to fu r th er con fu se th e lateral w all of th e cavern ous sin us.
th e pict u re. Several ar terial bran ch es arise from th e cavern ou s segm en t ,
Over th e last decade, th e detect ion of CCAs h as in creased w ith n am ely th e division s of th e m en ingohyp op hyseal t run k (in ferior
th e u se of n on invasive im aging st u dies for variou s n eu rologic hyp op hyseal ar ter y, ten tor ial ar ter y, an d clival bran ch es), t h e
com plaints. Cerebrovascular specialists com m only encounter pa- in ferolateral t ru n k (blood supply to th e cavern ous sin us CNs,
t ien ts w ith u n ru pt u red, an d oth er w ise asym ptom at ic, CCAs in gasserian gan glion , an d caver n ou s sin u s d u ra), an d t h e cap su -
search of a t reat m en t recom m en dat ion . As th e m an agem en t lar ar teries of McCon n ell (blood supply to th e pit uitar y glan d).
ch oices h ave in creased, so h as th e qu est ion of ap prop riate gu id- An om alous em br yon ic vascular an astom oses can also occur to
an ce for m an aging th ese lesion s. th e cavern ou s segm en t , th e m ost com m on being a persisten t t ri-
Com m on in dicat ion s for t reat m en t of CCAs in clu de an eu r ysm gem in al ar ter y th at is foun d on 0.02 to 0.06% of cerebral angio-
grow th , ip silateral cran ial n er ve (CN) deficit s, ch ron ic h eadach es, gram s.1 The presence of these vascular anom alous connection s is
an d th e sequelae of rupt u re (e.g., cavern ou s carot id fist u la [CCF], often associated w ith an in creased prevalen ce of oth er vascular
cavern ous-sin u s syn drom e). Historically, th e t reat m en t opt ion s abn orm alit ies such as an eur ysm s, foun d in 14% of all cases.2
for t h e CCA in clu ded con ser vat ive n on su rgical m an agem en t
an d su rgical st rategies su ch as h u n ter ian ligat ion w it h or w it h -
ou t bypass revascu larizat ion . Over th e past decade, en dovascu-
lar tech n iqu es h ave n early su p p lan ted su rgical st rategies th rough ■ Natural History and
t h e u se of coils, vascu lar recon st r u ct ion , an d flow -d iver t in g
d evices. With th e litany of ch oices available an d th e con t in ued
Clinical Presentation
m yster y of th e act u al n at u ral h istor y of cavern ou s carot id le- Alt h ough t h e occu r ren ce of CCAs is often at t r ibu ted to t rau m a
sion s, decision s are often m ade on an in dividu al basis w ith ou t or in fect ion , a com m on sym ptom at ic presen tat ion in th e elderly
over w h elm ing eviden ce to su pp or t any sp ecific st rategy. populat ion suggest s a m ore ben ign or idiopath ic et iology. Ge-
Th is ch apter p resen t s th e in form at ion cu rren t ly available re- netic, environ m ental, and h abitual risk factors are sim ilar to those
garding CCAs, th e in dicat ion s for t reat m en t , th e available m o- of oth er in t racran ial an eur ysm s, but th e n at ural h istor y an d va-
dalit ies of t reat m en t , an d th e ou tcom es of th ose procedures. riet y of clin ical presen t at ion s of CCAs are m ore h igh ly varied.
Many cavern ous an eur ysm s are asym ptom at ic.
Cavern ou s carot id an eu r ysm s are th ough t to accou n t for 2 to
9% of all an eu r ysm s occurring distal to th e cer vical carot id seg-
m en t 3 an d are th e m ost com m on site for t raum at ic an eu r ysm s
■ Anatomy associated w ith skull base fract ures. CCAs are th e four th m ost
Th e cavern ou s sin u s p rovides a u n iqu e environ m en t for th is seg- com m on m irror an eu r ysm lesion s, w ith m iddle cerebral ar ter y
m en t of th e in tern al carot id arter y (ICA). Th e close proxim it y of an eur ysm s being th e m ost frequ en t .4
m ultiple cran ial n er ves, dural adh esion s, an d bony borders can Risk assessm en t of CCAs rem ain s difficult due to grou ping of
com p licate access to any path ology in th e region . Paradoxically, dissim ilar lesion s in th e literat u re, sh or t-term follow -u p , an d
it is also th is environ m en t t h at creates a m ore ben ign n at u ral variou s associated com orbit ies. Th e largest p rosp ect ive st u dy
h istor y of subarach n oid h em orrh age th an an eur ysm s on th e dis- to date on u n r u pt u red an eu r ysm s, t h e In ter n at ion al St u dy of
tal ICA. Un ru pt u red In t racran ial An eu r ysm s (ISUIA), rep or ted a h igh ly
Th e im por t an t bony relat ion sh ips of th e cavern ou s sin u s in - size-dep en d en t ru pt u re risk.5 Asym ptom at ic CCAs of sizes 13 to
clu de th e an terior clin oid p rocess (ACP), th e p osterior clin oid 24 m m an d ≥ 25 m m h arbor a 3% an d 6.4% rupt u re risk w ith in
process (PCP), an d th e lateral border of th e clivu s. Th e cavern ou s 5 years, respect ively.
ICA begin s at th e superior m argin of th e pet rolingu al ligam en t Cavern ou s carot id an eu r ysm s are u n iqu e in th e n u m ber of
an d exten ds to th e proxim al dural ring. Th is cavern ous segm en t w ays th at pat ients can presen t. A m ajorit y of CCAs are asym ptom -
is fu r t h er divid ed in to t h e p oster ior ascen ding or ver t ical seg- at ic an d are fou n d du ring th e w orku p for u n related con dit ion s.

529

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530 V Cerebral and Spinal Aneurysms

Th e acu it y of th e presen t at ion m ay p rovide som e clu e as to th e ography w ith or w ith ou t dyn am ic im aging is m ore suit able for
et iology of in cit ing even t . Rapidly developing sym ptom s are im aging bony relat ion sh ip s, w h ile m agn et ic reson an ce im aging
m ore often suggestive of rupture or acute throm bosis of a larger (MRI) en ables th e detail of th e cavern ous sin u s to be bet ter ap -
lesion, w h ereas a slow ly en larging lesion w ill produce a sim ilar, preciated . Hirai et al7 u sed con t rast-en h an ced th ree-dim en sion al
but m ore in sidious, on set of sym ptom s. con st r u ct ive in terferen ce in steady-st ate MRI (CE 3D- CISS) to ac-
Neu ro-op h th alm ologic sym ptom s are th e m ost com m on clin - curately predict in t radural presen tat ion of CCAs. Con e-beam CT
ical presen tat ion of CCAs. Th ese sym ptom s are related to m ass scan n ing en ables th e com bin at ion of cath eter angiograp hy an d
effect on th e su rrou n ding du ra an d cran ial n er ves. Var ying de- conven t ion al CT im agin g by acqu ir in g bot h im ages from a ro -
grees of oph th alm op legia m ay be th e resu lt of m ass or acute t at ing C-arm in th e angiograp hy su ite. Th is m odalit y augm en t s
th rom bosis of th e sin u s it self. St iebel-Kalish et al3 reported a d igit al su bt ract ion angiograp hy (DSA) by ren d er ing 3D im ages
com p lete cavern ou s sin u s syn drom e in 18.4% of p at ien t s in th eir of th e surroun ding bon e as w ell as vascular t issu e. High -field 4D
ser ies. Pain associated w it h CCAs m ay m an ifest as u n ilateral con t rast-en h an ced MR angiography 8,9 en ables h igh sp at ial im ag-
h eadaches, retro-orbital headaches, or facial pain related to irrita- ing an d th e abilit y to ren der h igh ly det ailed 3D im ages, perm it-
tion of th e trigem inal n er ve. Less com m on ocu lofacial con dition s t ing view ing from all angles an d th e su bt ract ion of su rrou n ding
in clu de ocu lar sym path et ic p aresis, com pressive opt ic n eu ropa- st ruct ures (e.g., bon e, dura).
thy, cor n eal hypesth esia, an d oth er dysesth esias related to t ri- Im aging is n ot lim ited to ju st th e m orp h ological det ails of th e
gem in al n er ve irritat ion . an eur ysm or its surroun ding an atom y. Ult rasoun d, in par t icu lar
Alth ough an ecdotal eviden ce suggest s th at th e larger th e CCA, t ran scran ial Dop p ler m easu rem en t s,10 h as t aken on a n ew role
th e greater th e p oten t ial for th rom bu s form at ion an d p ossible in determ in ing t h e p resen ce of em boli. Given th at th e clin ical
isch em ic p resen t at ion , th is h as n ot been born e out in th e litera- presentation can involve transient ischem ic-like sym ptom s, som e
t u re. Lesion size is also associated w ith dest r u ct ion of th e su r- par t ially th rom bosed lesion s m ay be prod u cing em boli. Detec-
rou n ding st r u ct u re of th e paran asal sin u ses an d tem p oral bon e. t ion of th ese em boli m ay sw ay th e m an agem en t st rategy to p o-
A dram at ic presen tat ion of subarach n oid h em orrh age, epistaxis ten t ially in clude an t iplatelet agen ts or even an t icoagulat ion . Th e
via th e paran asal sin u ses, or cavern ou s sin u s syn drom e is rare occuren ce of dist al em bolizat ion m ay also in fluen ce th e t reat-
but p lau sible. m en t of sm aller lesion s.
In all cases of r upt ured CCAs, th e clin ical presen tat ion varies
w ith th e locat ion of th e h em orrh age. If th e lesion h as en tered th e
in t racran ial su barach n oid sp ace, th e w ell-kn ow n presen t at ion
of su barach n oid h em orrh age is likely. Rupt u re of CCAs is also a ■ Treatment Indications
purpor ted cause of n on t rau m at ic cavern ous carot id fist ulas. Im -
Cavern ou s carot id lesion s w ith ou t a su barach n oid p resen t at ion
aging of th is p h en om en on is rare du e to th e likelih ood th at th e
are th ough t to h ave a low r upt ure risk an d n ot con fer life-th reat-
aneurysm itself is obliterated at the tim e of rupture. Fistulas from
en ing p roblem s. Even sym ptom at ic lesion s, w h ich often p resen t
rupt ured CCAs are t ypically classified as h igh -flow lesion s an d
w ith ocular m an ifestat ion s, m ay regress over t im e.3 Som e factors
direct (Barrow t yp e A6 ). As a result of direct ar terial flow th rough
th at m ay suggest a m ore m align an t h istor y in clu de ret ro-orbit al
th e su rrou n ding vein s, an d often th e su perior op h th alm ic vein ,
pain , larger size, presen tat ion to th e su barach n oid sp ace, an d
ven ou s reflu x occurs an d can lead to ch em osis, pu lsat ile exoph -
partial throm bosis. Ruptured CCAs, regardless of their clinical pre-
th alm os, an d proptosis. Orbital bru it s are n ot u n com m on .
sen tat ion , w arran t expedit iou s m an agem en t .
According to th e ISUIA, large CCAs are n ot benign , h aving a
rupt ure risk of 3% or greater over 5 years in lesion s > 13 m m in
size. In a st u dy of 136 lesion s, Ch ou lakian et al11 suggested th at
■ Imaging pat ien ts w ith CCAs > 15.3 m m w ere m ore likely to p resen t w it h
h em or rh age or cran ial n er ve p alsy. An elevated r u pt u re r isk is
On e of t h e m ost ch allen gin g asp ect s of CCAs is select in g an d
also p rop osed for t h ose lesion s t h at d em on st rate d om e p rot r u -
in terpret ing th e app rop riate im aging m odalit y. Th e cavern ous
sion in to t h e su barach n oid sp ace or su r rou n d ing sin u ses. It is
carot id ar ter y segm en t is su rrou n ded by bon e, blood, du ra, an d
u n derstood th at part ially th rom bosed lesion s can lead to th rom -
n eu ral st ru ct ures, m aking it difficult to precisely ch aracterize
boem bolic com plicat ion s.
th e CCA w ith a single im aging m odalit y. Th e com m on qu est ion
of w h eth er CCAs project in to th e subarach n oid space can often
go u n an sw ered d esp ite h igh -qu alit y im aging. Determ in ing t h e
an atom ic relat ion sh ips am ong th e dural rings, carot id cave, an d
cavern ou s sin u s bou n daries sh ou ld be th e goal of any im aging
■ Management Strategies
evalu at ion of CCAs. Th e goals of t reat m en t for CCAs are th e sam e as w ith oth er in t ra-
Non invasive im agin g m odalit ies h ave con t in u ed to advan ce cran ial an eur ysm s: elim in at ion of th e lesion , avoidan ce of injur y
our understanding of the anatom ic details of the cavernous sinus. to t h e su r rou n d ing an atom ic st r u ct u res, an d p reser vat ion of
Alth ough referen ces to less specific lan dm arks such th e an eu - adequ ate blood flow to th e dist ribut ion of th e ar teries involved.
r ysm relat ion sh ip to th e oph th alm ic arter y an d th e an terior cli- Disagreem en t st ill exist s regard in g t h e m an agem en t of CCAs,
n oid process are st ill com m on , m odern im aging tech n iques seek esp ecially t h ose th at are asym ptom at ic. Man agem en t by obser-
to exploit th e physiological proper t ies of cavern ous sin us com - vat ion alon e can h ave m ixed results in sym ptom at ic pat ien ts,
p on en t s alon g w it h im age m erge tech n iqu es to p rovid e bet ter especially in pat ien t s w ith ret ro-orbit al an d facial pain . In som e
an atom ic data. Mult idetector com puted tom ography (CT) angi- cases, an t ip latelet th erapy m ay be in it iated, esp ecially in ligh t of

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45 Management Strategies for Intracavernous Aneurysms 531

t ran sien t isch em ic at t acks. How ever, p at ien ts w ith m ore om i- m ass. Any surgical approach to CCAs w ill involve cran ial expo-
n ous sym ptom s, su ch as diplopia or oph th alm oplegia, often do su re of th e an eu r ysm an d p roxim al vascu lar con t rol of th e ICA
n ot respon d as w ell as to obser vat ion al m an agem en t .3 in th e n eck via su rgical exposure or en dovascu lar balloon occlu-
On ce arriving at a decision to t reat an eur ysm s of th e cavern - sion . Each approach is dictated by th e locat ion of th e CCA on th e
ous segm en t , it is in cum ben t on th e pract it ion er to un derstan d cavern ous segm en t .
th e risks of each th erapy. In order to deter m in e th e st roke r isk Lesion s located on th e an terior gen u an d distal h orizon t al
of per m an en t ar terial occlu sion a balloon occlu sion test (BTO) is segm en t can be ap proach ed u sing st an dard or exten ded pteri-
com m on ly p er form ed . Many specialt y cen ters add a secon dar y on al approach es (Fig. 45.1). An an terior clin oidectom y is often
test (e.g., single ph oton em ission com puted tom ography [SPECT], requ ired an d can be p er for m ed in an ext rad u ral or in t rad u ral
hypoten sion , elect roen ceph alogram [EEG], t issue oxygen m on i- fash ion . Alt h ough bot h ap p roach es im p rove t h e access to th e
toring) to assist further in evaluating patien ts w ho do not develop carot id cave an d cavern ou s segm en ts, th ere are n u an ces to con -
a clin ical deficit during th e BTO itself. If such test ing suggest s sider. Ext radu ral clin oid resect ion delays th e in t radu ral evalu a-
adequate collateral filling of th e ipsilateral an terior circulat ion t ion of th e an eu r ysm , th eoret ically decreases th e ch an ce of direct
an d th ere are n o con t ralateral vascular lesion s th at w ould be opt ic n er ve inju r y, an d jeop ardizes con t rol sh ould a carot id in -
th reaten ed by th e ch ange in blood flow, th en th e in tern al carot id jur y occur. An in t radural clin oid resect ion can be bet ter tailored
can be p r im ar ily occlu d ed w ith a < 10% isch em ic r isk.12 If t h e to operat ive n eed bu t requires th at th e resect ing tool operate
collateral circu lat ion is in adequ ate or if con t ralateral vascular le- closer to th e carot id ar ter y an d opt ic n er ve.
sion s exist th at m ay pu t th e p at ien t at risk of r u pt u re (e.g. an te- Cavern ou s carot id an eu r ysm s located on th e h orizon t al seg-
rior com m u n icat ing ar ter y an eu r ysm s), revascu larizat ion sh ou ld m en t of th e cavern ous carot id arter y can be approach ed th rough
be con sidered. Th e results of th e BTO w ill determ in e th e t ype of Parkin son’s t riangle. Th is t riangle is form ed by th e t roch lear
bypass graft n eeded. Total failure of th e BTO w ould suggest th e n er ve m edially an d th e V1 segm en t of th e t rigem in al n er ve later-
n eed for a h igh -flow bypass (e.g., saph en ous vein ). In term ediate ally, w ith th e base of th e t riangle exten ding from th e ten torial
failure of th e BTO w ould suggest th at m ediu m - to low -flow re- en t r y p oin t of t h e t roch lear n er ve to th e m edial edge of th e t ri-
vascu larizat ion m igh t su ffice (e.g., superficial tem poral or radial gem in al ganglion in Meckel’s cave. Posterior gen u an d proxim al
ar ter y to th e m iddle cerebral ar ter y [MCA]). h orizon t al segm en t CCAs are often n ot t reated w ith direct clip
Based on th e p rep rocedu ral evalu at ion , a recon st ru ctive or recon st ru ct ion , given th e in h eren t difficult y w ith th e surgical
decon st ru ct ive t reat m en t st rategy m ay be adopted. Recon st ru c- exposure an d th e in creased risk of p eriop erat ive m orbidit y.
t ive st rategies in clu de d irect m icrosu rgical clip ap plicat ion , coil If p r im ar y clip recon st r u ct ion is n ot p ossible bu t a en d ovas-
em bolizat ion w ith or w ith ou t th e u se of a vascu lar recon st ru c- cu lar access is proh ibited, paren t ar ter y sacrifice h as h istorically
t ion device, flow -diver t ing d evices, or th e u se of liqu id em bolic been th e opt ion of ch oice w ith or w ith out th e use of bypass re-
agents. Deconstructive strategies include parent artery occlusion, vascu larizat ion (Fig. 45.2). Paren t ar ter y sacrifice can involve
eith er su rgically or via en dovascu lar tech n iqu e, w ith an opt ion com p lete t rap p ing of th e CCA or proxim al carot id ligat ion to en -
for revascu larizat ion th rough bypass graft placem en t . Histori- able ret rograde th rom bosis of th e an eur ysm . W h en sacrifice is
cally, p aren t ar ter y occlu sion w ith or w ith ou t byp ass w as th e th e t reat m en t of ch oice, it is im por t an t to accou n t for all vessels
dom in an t st rategy; h ow ever, th e effect iven ess of en dovascu lar en tering an d exit ing th e an eu r ysm al segm en t . Ret rograde filling
devices h as en h an ced th e abilit y to m ain t ain th e paren t ar ter y of th e an eu r ysm via th ese vessels m ay lead to delayed rupt u re,
an d exclude th e CCA from th e paren t circu lat ion . In th e follow ing progression of cranial n erve sym ptom s, or throm boem bolic com -
sect ion s w e review th ese st rategies an d th eir ou tcom es. p licat ion s. W h en ever p ossible, any com p lete t rap p in g sh ou ld
in clu d e clip p lacem en t p roxim al to t h e op h t h alm ic ar ter y—a
com m on site for ret rograde su pply. W h en a byp ass is requ ired,
paren t vessel sacrifice sh ou ld occu r on th e sam e day to m in im ize
any ch allenge to bypass flow.
■ Surgical Management
Lim ited in dicat ion s exist for th e surgical m an agem en t of CCAs.
Alt h ough an argu m en t for im p roved d u rabilit y w it h su rgical
t reat m en t rem ain s, th e in it ial t reat m en t opt ion for th ese lesion s
is en dovascu lar. Despite th e su ccess of en dovascu lar th erapies,
■ Endovascular Strategies
all of th ese th erapies are depen den t on th e toleran ce an d effec- En dovascu lar st rategies for th e t reat m en t of CCAs con t in u e to
t iven ess of long-term an t ip latelet th erapies. W h en elevated an t i- progress. Alth ough it is im por t an t to take advan tage of n ew er
platelet risks, m edicat ion in toleran ce, or m edicat ion resistan ce tech n ologies, t h e p ract it ion er m u st d o so w it h an ap p reciat ion
h as been con firm ed, recon st ruct ive or decon st ru ct ive surgical of th e un derdeveloped risk profiles. W h en th e use of an t iplatelet
opt ion s sh ould be en ter tain ed. In th e curren t era, cavern ous an - agen ts is an t icipated, it is im por t an t to en su re respon siven ess to
eu r ysm s th at p resen t to th e su barach n oid space, or t ran sit ion al th e ch osen m edicat ion . Th e in ciden ce of asp irin resist an ce h as
an eu r ysm s, are occasion al can didates for su rgical m an agem en t . been est im ated to range from 0.4% to 60%, an d clopidogrel resis-
Th e com p lexit y of su rgical recon st r u ct ion of a CCA sh ou ld n ot tan ce from 5% to 31%.14,15 Th ere are m any test s for exam in ing
be u n derest im ated. Despite t reat ises to th e con t rar y,13 th e per- platelet dysfu n ct ion , bu t th ere is n o cu rren t stan dard m eth od of
m an en t m orbidit y th at can occu r du e to requ isite m an ip u lat ion m easu rem en t .
of m ult iple cran ial n er ves sh ould be a salien t poin t of th e pre- Sim ilar to su rgical m an agem en t , th e m ost establish ed of th e
operat ive discussion . Likew ise, th e in t roduct ion of th e m ass of endovascular strategies is parent arter y sacrifice (Fig. 45.3). Most
a surgical clip m ay carr y sim ilar long-term risks to a large coil often th is involves coil occlusion of th e paren t ar ter y, across th e

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532 V Cerebral and Spinal Aneurysms

Fig. 45.1 Illustration of intraoperative exposure of a transitional internal optic canal. Important anatom ic landm arks for this exposure are labeled. It
carotid artery (ICA) aneurysm . A left pterional craniotomy was perform ed is important to note the medial displacem ent of the optic nerve, as it will
for surgical repair of a transitional aneurysm . An anterior clinoidectomy cover the m edial lobe of the aneurysm that projects into the cavernous
has been perform ed for improved visualization and decompression of the sinus. ant., anterior; CN, cranial nerve. (Courtesy of Suzanne Truex.)

Fig. 45.2a–d Patient with a partially throm bosed an-


eurysm presenting with stroke. A 56-year-old wom an
a b
presented with a right hem isphere stroke. Her symp-
tom s were preceded by a progressive retro-orbital
headache on the right. (a) A com puted tom ography
angiography (CTA) at presentation dem onstrated a
partially throm bosed aneurysm of the right cavernous
sinus (arrow). (b) Following 6 weeks of dual antiplate-
let therapy, substantial recanalization of the aneurysm
occurred (arrow). A trial balloon occlusion resulted
in im m ediate improvement of her retro-orbital head-
aches, no clinical deficit, and minor asymmetry on sin-
gle photon em ission computed tom ography (SPECT)
imaging. A left-sided superficial temporal artery (STA)–
m iddle cerebral artery (MCA) bypass was perform ed
with proxim al sacrifice of the cervical carotid artery.
(c,d) Postoperative angiography dem onstrated retro-
grade throm bosis of the aneurysm and patency of the
c d
bypass.

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45 Management Strategies for Intracavernous Aneurysms 533

a b

c d

Fig. 45.3a–d A 66-year-old m an presented with 3 to 4 m onths of pro- im aging. (b) A lateral ICA projection angiogram dem onstrated the distal
gressive double vision, looking to the left. After he consulted with several aspect of the neck (arrow). Placem ent of a flow diversion device was unsuc-
physicians, a m agnetic resonance im aging (MRI) scan was ordered that cessfully at tempted. The aneurysm and parent artery were subsequently
demonstrated a 2.7-cm aneurysm of the left cavernous segment. (a) Formal coil embolized. Postprocedural follow-up demonstrated improvement in the
angiography revealed a giant aneurysm of the internal carotid artery (ICA) patient’s diplopia. (c) Lateral angiography dem onstrated proxim al aspect
(anteroposterior [AP] projection). Balloon test occlusion of the left carotid of the coil m ass (arrow). (d) Contralateral ICA injection on the AP projection
did not produce a neurologic deficit; there was no perfusion deficit on SPECT dem onstrates adequate filling of the ipsilateral circulation.

n eck of th e an eu r ysm . Involving th e n eck of th e an eur ysm ser ves vice n avigat ion an d ar terial w all dam age th at previously existed.
to m in im ize th e risk of distal em boli as w ell as th e exacerbat ion It is im p or t an t to ap p reciate t h e p rop er t ies of com p lian t an d
of cavern ous sin us sym ptom s via ret rograde filling of th e an eu- n on com p lian t balloon s to p rop erly u t ilize t h is tech n iqu e. Th e
r ysm . Alth ough th e m orbidit y of en dovascular carot id sacrifice u se of sten t s or vascu lar recon st r u ct ion d evices (VRDs) to p ro -
h as im proved propor t ion ally w ith cath eter an d coil tech n ology, vide a con t in uou s barrier to coil h ern iat ion h as also becom e a
t h e em p loym en t of t h is st rategy is becom in g less frequ en t as com m on t reat m en t m eth od. As a resu lt of th e m at u ring st roke
lu m in al p reser vat ion tech n iqu es h ave advan ced. th erapies, som e au th ors h ave docu m en ted th e u se of ret rievable
Coil em bolizat ion is st ill a m ore com m on ly em p loyed tact ic VRDs in an eu r ysm em bolizat ion .16 Th e u se of su ch a device of-
for en dovascular m an agem en t of CCAs. In m any cases, CCAs are fers th e ben efit of a rem ovable device w ith out th e vessel occlu-
w ide-n ecked or fusiform an d n ecessitate th e use of a but t ressing sion th at is in h eren t to any balloon -assisted tech n iqu e.
device to m aintain lum inal patency. The use of balloon assistance Th e prom ise of decreased com p act ion , or recu rren ce, th rough
to par t ially occlude th e an eur ysm n eck du ring coil deploym en t t h e u se liqu id em bolic agen t s h as been p rop osed for larger
rem ain s a w ell-p ract iced tech n iqu e. Im p rovem en ts in balloon CCAs.17 Th ese agen t s solidify w h en in con tact w ith blood, fill th e
tech n ologies h ave resolved m any of th e difficult ies related to de- an eur ysm dom e an d form a physical barrier to blood en tering

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534 V Cerebral and Spinal Aneurysms

a b c

d e f

Fig. 45.4a–f Tandem giant cavernous and ophthalmic segment aneu- apy achieved the goal of vessel preservation and treatm ent of both lesions
rysms. A 54-year-old woman presented with a palsy of her sixth cranial nerve with preservation of the ophthalm ic artery (arrow, in f). Headaches and a
on the right. (a–c) Digital subtraction angiography (DSA) dem onstrated transient worsening of her cranial nerve palsy complicated her postopera-
a 2.5-cm aneurysm of the right cavernous segm ent that was proxim al to a tive course despite a successful technical deploym ent. She had resolution
9-m m ophthalm ic segm ent aneurysm (arrow). (d–f) Flow diversion ther- of her postoperative symptom s at 3 m onths follow-up.

th e an eur ysm . A balloon m u st be u sed to cover th e an eu r ysm t reated w ith th is device; 30% of t reated th rom bosed an eu r ysm s
n eck to preven t th e distal m igrat ion of em bolic m aterial. Al- h ad com pletely disappeared, w ith an addit ion al 52% dem on -
t h ough occlu sion rates com p arable to th ose w it h coil em boli- st rat ing par t ial sh rin kage.23
zat ion h ave been rep or ted , en t h u siasm for t h is ap p licat ion of
em bolic liqu ids h as been tem pered by rep or t s of delayed vessel
occlusion.17–19
Th e t reat m en t of CCAs u sing flow -diver t ing devices (FDDs) is
th e m ost m odern m odalit y (Fig. 45.4). Un like m ore conven t ion al
■ Combined Strategies
sten t s, cu rren t FDDs are braided an d are design ed to decrease Although endovascular techniques dom inate the available options
th eir ou t w ard radial force. Accordingly, th ese devices require a for the treatm ent of CCAs, the com bin ation of m icrosurger y an d
m odified approach to deploym en t an d con st it ute a n ew en do- en d ovascu lar tech n iqu es sh ou ld rem ain a p oin t of discu ssion in
vascu lar tech n ique. Early success in Europe an d South Am erica cases in w hich there are cont raindicat ions to purely endovascular
resu lted in Food an d Drug Adm in ist rat ion (FDA) approval of th e therapies (e.g., bleeding diathesis, ant iplatelet resistance, tort uous
first FDD in th e Un ited States, th e Pipelin e Em bolizat ion Device proxim al an atom y). W h en em p loyed, a com bin ed st rategy m ay
(PED; Covidien , Man sfield, MA). Kan et al20 reported on 58 an eu - be used sim ultan eou sly or in st ages, depen ding on th e pat ien t ,
r ysm s t reated w ith FDDs; 63% of th e an eur ysm s w ere CCAs. Th e th e lesion , an d th e cap abilit ies of th e t reat ing facilit y (Fig. 45.5).24
rate of m ajor com p licat ion s w as 8.5%, com p r isin g 1.6% w it h As an adju n ct to su rger y, en dovascular tech n iques m ay be ap -
st roke an d 6.9% w ith fat al, postdep loym en t h em orrh ages, n on e plied for proxim al vessel con t rol, vessel sacrifice, as w ell as su rgi-
of w h ich w ere related to cavern ous an eur ysm s. On e of th e 37 cal salvage. Balloon occlu sion m ay be u sed for p roxim al con t rol
(2.7%) p at ien ts w ith an eu r ysm s th at p resen ted from th e cavern - in lieu of surgical exposure of th e cer vical carot id ar ter y. W h en
ous to hypophyseal segm en t developed w orsen ing of a cran ial perform ed w ith a large-lu m en cath eter, th e sam e exposu re m ay
n eu ropathy. O’Kelly reported on th e Can adian experien ce w ith be used to provide suct ion decom pression . Th is tech n ique is u se-
FDDs, w h ere 30% of th e cases w ere CCAs, an d 70% presen ted fu l to redu ce th e volu m e of th e an eu r ysm an d im prove visu aliza-
w ith cran ial n europathy, of w h ich 61% im proved, 11% h ad sub - t ion for prim ar y clip recon st r u ct ion . Fu lkerson et al25 repor ted a
tot al im provem en t , an d 11.5% w orsen ed.21 A large m ult icen ter com parative experience of ophthalm ic aneurysm s m anaged w ith
Italian ret rospective study of flow diverter treatm ent of 295 intra- an d w ith ou t th is en dovascular adjun ct in 2009. Endovascular
cran ial an eur ysm s repor ted a 1-m on th m orbidit y an d m ort alit y su ct ion decom pression p rovided variable ben efit th at w as p ri-
of 3.7% an d 5.9%, respect ively. Th is st u dy in clu ded 76 cavern ou s m arily related to th e p resen ce of calcificat ion w ith in th e an eu -
an eu r ysm s w it h a 4% (3/76) m or t alit y rate in t h is su bgrou p .22 r ysm w all. Most im por t an tly, th e u se an en dovascular adjun ct
In t h e Eu rop ean com m u n it y, th e SILK Flow Diver ter (Balt Ex- did n ot in crease th e procedu ral m orbidit y.
t r u sion , Mon t m oren cy, Fran ce) h as been evalu ated. Berge et al Th e n ecessit y to occlude th e ophthalm ic arter y during suct ion
repor ted on 77 un ru pt u red an eu r ysm s (32% CCAs) th at w ere decom p ression can n ot be overst ated . Th is m ay be addressed by

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45 Management Strategies for Intracavernous Aneurysms 535

a b c

Fig. 45.5a–c Transitional cavernous aneurysm . This 51-year-old wom an and subarachnoid components (arrow and arrowhead). Surgical exposure
presented with a history of chronic worsening headaches. Magnetic reso- of the aneurysm confirm ed this location. An intraoperative rupture lim ited
nance im aging (MRI) suggestion of a proxim al carotid aneurysm was clari- the surgical repair of the aneurysm . (b,c) The proxim al cavernous compo-
fied on angiography (a) to be a transitional aneurysm with both cavernous nent of the aneurysm was treated using prim ary coiling techniques.

im proved balloon tech n ology th at en ables coverage of th e an eu - En d ovascu lar p roced u ral com p licat ion s are also related to
r ysm n eck during clip recon st r u ct ion of larger lesion s.26 In addi- bot h t h e ap p roach an d th e t reat m en t ren d ered . Th e clin ical se-
t ion to proxim al con t rol of an in t raoperat ive r u pt u re, su ch distal qu elae of con t rast ad m in ist rat ion , ion izin g rad iat ion , an d vas-
balloon placem ent m ay also m inim ize vessel stenosis, w hich is an cu lar access sh ou ld be a p oin t of d iscu ssion in clu d ed in any
inherent concern during clip reconstruction of dysplastic lesions. p reprocedural coun seling. During prim ar y coil em bolizat ion of
The surgical addition to endovascular therapy com es prim arily sim ilar-sized lesion s, th e possibilit y of th rom boem bolism an d
from flow augm en t at ion , or byp ass, in th e case of vessel sacri- ar terial injur y (perforat ion /dissect ion ) do n ot su bst an t ially differ
fice. Surger y m ay also provide a m ore precise distal vessel occlu- du ring th e m an agem en t of CCAs com pared w ith oth er p roxim al
sion (p roxim al to th e op h th alm ic ar ter y) in th e sam e set t ing. In carot id lesion s.
cases of tort uous proxim al an atom y, surgical cut-dow n and direct With th e expan ded applicat ion of en dovascular tech n ology
can alizat ion of t h e ICA m ay en able th e p assage of m icrocat h eters for recon st r uct ive m an agem en t of CCAs, th e effect of th e in t ro-
to u t ilize th e d esired en dovascu lar st rategy. du ct ion of a coil m ass h as been a poin t of sign ifican t discu ssion .
As early as 1994, Halbach et al27 dem on st rated > 90% resolut ion
or im provem en t in pat ien t s presen t ing w ith n eurologic deficit s
from m ass effect w ho received endovascular treatm en t. In a 2005,
St iebel-Kalish et al3 suggested a greater im p rovem en t in sym p -
■ Complications tom s for th ose pat ien ts w h o presen ted w ith pain com pared w ith
Com p licat ion s in t h e m an agem en t of CCAs can occu r at any diplop ia, alth ough 56% of p at ien t s w h o p resen ted w ith eith er
p oin t after an obser vat ion or procedural t reat m en t m eth od h as com plaint noted im provem ent w ithout inter vention. More recent
been selected. Th e un ique an atom y of th e cavern ous sin us can rep orts h ave dem onst rated th e p ossibilit y of an overall reduc-
resu lt in sim ilarly n ovel com p licat ion s. We h ave com m en ted on t ion in an eu r ysm al volu m e follow ing th e placem en t of coils, an d
th e r u pt u re risk of CCAs in th e in t rod uct ion . Com m on , n onp roc- con t in u e to d ocu m en t sym ptom at ic relief from m ass effect .24,28
edu ral m orbidit ies related to th ese lesion s in clu de cran ial n er ve The recover y process of sym ptom s related to m ass effect is closely
palsy, ch ron ic h eadach e, an d th rom boem bolic even ts. Surgical related to th e specific sym ptom , th e du rat ion of th e sym ptom ,
m an agem en t in t rodu ces th e p ossibilit y of ven ou s in farct ion an d an d th e p at ien t’s com orbidit ies.
cerebrospin al flu id (CSF) leakage. En dovascular com plicat ion s Alth ough flow diversion th erapy m ay produ ce a m ore reliable
m ay be related to th e com m on addit ion of an t iplatelet agen t s as m ass redu ct ion over t im e, in creased use of th is t ype of th erapy
w ell as d elayed sequ elae from t h e p rogressive t h rom bosis t h at h as produced a n otable set of com plicat ion s th at rem ain poorly
is par t of th e t reat m en t process. qu an t ified or u n derstood. Morbidit y related to flow diversion
Microsu rgical com plicat ion s are t yp ically related to t w o as- t reat m en t in clu des an eu r ysm r u pt u re days to several m on th s
pects of th e t reat m en t , n am ely th e ap p roach an d th e t reat m en t after treatm ent as w ell as delayed lobar h em orrhage rem ote from
ren d ered. Any ap p roach to th e cavern ou s sin u s can lead to com - th e t reated an eu r ysm .22,23,29–32 Th e m ech an ism for delayed rup -
plications of ven ous in farction due to sacrifice of th e sylvian vein s, t u re m ay in clu d e in su fficien t flow d iversion resu lt in g in en t r y
dam age to cran ial n er ves located in th e sin u s w all, an d CSF fis- to rest ricted exit of blood from th e an eu r ysm , an eur ysm w all
t u la form at ion w ith th e sp h en oid sin u s. Prim ar y p aren t arter y degradat ion by secreted p roteases from red th rom bu s, or a com -
recon st ru ct ion can lead to n arrow ing an d even t ual th rom bosis bin at ion of th ese. W h ile t ran sform at ion of un diagn osed isch em ic
of th e p aren t ar ter y, dam age to surrou n ding bran ch es of th e in farcts seem s a likely exp lan ation for th e delayed h em orrh ages,
proxim al in t racran ial ICA (e.g., oph th alm ic ar ter y, m en ingohy- a decrease in vessel com plian ce related to device placem en t h as
pop hyseal t r u n k), an d in com plete an eu r ysm obliterat ion . Any also been th eorized to alter hem odyn am ics w ith in th e paren t
su rgical app roach to th e cavern ou s sin u s w ill create a n ew su b - vessel. Fur th er scr ut iny of th e in creasing n um ber of flow diver-
arach n oid por t ion of th e ICA. Th e rupt u re risk of any residual sion t reat m en t s is cru cial to bet ter u n derstan d com p licat ion
an eu r ysm sh ou ld be calcu lated w ith th is in m in d. avoidan ce in th e t reat m en t of CCAs.

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536 V Cerebral and Spinal Aneurysms

use ranges from im m ediate cessation or reversal follow ing therapy


■ Postprocedure Care to 12 to 24 h ours of in t raven ou s h eparin to m in im ize th rom bo-
Regardless of m odalit y, th e care of CCAs does n ot cease w ith th e em bolic events. The presence of a non–flow diversion endolum inal
form ulat ion an d execut ion of th e in ter ven t ion . Vigilan ce for de- device requ ires d u al an t ip latelet th erapy for a period of 6 w eeks
layed com p licat ion s of th erapy is essen t ial. Recon st ru ct ive an d to 3 m on th s. Literat ure on FDDs suggests a m in im um dual an t i-
decon st ru ct ive st rategies carr y u n iqu e postop erat ive con sider- platelet du rat ion of 3 m on th s, bu t 1-year du rat ion is n ot ou t side
at ion s. Alth ough th e du rat ion of com p lem en tar y m edical th era- of th e stan dard of care.
pies varies am ong in st it u t ion s, n o on e w ou ld d isagree abou t th e Th ere is cu rren tly n o st an dard for follow -u p im aging in t h ese
n ecessit y of an establish ed protocol addressing an t iplatelet an d pat ien ts. As w ith th e ch oice of th erap ies, th e an atom y to be eval-
an t icoagu lat ion regim en s in th e postop erat ive period. u ated an d th e device used frequen t ly dict ate th e im aging follow -
In pat ien ts un dergoing decon st r uct ive st rategies, m a xim ized u p u sed. Digital subt ract ion angiography rem ain s th e im aging
collateral circu lat ion an d bypass p aten cy are a m ajor con cern . m odalit y of ch oice d u e to th e bony con fin es an d frequ en t u se of
Mean ar terial p ressu re m an agem en t an d volu m e st at u s are im - m etallic devices in th e t reat m en t of CCAs. How ever, n on invasive
por t an t con siderat ion s d u ring an d follow ing disch arge from th e st u d ies, su ch as h igh -field m agn et ic reson an ce angiograp hy, are
in ten sive care u n it . In large or gian t CCAs, steroids are often u sed gain ing in pop ularit y.
to reduce th e in flam m at ion an d in creasing h eadach es th at can
resu lt from an eu r ysm th rom bosis. Ret rograde filling of a lesion
t h at h as been in com p letely t rap p ed m ay p rod u ce a scen ar io of
d u ral exp an sion an d ir r it at ion in a t r igem in al n er ve dist r ibu -
■ Conclusion
t ion th at can severely affect th e fu n ct ion al, if n ot clin ical, ou t- An eu r ysm s of th e caver n ou s ICA can p resen t in a var iet y of
com e of th e pat ien t . An t iconvu lsan t m edicat ion s (e.g., ph enyt - clin ical sit u at ion s. Th e severit y an d du rat ion of th e clin ical com -
oin , levet iracetam ) are appropriate th erapeut ic opt ion s in th is plain t s, as w ell as th e an atom y of th e an eu r ysm , t yp ically govern
in st an ce. You nger p at ien ts w ith lesion s t reated by a decon st ru c- th e m an agem en t of th ese lesion s. Alth ough en dovascu lar st rate-
t ive tech n iqu es w arran t long-term su r veillan ce for de n ovo an - gies dom in ate cu rren t t reat m en t preferen ces, it is n ecessar y to
eu r ysm form at ion .33 u n derst an d th e m icrosurgical adjun ct s th at m ay provide a m ore
Follow ing th e tech n ical su ccess of a recon st ru ct ive st rategy, it du rable t reat m en t . Despite a low er risk of r u pt u re, th e n u m ber
is im port an t to d evelop a u n iform p rotocol for th e m edical m an - of cavern ous an eur ysm s w ill in crease w ith th e prevalen ce of
agem en t of th e pat ien t . Du e to th e pau cit y of defin it ive litera- n on invasive im aging. It is in cum ben t upon th e cerebrovascular
t ure, th e pract ice of post procedural an t icoagulan t an d an t iplate- sp ecialist to u n d erst an d t h e t reat m en t opt ion s available for
let use is frequ en t ly an in st it u t ion al ph en om en on . An t icoagu lan t sym ptom at ic an eur ysm s of th e cavern ou s sin us.

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an eur ysm s: an alysis of risks an d clin ical outcom es. Neurosurger y 2009; n ial an eur ysm : a system at ic review. Clin Neuroradiol 2012;22:295–303
64(3, Suppl):on s107–on s111, discussion on s111–on s112 33. Fujiw ara S, Fujii K, Fukui M. De novo an eur ysm form at ion an d an eur ysm
26. Steiger HJ, Lin s F, Mayer T, Schm id-Elsaesser R, St u m m er W, Turow ski B. grow th follow ing th erapeut ic carot id occlusion for in t racran ial in tern al
Tem porar y an eur ysm orifice balloon occlusion as an altern at ive to ret ro- carot id arter y (ICA) an eur ysm s. Act a Neuroch ir (Wien ) 1993;120:20–25
grade su ct ion decom p ression for gian t p araclin oid in tern al carot id ar ter y

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46 Surgical Therapies for
Carotid-Ophthalmic Aneurysms
Arthur L. Day, Yoshua Levy Esquenazi, and Buelent Yapicilar

An eur ysm s origin at ing from th e proxim al in t racran ial in tern al Vascular Relationships
carot id ar ter y in close p roxim it y to th e an terior clin oid process
Th e op h th alm ic segm en t (Oph Seg) is th at p or t ion of t h e su pra-
h ave been collect ively iden t ified as paraclin oid an eur ysm s. Th is
clin oid ICA th at begin s at th e DR an d en ds at t h e t akeoff of th e
ch apter ad d resses on ly t h e an eu r ysm s ar isin g from t h e op h -
posterior com m u n icat ing (PCoA) ar ter y. Th is segm en t is en t irely
t h alm ic segm en t , an d d iscu sses th e u n iqu e set of an atom ic an d
con t ain ed w ith in th e su barach n oid sp ace; h en ce, any an eu r ysm
clin ical feat u res, h em orrh age risk, in dicat ion s for in ter ven t ion ,
arising from th is region carries at least som e risk for in t racran ial
an d m eth ods for safe an d effect ive surgical t reat m en t w ith an eu-
h em orrh age regardless of size. Th e Oph Seg h arbors t w o m ajor
r ysm s arising from th is segm en t .
ben ds an d t w o prom in en t ar terial bran ch es, w h ich create h em o-
dyn am ic st ress poin ts predisposing to an eur ysm form at ion . Th e
first ben d , seen best on lateral p roject ion an giogram s, is t h e
cur ve form ed by th e ascen ding ICA as it ben ds posteriorly after
■ Pertinent Anatomy and Terminology pen et rat ing th e DR. Th is ben d creates h em odyn am ic st resses
Osseous and Dural Relationships u pon th e dorsal w all of th e Oph Seg. Th e secon d ben d, m ore con -
spicuous on a dorsal view, is a gen tle lateral-to-m edial-to-lateral
Th e an terior clin oid p rocess (ACP) represen t s th e m ost m edial ben d as th e ICA ascen ds an d pen et rates th e DR m edial to th e ACP,
exten sion of th e lesser w ing of th e sph en oid bon e, form ing th e produ cing a h em odyn am ic st ress on th e m edial ICA w all w ith in
roof of th e su perior orbit al fissu re (SOF) an d an terior cavern ous th e Op h Seg.
sin u s. Th is bony p rom in en ce also st raddles th e an terior an d lat- Th e op h t h alm ic ar ter y (Op h Ar t ) t yp ically ar ises from t h e
eral border of th e ascen ding in tern al carot id ar ter y (ICA) as it d orsom edial surface of th e Oph Seg ju st beyon d th e DR, to ac-
exit s t h e cavern ou s sin u s, an d it s exten sive rem oval op en s access com pany the optic ner ve through the optic canal, providing blood
broadly to th is region . Th e opt ic st r ut exten ds bet w een th e in - su p ply to th e ret in a an d orbit . Th e su p erior hypop hyseal ar ter y
ferom edial surface of th e ACP an d body of th e sph en oid bon e an d (SupHypAr t) usu ally origin ates from th e m edial or in ferom edial
separates th e opt ic can al from th e con ten ts w ith in th e SOF. aspect of th e Oph Seg, as on e of several ar teries th at supply por-
Dura m ater covers th e ACP an d all oth er in t racran ial bony sur- t ion s of th e p it u itar y st alk an d glan d, cavern ou s sin u s du ra, an d
faces, an d u n derstan ding th e follow ing specific dural relat ion - opt ic apparat us. On occasion , eith er of th ese ar terial bran ch es
sh ip s is im p erat ive in effect ively dealing su rgically w ith lesion s can origin ate proxim al to th e Op h Seg, along th e clin oidal or cav-
in th is area: ern ou s ICA segm en ts.

1. Each cavern ous sin us is a dura-en cased ven ous space located
lateral to t h e sella t u rcica an d body of t h e sp h en oid bon e, Neural Relationships
exten ding from th e SOF an teriorly to th e m ed ial ap ex of th e
Th e oculom otor, trochlear, abducens, t rigem in al (first and second
p et rous bon e p osteriorly.
division s), an d sym p ath et ic n er ves are all in t im ately associated
2. Th e falciform dural ligam en t span s from th e ACP to th e t u ber-
w ith the cavernous sinus and its dura, below the plane of the ACP.
culum an d dorsum sella an d span s over th e posterior port ion
All of th ese n er ves even t ually t ravel from th e cavern ous sin us to
of th e opt ic n er ve after it leaves th e bony opt ic can al.
th eir resp ect ive orbit al t arget s, an d th ey u su ally rem ain u n af-
3. The dural ring (DR) represents an aperture in the sheet of dura
fected by OphSeg aneur ysm s because th ese lesions generally pro-
th at reflect s off th e su perior an d m edial ACP su rface to m erge
ject su periorly aw ay from th e superior orbital fissure an d lateral
m ed ially w it h t h e diap h ragm a sella an d opt ic can al du ral
cavern ou s sin u s w all. Th e opt ic n er ves, h ow ever, are directly in
floor. Th e DR rep resen t s t h e exact p oin t w h ere t h e ascen d -
line w ith the direction of aneurysm expansion, and are com m only
in g ICA en ters th e su barach n oid space. Th e DR h as an obliqu e
distor ted by an eu r ysm s arising from th e Oph Seg (Fig. 46.1).
slop e in t w o plan es, dow nw ard from an terior-to-p osterior
an d lateral-to-m edial, th u s form ing a sm all subarach n oid di-
ver t iculu m m edial to th e ICA term ed th e carot id cave.
4. The carotid-oculom otor m em brane (COM), form ed by the peri-
osteal dural reflect ion off th e in ferior ACP surface, exten ds
■ Aneurysm Types
from th e ocu lom otor n er ve laterally to th e ICA m edially, an d Th e vast m ajorit y of Op h Seg an eu r ysm s are saccu lar, as ou tlin ed
m arks t h e exit of t h e ascen d ing ICA from th e t r u e ven ou s by Rh oton ,1 an d gen erally form along ar terial cu r ves at th e jun c-
lu m en of th e cavern ou s sin u s. t ion bet w een th e paren t ar ter y an d a n am ed bran ch w ith in th e

538

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46 Surgical Therapies for Carotid-Ophthalm ic Aneurysm s 539
Fig. 46.1 Osseous, dural, vascular, and neural anatomy of
the ophthalm ic segm ent, lateral view. The anterior clinoid
(AC) has been removed; its superior dural covering m edially
form s the dural ring (DR); its inferior dura extends laterally as
the carotid-oculom otor m em brane (COM). The ophthalm ic
segm ent (OphSeg) is entirely subarachnoid, beginning at the
DR and ending at the origin of the posterior comm unicating
artery (PCoA). Two consistent internal carotid artery (ICA)
branches arise from this segm ent: the ophthalm ic artery
(OphArt) arises just beyond the DR and projects anterolater-
ally beneath and along with the optic nerve (ON) into the
orbit; and the superior hypophyseal arteries (SupHypArt) proj-
ect m edially from the OphSeg (independent of the OphArt)
to supply the ONs, chiasm , and pituitary gland.

segm en t , t yp ically p roject ing in th e direct ion flow w ou ld h ave t akeoff of t h e su p erior hyp op hyseal ar ter y.2–5 Th ese lesion s
gon e h ad th e paren t ar ter y n ot t u rn ed. Th ree an eur ysm sub - gen erally arise from th e in ferior-m edial surface of th e ICA,
t yp es arise from th e Oph Seg (Fig. 46.2): lateral to th e parasellar dura an d just beyon d t h e DR. Som e
bu r row in feriorly an d m ed ially tow ard an d below t h e d ia-
1. OphArt: Th ese an eu r ysm s h ave a clear associat ion w it h t h e
p h ragm a sella, exp an d in g t h e carot id cave, an d are h erein
op h th alm ic ar ter y. Th ese lesion s t yp ically arise along th e p os-
term ed p arasellar varian t s.6,7 Th is is th e m ost com m on t yp e
ter ior ben d of t h e ICA ju st d ist al to t h e Op h Ar t , ju st above
of Oph Seg an eu r ysm ; th e fu ndus of sm all lesion s is invested
t h e DR. Oph Ar t an eu r ysm s p roject dorsally or dorsom ed ially
by adjacen t du ra, an d it s risk of su barach n oid h em orrh age
tow ard th e lateral h alf of th e opt ic n er ve, often elevat ing th e
(SAH) is qu ite low . As t h ese lesion s en large, h ow ever, t h ey
n er ve superiorly an d m edially again st th e sh arp edge of th e
expan d superom edially into the suprasellar space, w here their
overlying falciform ligam en t .2–5
h em orrh age risk becom es greater. An oth er SupHypAr t an eu-
2. SupHypArt: Th ese an eur ysm s arise along th e gen tle lateral-
r ysm t yp e, th e su p rasellar varian t , origin ates w ith in a sh allow
to-m ed ial-to-lateral ICA ben d in close associat ion w it h t h e
carot id cave or m ore dist ally along th e ICA, an d do n ot bu rrow
in ferom edially even w h en sm all, bu t in stead p roject m edially
to expan d in to th e m edial suprasellar space w ith out invest-
m en t by th e parasellar du ra.
3. Dorsal variant: Th ese an eu r ysm s ar ise along t h e d orsal ICA
su r face clearly d ist al to an d u n associated w it h t h e op h t h al-
m ic ar ter y. Som e ap p ear to be p u re h em odyn am ically in -
du ced lesion s associated w it h an accen t u ated ben d or angu -
lat ion in th e arter y; m ost represen t dissect ion s often term ed
“blister an eu r ysm s” based on t h eir in it ial ap p earan ce after
h em orrh age.3,8,9

■ Clinical Presentation
Th e t yp ical Op h Seg an eu r ysm p at ien t is fem ale (80–90%p rep on -
deran ce), gen erally in h er fifth an d sixth d ecade of life (esp e-
cially if sym ptom at ic), an d h as an oth er an eu r ysm elsew h ere
(40–50%of pat ien ts h ave at least on e addit ion al lesion ). Most are
also sm all in ciden tal lesion s discovered du ring w orkup of oth er
lesion s or sym ptom s.
Pat ien t s w ith sym ptom at ic Oph Seg an eu r ysm s presen t w ith
visu al sym ptom s or SAH, in rough ly equ al proport ion s. Th ose
Fig. 46.2 Ophthalm ic segm ent aneurysm s schem atic, lateral view. Aneu- w ith visual sym ptom s alm ost alw ays h ave an eur ysm s th at h ave
rysm t ypes (hatched areas): 1, ophthalm ic artery; 2, superior hypophyseal reached very large or giant proportions (≥ 2.0 cm ), suggesting that
artery; 3, dorsal variant. con sid erable m ass effect m u st t ake p lace before visu al d eficit s

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540 V Cerebral and Spinal Aneurysms

occur an d are n oted by th e pat ien t .2,3,5 Th e larger size an d low er sylvian fissu re is n ot u n u su al.2,3,10 CT scan s provide im portan t
h em orrh age rate is likely at t ributable to th e rein forcem en t of in form at ion regarding th rom bus or calcificat ion w ith in th e an -
sm aller lesion s p rovided by n earby p arasellar d u ra or overlying eu r ysm n eck or fu n d u s or dem on st rable ACP or opt ic st r u t ero-
opt ic n er ve again st th e an eur ysm fu n du s. sion th at in d icates a m ore proxim al origin of th e lesion w ith in
th e clin oid segm en t (Clin Seg).
Th e an eu r ysm ’s an atom ic relat ion sh ip to soft t issu e st ru c-
Ophthalmic Artery Aneurysms t u res su ch as opt ic n er ves, ch iasm , an d p it u itar y glan d is m u ch
Most Oph Ar t an eu r ysm s en cou n ter th e overlying opt ic n er ve as m ore clearly defin ed w ith m agn et ic reson an ce im aging (MRI).
th ey en large, an d th is st r u ct u re effect ively cap s th e lesion an d Th is m odalit y is less u sefu l th an CT for delin eat ing bony an at-
som ew h at p rotect s th e an eu r ysm from ru pt u re. Op h Ar t an eu - om y, but it has a role as a screening tool in high-risk patient popu-
r ysm s often cause th eir field defects by elevat ing th e ipsilateral lat ion s, esp ecially pat ien ts w h o m igh t n eed serial exam in at ion s,
opt ic n er ve su periorly an d m edially in to th e sh arp edge of th e because n o radiat ion is required.14,15
falciform ligam en t , dam aging th e superior-lateral port ion of th e Four-vessel transfem oral cerebral arteriography is the preferred
n er ve. Th e result an t m on ocular in ferior-n asal field defect m ay m eth od for defin ing Oph Seg an eur ysm s in w h ich in ter ven t ion is
go un n ot iced by th e pat ien t un t il th e lesion en larges to gian t size, being con sidered. Mu lt iple project ion s an d th ree-dim en sion al
at w h ich t im e loss of th e en t ire ip silateral n asal field is eviden t , (3D) recon st r u ct ion s d efin e t h e an atom ic ch aracter ist ics of a
follow ed by a superior tem poral field loss in the con tralateral eye. p ar t icu lar lesion . Th e cer vical carot id ar ter y an d su p er ficial
tem porar y ar ter y sh ou ld be sim ult an eously evaluated to defin e
th e risks/p ossibilit ies of tem p orar y p roxim al ICA occlu sion an d
Superior Hypophyseal Artery Aneurysms bypass con siderat ion s. An aw ake balloon test occlusion w ith in -
Most Su p Hyp Ar t an eu r ysm s exp an d m edially to en cou n ter th e du ced hyp oten sion or cerebral blood flow st u dies (single ph oton
lateral sella w all d u ra an d bu r row in to t h e carot id cave, receiv- em ission CT or xen on CT) can be u sefu l p rior to t reat m en t of
in g substan t ial m ech an ical suppor t again st th e fun dus. On ce com plex lesion s th at m igh t requ ire p rolonged tem p orar y or p er-
th ese lesion s exten d in to th e su prasellar space, h ow ever, th is re- m an en t ICA occlu sion .
in forcem en t is lessen ed an d h em orrh age risks escalate. Because Th e Op h Ar t an eu r ysm s arise from th e dorsal or dorsom ed ial
th ese lesion s gen erally p roject m ore dist ally an d m edially along ICA su rface ju st dist al to th e Op h Ar t t akeoff (Fig. 46.3). Th e ex-
th e ICA, th eir su p rasellar expan sion ten ds to elevate an d com -
press th e opt ic ch iasm or t ract from below, m ore t ypically p ro-
ducing bilateral ch iasm al p at tern visu al deficit s.2,3,5

Dorsal Variant Aneurysms


Th ese u n com m on Oph Seg an eu r ysm s arise m ore dist ally along
th e d orsal ICA su rface as th e vessel app roach es th e PCoA, u n -
associated w ith any par t icular bran ch poin t .1,6,8,10 Many repre-
sen t dissect ion s th at cau se SAH, ap pearing as a sm all “blister” on
th e dorsal ICA su rface beyon d th e origin of t h e Op h Ar t . Many are
in terp reted as a n on specific focal spasm on th e origin al diagn os-
t ic angiogram , bu t over several days th e en t ire affected segm en t
dilates an d th e lesion becom es m ore obvious.11
A sm aller propor t ion of th ese are t r ue saccular an eu r ysm s as-
sociated w ith a m arked h em odyn am ic ben d of th e ar ter y from
m edial to lateral as it approach es th e com m un icat ing segm en t .
Occasion ally, th e th icken ed or ar teriosclerot ic an terior w alls of
large or gian t Op h Ar t an eu r ysm s create a radiograph ic gap be-
t w een th e an eur ysm origin an d th e Op h Art t akeoff on th e lateral
ar teriogram , m im icking a h em odyn am ically in duced dorsal vari-
an t lesion . Dorsal var ian t lesion s u n com m on ly p resen t w it h
sym ptom s related to visu al system com p ression becau se t h ey
arise m ore distal along th e ICA, lateral to th e visual system .12,13
Fig. 46.3 Ophthalmic segm ent aneurysm , ophthalm ic artery (OphArt)
t ype. Note the origin just beyond the OphArt, and the superior-m edial pro-
jection for exposure and clipping technique. The patient was a wom an in
■ Radiographic Evaluation her early 40s, who presented with acute right-sided headache. Neurologic
exam revealed dim inished visual acuit y in the right eye and a dense inferior
A rupt ured Oph Seg an eur ysm t ypically produ ces h em orrh age nasal field loss. The computed tom ography (CT) scan showed no evidence
w ith in th e ch iasm at ic an d p arasellar cistern s, occasion ally cau s- of subarachnoid hem orrhage (SAH). Arteriography dem onstrated an 8- to
9-m m ophthalm ic segm ent aneurysm projecting superiorly just beyond
ing a focal clot w ith in th e orbitofron tal gyri, fin dings th at are
the origin of the ophthalm ic artery; it was an ophthalm ic artery aneurysm .
best appreciated on com puted tom ography (CT). Becau se both The lesion was clipped, and visual acuit y markedly improved within 24 hours
Oph Ar t an d Su pHyp Ar t an eu r ysm t ypes often project m ed ially, of surgery; the inferior nasal field loss persisted. Postoperative arteriogra-
exten sion of th e su barach n oid bleeding in to t h e con t ralateral phy showed complete obliteration of the aneurysm .

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46 Surgical Therapies for Carotid-Ophthalm ic Aneurysm s 541

pan ding lesion elevates th e overlying opt ic n er ve su periorly an d


m edially, often produ cing a flat ten ing along th e su perom edial
an eur ysm surface, an d causing an in ferior deflect ion of th e ICA
w ith “closing” of th e carot id sip h on .
Th e Su p Hyp Ar t an eu r ysm s arise from th e in ferior or in fero-
m edial ICA surface an d project m edially tow ard th e sella (Fig.
46.4). Larger lesion s t ypically h ave broad n ecks th at en com pass
m uch of th e Oph Seg m edial ICA w all. As th e lesion expan ds, th e
ICA is often d eflected laterally an d su p er iorly, lead ing to an
“op en ing” of t h e carot id sip h on . Larger su p rasellar exten sion
en ables th e an eu r ysm to expan d su perom edially in to th e su pra-
sellar sp ace, u n in h ibited from crossing th e m idlin e by th e ip silat-
eral opt ic n er ve.
Dorsal variant carot id w all aneurysm s arise from the dorsal ICA
surface an d project su p eriorly, sim ilar to Oph Ar t an eur ysm s, bu t
the poin t of aneur ysm origin is distinctly distal (usually 2–4 m m )
from th e Op h Ar t t akeoff. W h en du e to a dissect ion , th is varian t
in it ially appears as a focal n arrow ing or m ild bulge, due to in t ra- Fig. 46.4 Ophthalmic segm ent aneurysm , superior hypophyseal artery
m ural h em orrh age or focal vasospasm , follow ed by progressive (SupHypArt) t ype. Note the inferior and m edial origin and projection lateral
en largem en t du e to th e w eaken ed ar terial w all (Fig. 46.5). to the sella, proxim al to the posterior com m unicating artery.

Fig. 46.5a,b (a) Ophthalm ic segm ent aneurysm, dorsal variant t ype. This 3 days. Note the fusiform shape of the dissected carotid artery in the oph-
patient presented with subarachnoid hem orrhage (SAH), and the initial thalm ic segm ent well beyond the ophthalmic artery (OphArt) origin on the
right internal carotid angiogram (left) and 3D reconstruction (right) show a arteriogram (left) and the 3D reconstruction (right). The focal “bleb” repre-
sm all irregularit y on the dorsal internal carotid artery (ICA) surface of the sents the site of hem orrhage from a thinned point in the dissection of the
ophthalmic segment (OphSeg). (b) Aneurysm enlargement occurred within dorsal carotid wall.

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542 V Cerebral and Spinal Aneurysms

tem poral ar ter y–m iddle cerebral ar ter y an astom osis or in terpo-
■ Indications for Treatment sit ion sap h en ou s vein graft is n eeded in on ly a ver y sm all n u m -
Su rgical clip p ing provides an effect ive t reat m en t w ith favorable ber of cases, an d sh ould gen erally be preclu ded by a balloon test
outcom es an d a low com plicat ion rate in experien ced h an ds.2,16 occlusion .27–30
In creasingly, h ow ever, en dovascu lar surger y h as provided m ore
opt ion s for som e of th ese ch allenging lesion s.17–20 W h ich lesion s
sh ou ld be t reated, an d by w h at m eth od, h as been qu ite con t ro-
versial. Con t r ibu t in g factors in t h e m an agem en t d ecision s re- ■ Operative Procedure
gard in g op h t h alm ic segm en t an eu r ysm s in clu d e t h e p resen ce
of SAH, th e size of th e an eu r ysm (sm all, large, or gian t), th e t ype Anesthesia and Neurophysiological Monitoring
(oph th alm ic, superior hypophyseal, dorsal variant), visual sys- Prophylactic antibiotics, intravenous steroids, m ild hypotherm ia,
tem com prom ise, an d pat ien t age. an in dw elling radial ar terial lin e for blood pressure m on itoring,
Several sit u at ion s an d scen arios are clearer th an oth ers. Ru p - an d con t in uous evoked poten t ial an d elect roen ceph alograph ic
t u red an eu r ysm s of th e Op h Seg sh ou ld alw ays be t reated. Al- (EEG) m on itoring are rou t in ely used du ring surger y for th ese le-
th ough m icrosu rger y an d en dovascu lar tech n iqu es are both ap - sion s. Wid e sylvian fissu re split t ing an d gen erou s cerebrospin al
plicable opt ion s, th e com plex an atom y an d risks associated w ith flu id (CSF) drain age from th e basal cistern s are ut ilized for brain
su rger y du ring th e vasospasm period h as prom oted en dovascu - relaxat ion . For ru pt ured an eu r ysm s, in t raven ous m an n itol ad-
lar opt ion s as p referable in m any in st an ces.17–20 Th e addit ion of m in istered 20 m in u tes prior to dural open ing, or a ven t riculos-
sten t ing to th e en dovascu lar t reat m en t gen erally requ ires clopi- tom y placed on th e con t ralateral side, is used to fur th er aid brain
dogrel, a riskier sit u at ion w h en th e SAH is recen t an d ven t ricu lar relaxat ion . Sp in al drain age gen erally is n ot em ployed for th ese
drain age is op eran t . lesion s. In cases w h ere tem p orar y region al circu lator y arrest is
Sm all u n r u pt u red parasellar Su pHyp Ar t an eur ysm s ap pear to em p loyed, m ild hyper ten sion is in du ced an d in t raven ou s barbi-
h ave a ver y low risk of bleeding, an d m any are often best t reated t u rates are t it rated to EEG bu rst su ppression .
con ser vat ively. Un r u pt u red an eu r ysm s larger t h an 5 m m , es-
p ecially t h ose t h at p roject freely in to t h e su barach n oid sp ace
(Oph Ar t , suprasellar SupHypAr t , dorsal varian t) sh ou ld be con - Patient Positioning
sidered for t reat m en t .21 En dovascular tech n iques are preferable
Th e p at ien t is placed sup in e u pon th e operat ing table w ith a roll
in older p at ien t s w ith h igh er su rgical risks, w h ereas surgical in -
placed ben eath th e ip silateral sh ou lder. A radiolu cen t rigid fixa-
ter ven t ion is recom m ended for you nger h ealthy pat ien ts w ith a
t ion system is secu red to t h e h ead , allow in g in t raop erat ive an -
life expect an cy > 10 years,22 p ar t icu larly w ith Op h Ar t an eu r ysm s
giograp hy as n eed ed. Th e h ead is t urn ed 45 degrees tow ard th e
in w h om sim p le coiling alon e often does n ot cu re th e lesion .
con t ralateral side an d elevated above th e h ear t to p rom ote ve-
Su rger y is p referable for large an d gian t lesion s p resen t ing
n ous drain age. Th e ver tex is low ered below th e m axilla to allow
w ith visual loss, as th e visu al system can be im m ediately decom -
gen tle gravitat ion al ret ract ion of th e fron tal an d tem poral lobes.
p ressed an d d eficit s rap idly reversed .23 Sku ll base ap p roach es,
as outlin ed below an d in cluding broad rem oval of th e ACP an d
open ing of th e DR, m ust be applied to get effect ive result s w ith Cervical Internal Carotid Artery Exposure
low m orbidit y. In Day’s 2 origin al series, 17 of 23 Oph Seg an eu-
r ysm pat ien ts presen t ing w ith visual deficit im proved after clip - Th e region overlying t h e ip silateral carot id bifu rcat ion is m arked,
ping an d decom pression . Th ree p at ien t s w ith ou t docu m en ted prep ped, an d drap ed in to th e sterile field in all cases. Cer vical
preop erat ive visu al deficits h ad dim in ish ed visu al acu it y after exp osu re is often n ot don e for sim p le or larger u n ru pt u red cases,
su rger y. Kat t n er et al24 rep or ted a series of 29 p at ien ts t reated bu t is alm ost alw ays d on e for gian t , com p licated , or r u pt u red
su rgically for gian t op h th alm ic an eu r ysm s. Five p at ien ts h ad im - Clin Seg an eur ysm s.
proved vision postop erat ively, fou r h ad n o ch ange, an d in on e it Exp osu re is obt ain ed as h igh as p ossible along th e ICA, so th at
w orsen ed. Heros et al25 review ed 34 cases of gian t an d large oph - if clam ping is n ecessar y, any ath erom a n ear th e bifu rcat ion w ill
th alm ic segm en t an eu r ysm , n ot ing th at t h e vision w as im p roved be un dist urbed. Proxim al con t rol en ables ret rograde suct ion de-
in 10, w orse in fou r, an d u n ch anged in t w o of 18 pat ien ts pre- com pression or a site for bypass graft ing as n eeded.
sen t ing w ith preoperative visu al loss; th e rem ain ing t w o died.
Most recen tly Deh dash t i et al23 presen ted a series of 38 gian t
Scalp Flap and Craniotomy
an d large an eu r ysm t reated surgically; of th e 12 pat ien t s w ith
docu m en ted p reop erat ive visu al d eficit s, n in e (75%) h ad im - Th e scalp in cision exten ds beh in d th e h airlin e from th e m idlin e
proved vision p ostoperat ively, t w o (16%) rem ain ed st able, an d to th e zygom a, sparing th e superficial tem poral ar ter y th at m ay
on e (8%) w orsen ed. Man agem en t w ith coil packing of th e an eu- be n eeded later as a bypass con duit . An in terfascial tem poralis
r ysm m ay act ually w orsen th e m ass effect on th e visual system .18 m uscle flap is perform ed, reflect ing th e tem poralis m u scle aw ay
Persisten t m ass effect w ith out decom p ression h as a redu ced from th e orbit al rim .31 An orbitofron tal osteotom y is n ot rou-
ch an ce of deficit reversal, as w ith PCoA an eu r ysm s an d ocu lom o- t in ely requ ired for m ost lesion s. A fron totem poral free bon e flap
tor palsies.26 is th en elevated, w ith at least 2 cm of fron t al fossa floor exposed.
W h en su rger y is p erform ed, direct an eu r ysm clipp ing is th e Th e lesser w ing of th e sp h en oid bon e is rem oved ext radu rally
m ost st raigh tfor w ard m eth od, w ith or w ith out p roxim al con t rol dow n to th e base of th e ACP, along w ith th e p osterior orbital roof,
obtain ed in th e cer vical ICA region . In direct surger y to proxi- orbit al lateral w all, an d su perior aspect of th e greater sph en oid
m ally ligate or t rap th e an eur ysm w ith or w ith out a superficial w in g below t h e su p er ior orbit al fissu re. Th is bon e is rem oved

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46 Surgical Therapies for Carotid-Ophthalm ic Aneurysm s 543

Fig. 46.6 The bony resection for ophthalmic segment (OphSeg) aneu-
rysm surgery. The extradural bone rem oval includes the frontotemporal
craniotomy (hatched area 1) and the sphenoid ridge, posterior orbital roof,
and medial floor of the superior orbital fissure (hatched area 2). The rem ain- Fig. 46.7 The dural incisions for intradural anterior clinoid process (ACP)
ing m edial sphenoid wing and anterior clinoid process (area 3) rem oval is rem oval. The dashed lines along the m edial sphenoid wing and anterior cli-
generally perform ed intradurally to reduce the risk of intraoperative aneu- noid rem nant represent the dural incision. An extension of this incision is
rysm rupture. carried through the falciform ligam ent and lateral optic nerve ensheath-
m ent to decompress and m obilize the optic nerve (ON).

regardless of w h eth er ACP rem oval is plan n ed on ce th e dura is


open ed an d th e lesion exp osed (Fig. 46.6). d issect ion s, h ow ever, in t rad u ral clin oid rem oval u su ally p ro -
vid es t h e n ecessar y p roxim al exp osu re for tem p orar y p roxim al
con t rol as p ar t of t rap p in g of t h e Op h Seg p r ior to clip re-
Anterior Clinoid Process Removal con st r u ct ion .
We p refer an in t rad u ral clin oid rem oval for all large, com p lex,
or rupt u red Oph Seg an eur ysm s.2 Th e proxim it y of m ost paracli- Temporary Clipping and
n oid an eur ysm s to th e ACP, par ticularly th ose arising proxim al
Aneurysm Decompression
to th e DR, m akes ext radu ral ACP rem oval m ore h azardous.32
W h en th e ACP is rem oved ext radu rally, th e p osterior h alf of Wide split t ing of th e sylvian fissu re from lateral to m edial is u t i-
th e roof an d lateral w all of th e orbit an d th e sph en oid ridge cov- lized in all cases to facilitate exp osu re an d clip p lacem en t w ith -
ering th e SOF are resected u n t il th e orbit al p or t ion of th e opt ic out un due brain ret ract ion . All tem porar y clipping or t rapping
nerve is clearly iden tified. The ACP is then internally th inn ed w ith p roced u res, w h et h er su rgical or en d ovascu lar, are p er for m ed
a high -speed diam on d drill, an d th e rem ain ing th in rem n an t s of u n d er barbit u rate-in d u ced EEG su p p ression an d m ild hyp er-
th e ACP are carefu lly rem oved w ith sm all rongeu rs. Bleeding is ten sion . Com plex or gian t paraclin oid an eur ysm s often requ ire
easily con t rolled w ith bon e w ax an d Gelfoam (Pfizer, New York). lesion decom p ression to en able th e su rgeon to clearly iden t ify all
W h en th e ACP is rem oved in t radu rally (Fig. 46.7), a 3- to 4-cm aspect s of th e an eur ysm n eck, n earby perforators, an d th e visual
longit udin al dural in cision is th en m ad e from th e ACP t ip to w ell system . Tem p orar y cer vical ICA ligat ion often relaxes th e an eu -
beyon d th e resected edge of th e m edial sph en oid ridge. An ad- r ysm en ough to en able clipping w ith out t rapping in m any cases.
dit ion al rela xing in cision is m ade th rough th e falciform ligam en t Altern at ively, a p roxim al tem porar y clip can be applied to th e
to decom press th e opt ic n er ve. Th e ACP an d th e opt ic can al roof exposed Clin Seg, alth ough a m ild ptosis an d m iosis often result .
and lateral w all are thinn ed w ith a high -speed diam ond drill, and W h en t rap p ing is requ ired , t h e d ist al clip is p laced across
th e rem ain ing bony sh ell is carefu lly rem oved w ith sm all ron - t h e ICA p roxim al to th e PCoA if p ossible, to keep as m u ch blood
geu rs. Fin ally, th e opt ic st ru t is drilled dow n to expose th e an te- flow ing in to th e h em isph ere th rough th e circle of Willis as pos-
rior border of th e Clin Seg. sible. Ret rograde cer vical ICA su ct ion decom pression tech n iqu es
Dorsal var ian t ICA an eu r ysm s, w h en saccu lar, often d o n ot or direct an eur ysm pun ct ure can be added to prom ote fu r th er
requ ire ACP rem oval for effect ive visu alizat ion an d clip p in g. For an eur ysm collapse.33–37

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544 V Cerebral and Spinal Aneurysms

Fig. 46.8 Exposure following intradural anterior clinoid process (ACP) re-
m oval and optic strut (OS) drilling. The dashed line represents the dural
incision along the subarachnoid space surrounding the optic nerve within
the optic canal. The optic nerve is then m arkedly decompressed and mo-
bile; a stitch is placed at the intracranial end of the opening of the optic
canal dura, and retracted in the direction of the arrow to allow a completely Fig. 46.9 Clipping a superior hypothyseal artery (SupHypArt) aneurysm .
open view of the dural ring and the ophthalmic artery (OphArt) origin. The internal carotid artery (ICA) lum en is reconstructed with right-angled
fenestrated clips proceeding to but sparing the posterior comm unicating
artery origin and any other ICA perforators. Atherom a in these lesions
tends to occur inferiorly and m edially, and this proxim al region is often best
reconstructed with stacked short straight fenestrated clips that carefully
Aneurysm Dissection and Clipping spare the origins of the superior hypophyseal vessels.
For Oph Ar t an eu r ysm s, th e falciform ligam en t is sect ion ed an d
th e cu t exten ded along th e lateral aspect of th e opt ic n er ve to
provide exposure to th e jun ct ion of the proxim al n eck and Op h Ar t
(Fig. 46.8). Th e dist al n eck is u su ally easily iden t ified an d t yp i-
th rom bu s an d calcificat ion rem oved, an d th e an eu r ysm fu r th er
cally free of p erforators, an d a gen t ly cu r ved or side-angled clip
collapsed, enabling adjacent neural structures to be decom pressed.
placed just distal to the OphArt origin an d directed parallel to the
plan e of th e ICA obliterates m ost lesion s. Fen est rated clip s m ay
be u sed w h en ever sign ifican t ath erom a is en coun tered, w h ich
for th is lesion t ype is usually iden t ified on th e an terior surface of
th e an eu r ysm . Dorsal carot id w all an eu r ysm s are clipp ed in a
■ Closure
sim ilar fash ion , w ith easier iden t ificat ion of th e proxim al n eck. Th e risk of im p erfect clip applicat ion an d result ing paren t vessel
Th e m ost difficu lt part of th e dissect ion for Su pHyp Ar t an eu - lu m en com p rom ise or residu al an eu r ysm n eck, esp ecially w h en
r ysm s is in ferior an d m edial, w h ere th e an eur ysm w all is den sely at h erosclerot ic p laqu e or calcificat ion is en cou n tered w it h in
adh eren t to th e parasellar dura an d th e an eu r ysm w all often t h e an eu r ysm n eck or ICA w all, m an d ates t h e availabilit y of in -
t h icken ed . Circu m feren t ial sect ion in g of t h e DR, esp ecially m e- t raop erat ive ar ter iograp hy.38,39 In d ocyan in e green an giograp hy
d ially ben eath th e Oph Art origin , provides a clear view of th e inject ion u sed in coord in at ion is ver y effect ive in d em on st rat -
an eu r ysm n eck, an d aid s in t h e p reser vat ion of p er forators to in g p er forator paten cy.
t h e visu al system . Dist ally th e ICA lu m en is recon st r u cted w ith On ce opt im al clip p lacem en t is en su red , t h e sku ll base is
right-angled fenestrated clips proceeding to but sparing the PCoA in spected for p oin ts of p oten t ial CSF leak. Any com m u n icat ion s
origin an d any oth er ICA perforators. Ath erom a in th ese lesion s are sealed w ith m uscle, Gelfoam , an d m ethyl m eth acr ylate. Th e
ten ds to occur in feriorly an d m edially, an d th is proxim al region du ral leaflets overlying th e form er posit ion of th e ACP are loosely
is often best recon st r u cted w ith st acked sh or t st raigh t fen es- closed w it h in ter r u pted su t u res, carefu lly avoid in g any com -
t rated clip s t h at carefu lly sp are t h e or igin s of t h e su p er ior hy- p ression on th e exposed opt ic ner ve. After th e su perficial dura is
pop hyseal vessels (Fig. 46.9). closed, th e bon e flap is secu red w ith t it an iu m fixat ion devices,
If th e ICA lum en is com prom ised, a secon d clip is placed dist al an d any residual bony defects are corrected w ith m ethyl m eth -
to th e first , an d a th ird clip added, allow ing th e origin al clip to be acr ylate. Th e tem poralis m u scle is reapproxim ated an d a subga-
rem oved; th is process is rep eated u n t il w ide carot id paten cy is leal drain is p laced before th e skin is closed an d a sterile ban dage
en su red. On ce clip p ed, th e an eu r ysm is op en ed, in t ralu m in al applied.

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46 Surgical Therapies for Carotid-Ophthalm ic Aneurysm s 545

gen tle an d m et iculous operat ive tech n ique, an d are for t un ately
■ Postoperative Care u su ally t ran sien t .
Any postoperat ive eviden ce of n ew an d un expected h em ibody
n eu rologic d eficit s sh ou ld be em ergen t ly ad d ressed w it h angi-
ography or a ret urn to th e operat ing room for em ergen t reex-
ploration and clip adjustm ent. Visual deterioration (either im m e-
diate or delayed) is usually at tributable to perforator com p rom ise.
■ Conclusion
Reexp lorat ion an d clip adju st m en t sh ou ld be en ter tain ed on ly if Alth ough m any oph th alm ic segm en t an eur ysm s can be t reated
in t raoperat ive even ts do n ot adequ ately explain a postoperat ive via endovascular techniques, m astery of the anatom y and of skull
visu al deficit . Oth er cran ial n er ve deficits, in clu ding oculom otor, base approach es to th ese lesion s is essen t ial for n eurovascular
sym path et ic, t roch lear, or abdu cen s p alsies, are gen erally th e re- su rgeon s. Th e dorsal ICA an eu r ysm s rep resen t a rare bu t ch al-
sult of su rgical t raum a du ring an terior clin oidectom y, clip blade lenging su bset of an eu r ysm s th at m ay requ ire advan ced m icro-
advan cem en t , excessive cran ial n er ve m an ipulat ion , or overzeal- su rgical tech n iqu es, in clu ding h igh -flow bypass or clip w rapp ing
ous cavern ou s sin us packing. Th ese deficits are best avoided by for effect ive t reat m en t.

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33. Batjer HH, Sam son DS. Ret rograde su ct ion decom pression of gian t para- 37. Arn autović KI, Al-Meft y O, Angt u aco E. A com bin ed m icrosu rgical sku ll-
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of paraclin oid an eur ysm —a revised tech n ique. Surg Neurol 1999;51:129– 38. Rauzzino MJ, Quin n CM, Fish er WS III. Angiography after an eur ysm sur-
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grade suction decom pression. Acta Neurochir (Wien) 1997;139:1026–1032

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47 Endovascular Treatment of
Carotid-Ophthalmic Aneurysms
Rosa Mart inez, Marta Aguilar Perez, Nikolai J. Hopf, Hansjörg Bäzner, and Hans Henkes

Desp ite a large body of literat u re, th e ideal t reat m en t for p at ien t s level, as Drake et al1 described in a detailed an atom ic st udy. Apart
w ith in t racran ial an eur ysm s rem ain s con t roversial. Par t of th e from local bone st ruct ures, there is a com plex of connective t issue
challenge associated w ith iden tifying an ideal treatm ent regim en w ith areas of st rong con den sed st ran ds, also called “ligam en ts,”
is th e difficult y in design ing a d efin it ive prosp ect ive ran dom ized w h ich in flu en ce t h e p roject ion of th e longit u d in al a xis of t h e
t rial. As a resu lt , th e debate abou t th e ideal m an agem en t of cere- an eur ysm fun dus in th is segm en t , depen ding on th e site from
bral an eu r ysm s rem ain s divided bet w een th e cam p favoring m i- w h ich th ese an eur ysm s em erge.
crosu rgical clipping an d th e on e favoring en dovascular em boli- Th e an terior clin oid p rocess laterally lim it s th e du ral t ran si-
zat ion . Th e debate is probably n ow h ere m ore vibran t th an about t ion area of th e ICA, w ith con siderable in dividu al variat ion th at
th e ideal t reat m en t for an eu r ysm s at th e p araop h th alm ic seg- can in flu en ce th e su rgical tech n iqu e. Medial to th e an terior si-
m en t of th e in tern al carot id arter y (ICA). Th e paraoph th alm ic ph on kn ee is th e corpu s of th e sp h en oid bon e. Th ree ligam en t s
segm en t is p ar t icu larly com p lex becau se of it s an atom ic feat u res originate from the anterior clinoid process: (1) the anterior petro-
an d th e special n at ural h istor y of an eur ysm s at th is locat ion . clin oid fold, an anterior extension of the superior m argin of the
Th is ch apter p rovid es an over view of t h e an atom y of t h e ten torium ; (2) th e ligam en t th at con n ect s an terior an d m edial
p araoph th alm ic ICA an d an eur ysm s along th is por t ion of th e clin oid processes over t h e dorsal ICA; an d (3) th e in terclin oid
ICA. We review th e in ciden ce an d evolu t ion of t reat m en t ap - ligam en t th at con n ect s an terior an d posterior clin oid p rocesses.
proach es, w ith p ar t icu lar em p h asis on th e n ew er en dovascu lar Th ese last t w o ligam en t s can be calcified, form ing th e so-called
approach es. carot id-clin oid can al an d th e in terclin oid bridge.5
Apar t from th is an terior clin oid process, t w o dural rings (su -
perior an d in ferior) h ave been defin ed th at lim it th e p araclin oid
segm en t of th e ICA. Th e in ferior ring form s th e roof of th e cav-
■ Demographic Data ern ou s sin u s, an d is con t in u ou s w ith th e du ra covering th e in -
ferolateral par t of th e an terior clin oid process. Th e in ferior ring
According to several publish ed series, th e in ciden ce of carot id-
m ay be functionally incom petent. Consequently, in a variable pro-
oph th alm ic an eur ysm s ranges bet w een 5% an d 20% of all an eu-
port ion of cases, ven ou s elem en t s can be seen h ern iat ing from
r ysm s.1–4 An in creased frequen cy of large an d gian t an eur ysm s
th e cavern ou s sin u s. Th e su p erior ring covers th e opt ic n er ve,
h as been d escr ibed w it h in t h is segm en t . Th ere ap p ears to be an
con t in u es w ith th e falciform ligam en t m edially, an d is con t in u -
over w h elm in g p red om in an ce in fem ales, w it h a fem ale/m ale
ou s w ith th e extern al layer of th e ICA in a w ay th at severely h in -
rat io of 5:1 in m ost of t h e review ed ser ies.1–4 Th ere also seem s
ders it s su rgical d issect ion . Th is su perior ring h as a redu n dan t
to be an associat ive ten den cy for m ultiplicit y. Th e m ean age of
form at ion in it s m edial aspect th at is also kn ow n as th e “carot id
pat ien ts at presen t at ion is 50 years.
cave.”6 Kobayash i et al6 described th e lateral w all of t h e ICA as
th e “clin oid sp ace,” con sid ering it a n on cavern ou s an d n on in t ra-
du ral segm en t .
According to th e series by De Jesú s et al2 an d th e classificat ion
■ Anatomy of Bouth illier et al,7 th ere w as an agreem en t to defin e th e “op h -
Th e an atom ic st ru ct u res w ith in th e p roxim it y of th e op h th alm ic th alm ic segm en t” of th e ICA (C6) as exten ding from th e su perior
segm en t of th e ICA are qu ite com p lex. Th is m ay h elp to explain du ral ring to th e origin of th e p osterior com m u n icat ing ar ter y
th e ch allenges associated w ith th e diagn osis an d t reat m en t of (PCoA). Th e “clinoid segm en t” (C5) w as defin ed as th e segm en t
path ologies at th is segm en t of th e ICA. Th ere is a close an atom ic th at lies bet w een th e t w o du ral rings. Th e clin oid segm en t bears
relat ion sh ip bet w een th is vessel segm en t an d th e opt ic n er ve, n o bran ch es, an d thu s an eur ysm s in th is locat ion are n ot associ-
w h ich com es in con t act w ith th e paraclin oid ICA superom edially ated w ith bran ch es.
an d w ith cran ial n er ves III, IV, an d VI as w ell as w ith th e first di- Several classificat ion s h ave been proposed for an eu r ysm s in
vision of cran ial n er ve V. th e paraoph th alm ic segm en t of t h e ICA. Th e classificat ion by
Moreover, th e oph t h alm ic segm en t of th e ICA lies in th e t ran - Ogilvy w as ch osen as our stan dard d ue to it s w ide use in several
sit ion al area bet w een th e su barach n oid an d th e ext radu ral sp ace, series in th e literat ure.8 Ogilvy classified an eu r ysm s associated
an d t h is segm en t h as in t im ate con t act w it h t h e d u ra, t h e cav- w ith th e paraoph th alm ic segm en t of th e ICA in to th e follow ing
er n ou s sin u s, an d th e clin oid process of th e sph en oid bon e. Th e t ypes:
basal cran ial dura is n ot a sim ple border bet w een th e in t racran ial
por t ion of th e ICA an d it s in t racavern ou s p or t ion . Th e ICA is n ot • Transit ional aneurysm s origin ate in th e cavern ou s sin u s, bu t
su rrou n ded by th e cavern ou s sin u s im m ed iately below th e du ral exten d in to th e subarach n oid space.

547

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548 V Cerebral and Spinal Aneurysms

• Carotid-cave aneurysm s or m edial-clinoid aneurysm s are located lim it at ion s. In gen eral, a com p arison bet w een en dovascular an d
on angiography m edial to th e an terior ben d of th e ICA, an d are m icrosurgical resu lt s is ch allenging an d con t roversial.
best seen in an teroposterior an d oblique view s; th ese an eu- In 2005, the International Subarach noid Aneur ysm Trial (ISAT)
r ysm s project an d ru pt u re in to th e su barach n oid space. reported a redu ct ion of 7.4% in th e absolute risk (22.6% relat ive
• Ophthalm ic-artery aneurysm s arise at th e origin or ju st dist al risk) associated w ith en dovascu lar t reat m en t of r u pt u red an eu -
to th e origin of th e oph th alm ic ar ter y. r ysm s.3 Th e ISAT results h ave been w idely scrut in ized. Th e in it ial
• Posterior carot id-w all aneurysm s originate distal to th e ophth al- resu lt s of t h e st u dy rep or ted a sh or t follow -u p of on ly 1 year.
m ic ar ter y on t h e p osterior or p osterolateral w all, project ing Th is is too sh ort a p eriod to accou n t for an eu r ysm recan alizat ion ,
posterior-in feriorly. regrow th , or de n ovo an eu r ysm form at ion .10 Despite th e sh or t-
• Superior hypophyseal aneurysm s origin ate from th e m edial or com ings of th is st u dy, th e Am erican Societ y of In ter ven t ion al
in ferior-m edial w all of th e ICA, w ith th e part icipat ion of hy- an d Th erapeut ic Neuroradiology an d th e Am erican Societ y of
pop hyseal perforat ing bran ch es. Neu roradiology 11 h ave in terpreted th e ISAT resu lt s to suppor t
th e u se of en dovascu lar th erapy for ru pt u red an eu r ysm s as a
first-lin e t reat m ent .
Th e first en d ovascu lar t reat m en t w it h su fficien t safet y an d
efficacy w as in t rasaccu lar coil occlu sion w it h t h e Guglielm i De-
■ Clinical Presentation tach able Coil (GDC) (Target Th erapeut ics, Freem on t , CA), devel-
Th e m ost com m on clin ical p resen t at ion for pat ien t s w ith para- oped by Guglielm i et al.12,13 Th ese coils w ere m ade of soft p lat i-
oph th alm ic an eur ysm s is subarach n oid h em orrh age (SAH) ac- n um spirals an d w ere used to fill as m uch of th e an eu r ysm sac
cording to available literat u re.2 How ever, SAH is n oted in on ly volum e as possible (Fig. 47.1).
about a quar ter of all pat ien ts w ith an eur ysm s at th is locat ion .2 Th e m ajor ach ievem en t w ith th is advan ce in t reat m en t w as
Th e frequ en cy of SAH seem s to be low er in p at ien t s w ith para- t h e con t rolled d et ach m en t of t h e coil from t h e in ser t ion w ire
oph th alm ic an eur ysm s com pared w ith oth er an eur ysm localiza- u sin g elect rolyt ic d egrad at ion of a m et allic zon e. Th e elect ro -
t ion s,5 p robably d u e to th e an atom ic rest rict ion by th e du ra, th e t h rom bosis, w h ich w as in it ially in ten d ed to be in d u ced by a
lateral w all of th e sella, th e cavern ou s sin u s roof, an d th e opt ic d irect cu rren t , t urn ed ou t to h ave n o effect on th e m edical fu n c-
ch iasm in som e cases. t ion of coil occlu sion . Coils, n o m at ter h ow th ey are detach ed,
Other com m on clinical presentations include optic-nerve com - in terrupt th e blood circu lat ion in th e an eu r ysm sac an d in duce
pression w ith m ild-to-severe visu al ch anges (15%), severe h ead- th rom bu s form at ion bet w een th e coil loops. Th is even t u ally
ach e (20%), st roke or in t racran ial h em orrh age n ot related to th e leads to a fibrot ic p rocess th at prom otes h ealing at th e level of
an eur ysm (13%), an d u n related sym ptom s (13%) su ch as ver t igo th e an eu r ysm n eck an d th ereby exclu des th e an eu r ysm from th e
or dizzin ess. Visu al ch anges due to opt ic n er ve com pression are blood flow. Th is process preven ts un ru pt ured an eur ysm s from
m ore frequen t in oph th alm ic an d superior hypophyseal an eu - grow ing an d ru pt u ring an d reliably protect s again st rebleeding
r ysm s an d are in fluen ced by th e locat ion , orien t at ion , an d size in previou sly rupt ured an eur ysm s.
of the aneur ysm .2 A rare clinical presen tation is oculom otor palsy During th e past t w o decades, a large variet y of m odificat ion s
du e to cran ial n er ve com pression .2 A p ossible presen t at ion w ith of th e origin al coil h ave been developed. Com m on m odificat ion s
hypopit uitarism due to m ass effect on th e adjacen t pit uitar y that are w idely used include th ree-dim ensional coils, coils of vari-
glan d an d hypoth alam u s h as also been described.9 ous soft n ess grades, an d bioact ive coils th at prom ote h ealing of
th e en doth elial surface of the an eu r ysm .
The m ain issue w ith coiling is its lim itation in com plex-shaped
an eur ysm s, especially in th ose w ith w ide n ecks (> 4 m m ); w h en
u sed in th ese an eur ysm s, th e spirals ten d to prot r ude in to th e
■ Endovascular Treatment paren t vessel. To avoid th is problem , balloon -assisted coiling,
An expan ding array of en dovascu lar t reat m en t opt ion s en ables also called “balloon rem odeling,” an d sten t-assisted coiling tech -
clin ician s to t reat m any kin ds of an eu r ysm s, w ith few tech n ical n iqu es h ave been developed.

a b c

Fig. 47.1a–c Coil occlusion of an unruptured paraophthalm ic aneurysm . Lateral digital subtraction angiogram (DSA) views before (a), during (b), and
after (c) the procedure.

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47 Endovascular Treatment of Carotid-Ophthalmic Aneurysm s 549

Unassisted Coil Occlusion sized t h at t h e h em odyn am ic w all-sh ear st ress is h igh in t h e re-
gion of th e carot id siph on . W h en th e an eur ysm ’s spat ial con figu-
Th e u se of coil occlu sion in carot id-oph th alm ic an eu r ysm s h as
rat ion allow s it , th e w ater-h am m er effect of blood flow again st
been w idely discu ssed in several p u blicat ion s.
th e coil loop s com p act s t h e coil m ass an d d isp laces it in to t h e
In 1996, Gu r ian et al14 st u d ied a ser ies of 11 su p er ior hy-
aneurysm al fundus. Furtherm ore, the m icrocatheter tends to pre-
p op hyseal an eur ysm s, both r upt ured an d un r upt ured, th at w ere
m at u rely back ou t of th e an eu r ysm d u ring coil in ser t ion becau se
t reated w ith GDC coils. Th e au th ors focu sed th eir at ten t ion on
of th e com plex cur ve of th e cavern ous an d oph th alm ic ICA.
th is an atom ic region because of th e p resen ce of p erforat ing ves-
Th ese obser vat ion s p ar t ially explain th e h igh rates of an eu r ysm
sels th at supp ly th e p it u itar y glan d an d th e opt ic ch iasm . Micro-
recan alizat ion at th is segm en t of th e ICA. Th e literat ure cites re-
su rgical m an ip u lat ion of th ese p erforators can resu lt in visu al
can alizat ion rates bet w een 32%8 an d 83%17 for coil-occluded an -
sym ptom s or hyp op it u itarism , w h ich h ave been repor ted in u p
eu r ysm s. In a m u lt ivariate ret rosp ect ive series, Sorim ach i et al18
to 10%of cases in on e series.4 Coil occlusion w as tech n ically suc-
fou n d t w o m ain predictors for fut ure recan alizat ion of coiled
cessfu l in 10 of th e 11 an eu r ysm s, an d n in e p at ien t s h ad good
paraclin oid an eu r ysm s: th e m axim u m diam eter of an eu r ysm s
or excellen t clin ical results. No m orbidit y or m or t alit y w as di-
(w ith a 75% recan alizat ion rate in an eu r ysm s > 10 m m ) an d an
rectly at t ribu table to th e tech n iqu e. On e pat ien t h ad a poor clin i-
u n favorable dom e/n eck rat io (> 50%ten d to sh ow h igh er rates of
cal ou tcom e du e to severe SAH an d m u lt ip le in farct s related to
recan alizat ion ). Th e problem of recan alizat ion can be par t ially
vasospasm .14
addressed by balloon rem odeling of th e an eur ysm to obtain bet-
Roy et al15 evaluated GDC coil em bolizat ion of 28 an eur ysm s
ter packing den sit y w ith in th e an eu r ysm sac. Du ring balloon re-
of th e carot id-oph th alm ic segm en t in 26 pat ien ts. An atom ic re-
m odeling, th e balloon n ot on ly p reven ts coil loop prot r usion but
su lts w ere satisfactor y in 25 (89%) of th e 28 an eu r ysm s, in clu d-
also fixes th e m icrocath eter in a p roper posit ion (Fig. 47.2).
ing com p lete occlu sion (14 cases), n ear-com plete occlusion (10
Balloon -assisted coilin g, also called t h e “rem od elin g tech -
cases), an d on e “dog ear” residu al filling. Resu lt s w ere in flu en ced
n iqu e,” w as described by Moret et al19 in 1997. It w as proposed
by pat ien t age an d an eur ysm size. On ly 36% of large an eur ysm s
as an adjun ct to coil occlusion for w ide-n ecked side-w all an eu-
w ere com pletely occlu ded. Size of th e an eur ysm n eck w as an -
r ysm s to avoid bulging of th e coil loops in to th e paren t vessel.
oth er im port an t factor; in on ly 9% of w ide-n ecked an eur ysm s
Th e rate of tot al occlu sion in w id e-n ecked an eu r ysm s reach ed
w as an opt im al an atom ic resu lt obt ain ed after coil occlu sion . For
61% in cases p er form ed by Moret ’s grou p bet w een 1992 an d
an eur ysm s of th e oph th alm ic segm en t , a rate of on ly 21% com -
1996.
plete occlu sion after coil t reat m en t w as ach ieved . Rem arkable
Sin ce th e in t rodu ct ion of th e tech n iqu e, balloon rem odeling
com plications w ere throm boem bolic events in t w o patients w ith-
h as becom e a w idely used tech n iqu e. Several com pan ies devel-
out clin ical sequelae, an d displacem en t of a coil loop in to th e ICA
oped dedicated com plian t balloon s (e.g., Copern ic an d Eclipse,
lu m en . If com p ared w ith su rgical t reat m en t , th e an atom ic resu lt
Balt Extrusion, Montm orency, Fran ce; Hyperform and Hyperglide,
is sligh tly w orse, w ith a low er rate of com p lete occlu sion .
ev3/Covidien, Plym outh, MN; Ascend, Micrus/Codm an, Raynham ,
Boet et al,16 in t h eir lon g-ter m review of p at ien t s w it h 21
MA). Balloon rem odeling h elps to m old t h e coils to create a
p araop h t h alm ic an eu r ysm s w it h a 7-year follow -u p , fou n d a
sm ooth er an d den ser in terface w ith th e paren t vessel, an d h elp s
recu r ren ce rate of 53% in t h e an eu r ysm s t reated w it h sim p le
to in crease th e den sit y of coil packing. Th e tem porar y in flat ion
coiling.
of a com plian t balloon requires som e experien ce. ICA dissect ion ,
dist al em boli, an d coil-loop prolapse after balloon deflat ion are
kn ow n risks of th is tech n ique. After balloon -assisted coil occlu-
Balloon-Remodeling for Coil Occlusion sion , an t icoagu lat ion is n ot requ ired.
Reduced packing den sit y associated w ith un assisted coiling m ay Several reports in the literature describe the use of the balloon-
be a con sequen ce of h em odyn am ic factors an d th e m orph ology rem odeling tech n ique for t reat ing p at ien t s w ith paraoph t h alm ic
of th e ICA in th e paraoph th alm ic segm en t . It h as been hypoth e- ICA an eu r ysm s.9,20,21 A series of 66 pat ien t s w ith 71 an eur ysm s

a b c

Fig. 47.2a–c Balloon-assisted coil occlusion (so-called balloon rem odel- pliant balloon (asterisk) fixates the m icrocatheter in a proper position and
ing) of a paraophthalm ic aneurysm . (a) The angle bet ween the internal retains the coil loops inside the aneurysm sac. (c) Balloon remodeling fre-
carotid artery (ICA) and the aneurysm fundus is ~ 90 degrees. (b) The com - quently allows for a complete coil occlusion.

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550 V Cerebral and Spinal Aneurysms

w as pu blish ed by Th orn ton et al22 in 2000. Sixt y-on e paraclin oid of self-expan ding sten t s for th e t reat m en t of in t racran ial an eu -
an eur ysm s w ere t reated by en dovascular m ean s in 90 proce- r ysm s becam e available (e.g., Leo+, Balt Ext ru sion ; En terprise,
du res. Th e ach ieved occlu sion w as rated m ore th an 95% in 52/61 Codm an ; Neu roform EZ, St r yker, Kalam azoo, MI; Solitaire, ev3/
(85%) an d less th an 95%in 9/61 (15%). On ly 46 (75%) pat ien ts h ad Covid ien ; LVIS, Microven t ion , Sain t - Ger m ain -en -Laye, Fran ce).
angiograph ic follow -up (6 m on th s or m ore). Eigh t out of 46 pa- Sten t ing in th e con text of coil t reat m en t is effect ive in preven t ing
t ien ts requ ired su rger y after en dovascu lar t reat m en t (p ar t ial coil loop s from p rot ru d ing ou t side th e an eu r ysm al sac an d m ay
coiling: 2, refilling of a neck rem nant: 2, persistent m ass effect: 2; redu ce th e rate of delayed coil com pact ion .25,26 Both of th ese as-
coil p rot ru sion : 2). From th e 90 procedu res p erform ed, 2 (2.2%) pects are relevan t in paraop h th alm ic an eu r ysm s. Sten t ing p ro-
pat ien ts h ad m ajor p erm an en t deficits (1 m on ocu lar blin dn ess, vides a perm an en t su pport for th e coil loops, com pared w ith th e
1 h em iparesis), 1 (1.1%) h ad a m inor visu al field cut , an d 2 (2.2%) t ran sien t coil reten t ion during balloon rem odeling (Fig. 47.3).
pat ien ts d ied from th rom boem bolic even ts. Despite th e advan t ages gain ed by th e u se of a sten t , sten t ing
Malek et al23 st u died 20 p at ien t s w ith 22 an eu r ysm s, 16 of requires pret reat m en t w ith asp irin an d clopidogrel (du al an t i-
th em in th e p araop h th alm ic segm en t (13 p araoph t h alm ic an d p latelet regim en ) for at least 6 w eeks, follow ed by 1 year of
th ree su perior hypop hyseal ar ter y). Th ey selected an eu r ysm s m on oth erapy (asp irin or clop idogrel). An t icoagu lat ion for sten t -
w ith w ide n ecks or w ith com p lex geom et r y. Th e tech n ical su c- assisted coiling in terferes w ith th e m an agem en t of pat ien t s in
cess rate of balloon -assisted coiling w as 77% (17 of 22), an d 88% th e acu te p h ase of SAH (e.g., cerebrospin al flu id [CSF] drain age,
of th e pat ien ts had excellen t or good clin ical ou tcom es. Th e rate in t raparen chym al probes) an d sh ould be avoided in th ose w ith
of tech n ical com p licat ion s w as 13.6%, all w it h ou t clin ical con - acu tely ru pt ured an eur ysm s.
sequen ce. Perm an en t m orbidit y (30 days after t reat m en t) an d Several grou ps h ave repor ted an in creased frequen cy of com -
m ort alit y w ere both 0%. Th is series repor ted a h igh er rate of p lete occlu sion associated w it h t h e u se of sten t s relat ive to
th rom boem bolic even t th an Moret et al’s 19 origin al descript ion sim ple coiling in t reat ing paraoph th alm ic an eur ysm s. Th e rates
of th e tech n ique (11% vs 5.2%, respect ively). In th e previously of com plete occlu sion reach 40 to 50% in som e series.27–29 Sten t
qu oted series by Th orn ton et al,22 it is sign ifican t to n ote th at a dep loym en t m ay stabilize th e degree of coil occlu sion , d ecreas-
2.2% m ort alit y rate w as associated w ith balloon -assisted coiling. ing th e likelih ood of su bsequ en t coil com p act ion an d an eu r ysm
In th is series, t w o p at ien t s died due to m ajor brain in farct s after recan alizat ion . In a review of t h e literat u re by Ogilvy et al,29
th e proced u re; th ese in farct s w ere sp ecu lated to be th rom bo- recan alizat ion at follow -u p is arou n d 4.3% of p reviou sly tot ally
em bolic in origin . Oth er series in th e literat u re, h ow ever, sh ow a occlu ded an d 14.1%of in com pletely occluded an eur ysm s. Not all
low er risk of th rom boem bolic even t s.19,20,23 Addit ion ally, th ese par t ially recan alized an eu r ysm s are can didates for ret reat m en t .
rates h ave im proved w ith tech n ical advan ces an d a st ringen t use In a series publish ed in 2012, Colby et al25 ach ieved a com -
of periprocedu ral an t icoagu lat ion an d an t ip latelet m edicat ion s. plete coil occlu sion in 13 of 30 (43%) of th e sten ted an d in 19 of
To m in im ize com plicat ion , such as ar ter y dissect ion or an eu - 60 (32%) of t h e u n sten ted an eu r ysm s. Th e recan alizat ion rate
rysm perforation w ith the tip of the m icrocatheter or w ith the coil at 12.8 m on th s (m ean ) w as 11.5% in sten ted an eur ysm s versus
loops, m ost practitioners advocate partial inflation of the balloon 36%for th ose an eur ysm s th at w ere coil occluded w ith out a sten t .
du ring th e p rocedu re. It is also recom m en ded th at th e balloon be W it h a lon ger follow -u p (sten t: 14.5 m on t h s; n o sten t: 37.6
in flated in th e proxim al segm en t of th e n eck of th e an eu r ysm to m on th s), th e recu rren ce rates w ere 15% an d 42%, respect ively.
avoid an in crease in in t rasaccu lar p ressure. In a ret rospect ive series w ith 459 pat ien ts an d 489 t reated
aneurysm s, Jahshan et al30 com pared stent-assisted w ith conven-
t ion al coilin g; t h e sten t grou p con t ain ed few er r u pt u red an eu -
Stent-Assisted Coil Occlusion r ysm s. Th e frequ en cy of com p lete occlu sion at t h e last angio-
An oth er w ay to st abilize th e posit ion of a m icrocath eter w ith in grap h ic follow -u p w as sign ifican t ly h igh er after sten t -assisted
th e an eu r ysm is to dep loy a self-expan ding sten t over th e an eu - coilin g (60% vs < 50%). Th e au t h ors obser ved n o sign ifican t d if-
r ysm n eck after t h e an eu r ysm h as been cat h eter ized 24 (also feren ce in p erm an en t p rocedu re-related m orbidit ies, w h ich w as
called th e “jailing” tech n iqu e). Du ring th e last decade, a variet y below 5% in all subgrou ps.

a b c d

Fig. 47.3a–d Stent-assisted coil occlusion of a wide-necked paraophthal- MN) stent. At the sam e tim e an artificial border is created bet ween parent
m ic aneurysm . (a) The aneurysm neck is too wide to retain coils inside the vessel and aneurysm , providing a perm anent support for the coil loops dur-
aneurysm sac. (b) In the “jailed” catheter technique, the m icrocatheter is ing (c) and after (d) the coiling.
fixed in a proper position by deploying a Solitaire (ev3/Covidien, Plym outh,

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47 Endovascular Treatment of Carotid-Ophthalmic Aneurysm s 551

a b c

Fig. 47.4a–c Treatm ent of an unruptured sm all paraophthalm ic aneu- with coverage of the aneurysm . (c) Follow-up DSA 2 m onths later confirm s
rysm by flow diversion. (a) Left carotid digital subtraction angiogram (DSA) the complete obliteration of the aneurysm with patency of the ophthalm ic
shows the aneurysm at the origin of the ophthalm ic artery. (b) Deploy- artery.
ment of t wo flow-diverting implants (Pipeline, ev3/Covidien, Plymouth, MN)

Th e m ain con cern w ith th e u se of sten t s in th e p araop h th al- th e an eu r ysm al sac, bu t to red irect t h e blood flow aw ay from th e
m ic ICA is th e tor t u osit y of th e vessel, w h ich m ay cause kin king, an eur ysm an d along th e longit udin al axis of th e paren t vessel.
t w ist ing, an d p oor w all ap p osit ion of t h e sten t . Disp lacem en t Hem odyn am ic exclu sion of an an eu r ysm t riggers both in t rasac-
of a Neuroform sten t h as been repor ted, togeth er w ith th e sub - cular clot form at ion an d rem odeling of th e vessel w all (Figs. 47.4
sequ en t su rgical m an agem en t.31 Com p licat ion s rates of sten t- an d 47.5).
assisted coiling are in th e ranges of 6 to 7%m orbidit y an d 3 to 4% Obliterat ion or sh rin kage of an an eur ysm due to flow diver-
m ortalit y.26,32,33 Several auth ors have proposed that th e long-term sion m ay t ake w eeks or m on th s to occu r. On e flow -d iver t ing
resu lt s con cern ing t h e st abilit y of coil occlu sion are bet ter after d evice is m ostly sufficien t to t reat sm all an eur ysm s an d focal
sten t-assisted th an after balloon -rem odeled coil occlusion .25,30 ar terial-w all disease. In an eur ysm s w ith a ver y w ide n eck an d
especially in fu siform an eu r ysm s, it m ay be n ecessar y to deploy
several of th ese im p lan ts to p rom ote an efficien t d isru pt ion of
Flow Diversion th e in t ra-an eu r ysm al blood flow. On e of th e t h eoret ical vir t u es
In 2005, a novel strategy for the ext rasaccular en dovascular treat- of using a flow diver ter is n ot on ly occlu ding th e an eur ysm dom e
m en t of an eur ysm s w as in t roduced, an d a n ew fam ily of devices, but also allow ing m orph ological recon st ru ct ion of th e paren tal
called “flow diver ters,” em erged. Cu rren tly, several flow diver t- vessel w all by providing th e en doth elial layer w ith a suppor t for
ers h ave received t h e CE (Con for m ité Eu rop éen e) m ark in Eu - th e process of n eoin t im al grow th . It h as been sh ow n th at flow
rop e (e.g., Pip elin e, ev3/Covid ien ; Silk+, Balt Ext ru sion ; Su rp ass diver ters en able h igh er rates of com p lete occlu sion of th e an eu -
NeuroEndoGraft, Str yker; p64, ph enox Gm bH, Boch um , Germ any) r ysm al sac w h en com pared w ith oth er en dovascular tech n iques.
an d Food an d Drug Adm in ist rat ion (FDA) approval in th e Un ited Th is is t r u e even in large an d gian t an eu r ysm s (occlu sion rates
States (Pipeline). All curren tly available flow diverters are braided, bet w een 52%34 an d 100%35 h ave been repor ted w ith th e u se of
self-exp an din g im p lan t s. Th e m esh d en sit y of a flow d iver ter flow diverters). Most of th e long-term series reported m orbidit y
is m uch h igh er th an th e m esh den sit y of a conven t ion al self- rates of less th an 15%36,37 an d m or talit y rates of less th an 8%.33,38,39
expanding stent , w h ich increases th e vessel w all coverage signifi- Th e u se of flow d iver ters requ ires a dedicated regim en of
can tly. Th e goal of th ese devices is n ot to im m ediately occlu de m id- or long-term an t iplatelet m edicat ion to avoid in t ra-device

a b c

Fig. 47.5a–c (a) Growing neck rem nant (arrow) of a paraophthalm ic an- MN) jumped too far proximal during deploym ent. (c) Two m onths later, the
eurysm after coil occlusion. The site of the aneurysm origin is covered by neck remnant is obliterated (arrow) and the ophthalm ic artery is patent.
one flow-diverting device. (b) A Pipeline device (ev3/Covidien, Plym outh,

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552 V Cerebral and Spinal Aneurysms

occlusion or th rom boem bolic even ts. Exten ded an t icoagulat ion rem odeling (32%), sten t-assisted coiling (9%), or paren t-vessel
m igh t be required if several layers of th e device are im plan ted. occlusion (36%). In th is series, th ere w as a predom in an ce of large
Long-term an t icoagulat ion m ay cause a variet y of h em orrh agic an d gian t an eur ysm s, because th ey are less suitable for conven -
com plicat ion s su ch as gast roin test in al or ret rop eriton eal bleed- t ion al en dovascu lar tech n iqu es. All p at ien ts w ere follow ed for
in gs. In -sten t sten osis d u e to in t im al hyp er p lasia is in frequ en t 6 to 12 m on t h s after t h e p roced u re. High er rates of com p lete
an d self-lim ited w ith flow diver ters. Oth er com plicat ion s associ- occlu sion at follow -up w ere n oted in th e Pipelin e group (76.2%)
ated w ith th e u se of flow diver ters are in t rap aren chym al h em or- t h an in t h e con t rol grou p (21.4%). Du r in g t h e follow -u p , n o
rh age w ith rates ranging bet w een 1.1%33 an d 3.4%.34 Hem orrh age p at ien t s w ith p erm an en t m orbidit y w ere en cou n tered in th e
is frequ en tly cau sed by tech n ical com plicat ion s (e.g., problem s Pip elin e grou p , an d th e com p licat ion rates w ere sim ilar in both
in th e dep loym en t of th e device, p erforat ion w ith th e m icro- grou p s. Th ese resu lt s com p are w ell to t h ose obser ved in t h e
w ire), hypersen sit ivit y to an t iplatelet m edicat ion , or m icroem - PUFS (Pipelin e™ for Un coilable or Failed An eur ysm s) t rial (86%
boli an d m icroin farcts after t reat m en t . Th rom boem bolic even ts com plete an eu r ysm occlu sion at 1 year) th at led th e U.S. FDA to
repor ted in variou s series are relat ively in frequ en t (1.4%).37 Th e approve th e Pipelin e device.48 In th e PUFS t rial, th e rates of m ajor
d elay in t h e obliterat ion of th e an eu r ysm d om e m akes flow ipsilateral st roke an d of in t racran ial h em orrh age w ere 5.6% an d
d iversion a su bopt im al t reat m en t st rategy for acutely rupt ured 4.7%, resp ect ively. In th e Lan zin o et al47 series, on ly on e asym p -
an eu r ysm s. Never th eless, it s u se in p at ien t s w it h a p reviou s tom at ic occlusion of th e ICA w as repor ted. Th ere w ere n o cases
h istor y of SAH h as been repor ted in th e literat ure. In differen t of bleeding w ith in th e first 2 w eeks after t reat m en t .
series, delayed m orbidit y an d m ort alit y h ave reach ed 4 to 15% In a single-cen ter series of 104 an eur ysm s (47 t reated w ith
an d 4 to 8%, respect ively.33,38 t h e Silk flow d iver ter, 57 t reated w it h th e Pip elin e) p u blish ed
Because th e use of flow diverters is fairly n ew, long-term ex- by Pian o et al46 (w ith follow -up at 6 an d 12 m on th s), th e m orbid-
perien ce h as yet to be accu m u lated . On e seriou s issu e con cern s it y an d m ort alit y w ere both 3%. Th e rate of all adverse even t s
th e repor ted cases of delayed ru pt u re in in ciden t al an eu r ysm s w ith out clin ical relevan ce w as 20%. At 6 m on th s, 86% of th e an -
after flow diversion . It h as been hypoth esized th at th e early for- eu r ysm s w ere com p letely occlu ded an d 12% w ere p ar t ially oc-
m at ion of a fresh clot w ith a low fibrot ic com pon en t u n ch ain s an clu d ed . Tw o an eu r ysm s w ere u n ch an ged . In t h is ser ies, 49% of
in flam m ator y react ion in side th e an eu r ysm al sac. Th e p art icipa- all pat ien ts h ad paraclin oid or supraclin oid an eur ysm s. In th ese
t ion of leu kocytes t rap ped in side th e sac along w ith p roteolyt ic p ar t icu lar locat ion s, t h e m id ter m occlu sion rate rose to 93%.
en zym es com bin e to w eaken th e an eu r ysm al w all. In flam m a- Th ese resu lt s, com bin ed w ith a favorable an atom ic environ m en t
tor y “digest ion ” of th e an eu r ysm w all togeth er w ith th e residu al (lim ited presence of perforating branches, proxim al location, and
flow t h at keep s en ter in g t h e an eu r ysm al fu n d u s can lead to an ad equ ate caliber of t h e ICA), m ake an eu r ysm s of t h e in t ra-
a rapid disin tegrat ion of th e w all an d delayed an eur ysm r up - d u ral ICA a preferred target for flow diversion .
t ure.40,41 Ku lcsár et al42 pu blish ed an an alysis of th e delayed r u p -
t u re in a series of an eu r ysm s t reated by flow diversion . Th ey
Endovascular Parent-Vessel Occlusion
con sider th e form at ion of a fresh clot an d an in flam m ator y p ro-
cess as th e m ost likely et iology beh in d rupt u re. Con firm ing th ese Paren t-vessel occlu sion (PVO) is a w ell-est ablish ed, tech n ically
fin dings, m agn et ic reson an ce im aging (MRI) st u dies h ave dem - straightforw ard, safe, and therefore w idely used m ethod for treat-
on st rated perian eur ysm al h igh -sign al in ten sit y in T2-w eigh ted ing large, gian t , an d part ially t h rom bosed an eu r ysm s. PVO m ay
im ages th at suggest an in flam m ator y process.43 Th is in flam m a- also be applied to m an age an eur ysm recan alizat ion after m icro-
tor y react ion can be associated w ith m ass effect, h eadach e, an d su rgical or en dovascu lar t reat m en t . PVO is gen erally tolerated if
visual disturbance after flow -diverter deploym ent. After flow di- th e t arget vessel is su fficien tly collateralized. Visu alizat ion an d
version for large an d gian t an eu r ysm s, low -dose h eparin an d ad- fu n ct ion al test ing of collaterals is m ostly perform ed by balloon
m inistration of corticosteroids and nonsteroid anti-inflam m atory test occlusion (BTO) of th e poten t ial t arget vessel. In paraoph -
drugs are recom m en ded.33 th alm ic an d oth er in t radu ral ICA an eu r ysm s, com p lian t balloon s
A less crit ical issue is th e paten cy of bran ch es, n ot ably perfo- w ork best for BTO. Using t w o in dep en den t fem oral accesses, th e
rat ing ar teries, covered by th e flow -diver t ing im plan t . In para- target ICA is occluded for n o longer th an 20 to 30 m in utes. Dur-
ophth alm ic an eur ysm s, it is of in terest to assess th e effect on ing th is test occlu sion , th e an terior com m u n icat ing arter y (ACoA)
covered op h th alm ic ar teries. Pu ffer et al44 review ed a series of 20 an d PCoA are visu alized by inject ion of th e con t ralateral ICA an d
paraclin oid an eu r ysm s t reated w ith flow diversion . Th ey fou n d on e ver tebral ar ter y. If both com m un icat ing ar teries are absen t
t h at 25% of covered op h t h alm ic ar ter ies u n d er w en t occlu sion or h ave a ver y sm all caliber, th e BTO sh ou ld be term in ated at th is
over t im e, bu t n on e of t h ese p at ien t s exp erien ced clin ical se- p oin t or as soon as th e p at ien t d evelop s any n eu rologic d eficit
qu elae. Th ey did n ot fin d any correlat ion , for exam p le, w ith th e or com p lain s of severe h eadach e. If t h e ACoA h as a caliber of
n um ber of devices im plan ted. How ever, on e single flow diver ter ~ 2 m m , th e t im ing of th e an terior circulat ion ph lebogram h as
can lead to bran ch occlu sion . th e h igh est p red ict ive valu e. If on e ICA is occlu ded an d th e con -
Both MRI an d com p uted tom ograp hy (CT) st u dies h ave sh ow n t ralateral ICA is injected , syn ch ron icit y of t h e ven ou s an gio -
th at th e size of th e an eu r ysm dom e decreases in 14% an d 61%, graph ic p h ase of both h em isph eres allow s on e to con clu de t h at
respect ively, of th e cases after flow diversion .45–47 Th is obser va- th e p erm an en t occlu sion of on e ICA w ill likely be tolerated . Ve-
t ion is p ar t icu larly im p or tan t in cases of p araop h th alm ic an eu - n ous delay of th e h em isph ere depen den t on th e occluded ICA
r ysm s w ith m ass effect on th e opt ic n er ve or ch iasm .45,46 Lan zin o in dicates in su fficien t collateral flow, even if th e BTO is clin ically
et al47 p erform ed a m atch ed-p air an alysis of 22 paraclin oid an - w ell tolerated (Fig. 47.6).
eu r ysm s t reated w ith th e Pipelin e em bolizat ion device. Th e con - In th e case of dubious or poor n at u ral collaterals, a conven -
t rol grou p con sisted of sim ilar an eu r ysm s t reated w ith balloon t ion al byp ass bet w een th e su perficial tem p oral ar ter y an d th e

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47 Endovascular Treatment of Carotid-Ophthalmic Aneurysm s 553

a b

Fig . 47.6a,b Balloon test occlusion of an internal carotid artery (ICA) sphere. The venous delay on the right side indicates insufficient collateral
without and with sufficient collateral flow through the anterior com muni- flow through the ACoA. (b) Venous phase angiogram in an otherwise anal-
cating artery (ACoA). In both cases the right ICA was temporarily occluded ogous set ting. Veins and sinuses of both hem ispheres are opacified sim ul-
with a balloon catheter (asterisk) and the left ICA was injected. (a) Venous taneously. The collateral flow through the ACoA is m ost likely sufficient,
phase angiogram with opacification of veins and sinuses of the left anterior and the right ICA could be occluded if necessary with only lim ited risk of
circulation and parenchym al opacification without veins of the right hem i- hem odynam ic comprom ise.

m iddle cerebral arter y or a h igh -flow bypass m ay allow th e PVO. in 25%, an d w orsen ed in 38%. Du ring th e follow -up period, 75%
After bypass su rger y, an atom ic assessm en t of collateralizat ion of th e pat ien t s experien ced stabilizat ion or im provem en t of th e
becom es less reliable an d t h e BTO is m ain ly based on clin ical visu al sym ptom s.
toleran ce. The m echanism s underlying the im pairm ent of the optic ner ve
In an eur ysm s w ith sign ifican t m ass effect , clin ical im prove- fu n ct ion after coil occlu sion of an adjacen t an eu r ysm cou ld be
m en t h as been described in t w o th irds of cases.47,49 In th e recen t (1) direct m ass effect of th e coils on th e opt ic n er ve, (2) sw elling
st u dy of Lan zin o et al,47 th e rate of carot id ar ter y sacrifice in th e of t h e an eu r ysm d u e to in t rasaccu lar t h rom bu s for m at ion , or
con t rol group w as 36.4%. (3) t ran sm ission of th e ar terial pu lse w ave via th e solid an eu-
If th e an eur ysm dom e rem ain s in com m u n icat ion w ith th e r ysm m ass on th e opt ic n er ve. A th rom boem bolic occlusion of
ar ter ial circu lat ion , t h e r isk of a d elayed r u pt u re p ersist s, as th e op h th alm ic or ret in al ar ter y is also possible, an d sym ptom s
rep or ted by Gurian et al50 for th e posterior circulat ion an d by rem ain t ran sien t if th e occlu ded vessel h as a su fficien t collateral
Vin cen t et al49 in a case of a carot id-op h th alm ic segm en t an eu - circulation. Postoperative occlusion of the ophthalm ic arter y after
r ysm . A lim ited risk of flow -related an eur ysm form at ion on th e m icrosurgical aneurysm clipping m ay also cause m onocular blind-
ACoA or PCoA also exist s an d sh ould be rem em bered du ring late n ess.51 Sch m idt et al52 repor ted on eigh t pat ien ts w ith n on acute
follow -u p exam in at ion s. progressive visu al loss after coil occlu sion of p araclin oid an eu -
For th e en dovascu lar PVO, coil occlu sion of th e target an eu - r ysm s. MRI dem on st rated both perian eu r ysm al in flam m at ion
r ysm an d t h e p aren t vessel is t h e p refer red m eth od . After th is an d m ass effect of th e an eur ysm s. Visual im pairm en t im proved
procedure, patients are m onitored in th e in ten sive care unit w ith w ith th e system ic adm in ist rat ion of cor t icosteroids.
induced arterial hypertension w ith target values for systolic blood Su rgical case series rep or t p ostoperat ive visu al im p airm en t in
pressu re of 150 to 160 m m Hg for 3 to 4 days. 10 to 12%2,53 of pat ien t s. In th e series of Deh dash t i et al,54 t h e rate
of w orsen ed visual sym ptom s after surger y reach ed 14%, w ith a
rate of 28%p ostoperat ive n eck rem n an t s. Th e assum ed causes of
Visual Impairment Before and After Therapy postop erat ive visu al im pairm en t in clu de in adver ten t occlu sion
Th e effect of en dovascu lar th erapy on visu al fu n ct ion in pat ien t s of t h e op h t h alm ic ar ter y, su rgical t rau m a to t h e opt ic n er ve,
w ith clin ical sign s an d sym ptom s due to opt ic n er ve com pres- ven ou s congest ion , an d ar terial vasospasm . Th e qu oted rates of
sion h as been w ell st u d ied . Heran et al17 review ed 17 p at ien t s st abilit y or im provem en t of th e visu al fu n ct ion after surger y are
w it h u n r u pt u red large p araop h t h alm ic an eu r ysm s. Pat ien t s arou n d 80 to 90% in d ifferen t ser ies.53,54 In p at ien t s w it h acu te
u n d er w en t u n assisted or assisted coiling for th e t reat m en t of an - or progressive visual im pairm en t du e to paraclin oid an eur ysm al
eu r ysm s w ith an u n favorable dom e/n eck rat io, dysp last ic m or- m ass effect , m icrosu rgical clip p in g sh ou ld be con sid ered as a
ph ology, or ext rem ely tor t u ou s sip h on . Most of th ese an eu r ysm s first-lin e t reat m en t . Th is is also t ru e if on ly par t ial clip ping is
w ere pure oph th alm ic arter y an eu r ysm s. After t reat m en t , visual possible, becau se p ostoperat ive an eu r ysm rem n an ts are alm ost
sym ptom s im proved in 38%of th e pat ien ts, rem ain ed u n ch anged alw ays accessible for flow diversion .

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554 V Cerebral and Spinal Aneurysms

• An eu r ysm of any size w ith sign ifican t m ass effect , in clu d ing
■ Conclusion visual im pairm en t:
Th e m an agem en t of p araop h th alm ic ICA an eu r ysm s requ ires • Microsu rgical clipping
carefu l decision m aking. Microsu rgical t reat m en t can be associ- • Rupt u red an eur ysm of any size:
ated w ith tech n ical d ifficu lt ies du e to th e an atom ic relat ion of • Nar row -n eck an eu r ysm s w ith any clin ical con d it ion —coil
th e p araclin oid ICA to th e opt ic n er ve, th e cran ial n er ves, an d th e occlu sion p referred over clip ping; n o flow diversion
cavern ou s sin u s. Never th eless, m icrosu rgical clip p ing h as p roven • Wide-n eck aneur ysm s—clipping preferred over coil occlusion;
to be a safe opt ion w it h good an atom ic an d clin ical resu lt s, es- n o sten t , n o flow diversion
p ecially in r upt ured an d su periorly projected an eur ysm s an d in • Blister an eur ysm s—m icrosu rgical clipp ing or flow diversion
th ose w ith opt ic n er ve com p ression . Par t ial clip p ing of com plex • Relat ive argu m en ts again st clip ping in r u pt u red an eu r ysm s
an eur ysm s w ith m ass effect , follow ed by coil occlusion or flow in clude poor clin ical con dit ion or advan ced age
d iversion , is an ot h er opt ion . Th e en d ovascu lar ap p roach h as • Large or gian t an eu r ysm s, failed su rgical or en d ovascu lar at -
becom e accepted w ith t im e as an altern at ive to m icrosurgical tem pt , or an t icipated difficult y for eith er m eth od, w ith con -
clip p in g. In u n r u pt u red an d r u pt u red p araop h t h alm ic an eu - firm ed sufficien cy of collaterals:
r ysm s, coil occlu sion (frequ en t ly w it h balloon rem od eling or • Paren t-vessel occlusion
sten t assist an ce) is a viable opt ion . It is advisable to avoid sten t • Relat ive argu m en ts again st PVO in clu d e advan ced age (> 70
d ep loym en t in t h e acu te p h ase after SAH. Sten t in g of t h e p ara- years) or severe n eurovascu lar ath erosclerosis
clin oid segm en t of th e ICA seem s to p reven t coil p acking an d • Neck rem n an t after previou s coiling or clipping:
related an eu r ysm recan alizat ion after coil t reat m en t . More re- • Flow diversion or m icrosurgical clipping
cen tly, flow diversion h as gain ed acceptan ce as an altern at ive to • Relat ive argu m en ts again st flow diversion in clu de p reviou s
coil em bolizat ion . deploym ent of a porous sten t (reduced efficacy of flow diver-
Th e follow ing criteria are based on person al an d in st it ut ion al sion), large aneur ysm (risk of throm bus-induced an eur ysm
exp erien ce an d cou ld be u sefu l in select ing th e p rop er th erap eu - h em orrh age), severe m ass effect of th e an eur ysm , or con t ra-
t ic st rategy for paraoph th alm ic an eu r ysm s: in dicat ion to du al an t iplatelet th erapy

• Sm all un ru pt ured an eu r ysm , n o visu al failu re: Th e fin al d ecision on t h e id eal t reat m en t d ep en d s on a bal-
• Coil occlu sion , flow diversion , or m icrosu rgical clip ping w ith an ce bet w een t h e r isks an d ben efit s of t h e var iou s t reat m en t
treatm en t decision based on individual and local criteria (e.g., m odalit ies.
pat ien t’s preferen ce, con t rain dicat ion s for tem p orar y an t i-
coagu lat ion , age, an eur ysm geom et r y, etc.)

References
1. Drake CG, Van derlin den RG, Am ach er AL. Carot id-oph th alm ic an eur ysm s. 10. Juvela S, Porras M, Poussa K. Nat ural h istor y of un rupt ured in t racran ial
J Neu rosu rg 1968;29:24–31 an eu r ysm s: p robabilit y of an d risk factors for an eu r ysm ru pt u re. J Neu ro-
2. De Jesú s O, Sekh ar LN, Riedel CJ. Clin oid and paraclinoid an eur ysm s: su r- su rg 2000;93:379–387
gical an atom y, operat ive tech n iqu es, an d outcom e. Surg Neurol 1999;51: 11. Derdeyn CP, Barr JD, Beren stein A, et al; Execut ive Com m it tee of th e
477–487, discu ssion 487–488 Am erican Societ y of In ter ven t ion al an d Therapeut ic Neuroradiology;
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Trial (ISAT) Collaborat ive Group. In tern at ion al su barach n oid an eu r ysm eur ysm Trial (ISAT): a posit ion st atem en t from th e Execut ive Com m it tee
t rial (ISAT) of n eurosurgical clipping versus en dovascular coiling in 2143 of th e Am erican Societ y of In ter ven t ional an d Th erapeut ic Neuroradiol-
pat ien t s w ith rupt ured in t racran ial an eur ysm s: a ran dom ised com pari- ogy and th e Am erican Societ y of Neu roradiology. AJNR Am J Neuroradiol
son of effect s on sur vival, depen den cy, seizures, rebleeding, subgroups, 2003;24:1404–1408
an d an eur ysm occlusion . Lan cet 2005;366:809–817 12. Guglielm i G, Viñ uela F, Sepetka I, Macellari V. Elect roth rom bosis of sac-
4. Day AL. An eur ysm s of the ophth alm ic segm en t . A clin ical an d an atom ical cular aneur ysm s via endovascular approach. Part 1: Electroch em ical basis,
an alysis. J Neurosu rg 1990;72:677–691 tech n iqu e, an d exp erim en t al resu lt s. J Neu rosu rg 1991;75:1–7
5. Garcia-Pastor C, Moren o-Jim en ez S, Gom ez-Llat a An drade S. Microan ato- 13. Guglielm i G, Viñ uela F, Dion J, Duckw iler G. Elect rothrom bosis of saccular
m ia de la region selar y paraclin oidea en especim en es m exican os. Arch an eur ysm s via en dovascular approach . Part 2: Prelim in ar y clinical expe-
Neurocien (Mex) 2005;10:212–220 rien ce. J Neurosurg 1991;75:8–14
6. Kobayash i S, Kyosh im a K, Gibo H, Hegde SA, Takem ae T, Sugit a K. Carot id 14. Gurian JH, Viñ uela F, Guglielm i G, Gobin YP, Duckw iler GR. En dovascular
cave aneur ysm s of th e intern al carot id ar ter y. J Neurosurg 1989;70: em bolizat ion of superior hypophyseal ar ter y an eur ysm s. Neurosurger y
216–221 1996;39:1150–1154, discussion 1154–1156
7. Bouth illier A, van Loveren HR, Keller JT. Segm en t s of th e in ternal carot id 15. Roy D, Raym on d J, Bou t h illier A, Bojan ow ski MW, Mou m djian R,
arter y: a n ew classificat ion . Neurosurger y 1996;38:425–432, discussion L’Espéran ce G. En dovascular t reat m en t of oph th alm ic segm en t an eu-
432–433 r ysm s w ith Guglielm i det ach able coils. AJNR Am J Neuroradiol 1997;
8. Sh erif C, Gruber A, Dorfer C, Bavin zski G, St an dh ardt H, Knosp E. Rupt ured 18:1207–1215
carot id ar ter y an eur ysm s of th e oph th alm ic (C6) segm en t: clin ical an d 16. Boet R, Wong GK, Poon WS, Lam JM, Yu SC. An eur ysm recurren ce after
angiograph ic long term follow -up of a m u lt idisciplin ar y m an agem en t t reat m en t of paraclin oid/oph th alm ic segm en t an eur ysm s—a t reat m en t-
st rategy. J Neurol Neurosurg Psych iat r y 2009;80:1261–1267 m odalit y assessm en t . Act a Neuroch ir (Wien ) 2005;147:611–616, discus-
9. Orozco LD, Buciuc RF. Balloon -assisted coiling of the proxim al lobule of a sion 616
paraop h th alm ic an eu r ysm cau sing p an hypop it u it arism : Tech n ical case 17. Heran NS, Song JK, Ku persm ith MJ, et al. Large oph th alm ic segm en t an eu-
report . Su rg Neurol In t 2011;2:59 r ysm s w ith an terior opt ic pathw ay com pression : assessm en t of an atom i-

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cal an d visu al ou tcom es after en d osaccu lar coil t h erapy. J Neu rosu rg 37. Byrn e JV, Beltech i R, Yarn old JA, Birks J, Kam ran M. Early experien ce in th e
2007;106:968–975 t reat m en t of in t ra-cran ial an eur ysm s by endovascular flow diversion : a
18. Sorim ach i T, Ito Y, Morit a K, et al. Long-term follow -up of in t ra-an eur ys- m u lt icen t re prospect ive st udy. PLoS ONE 2010;5:9
m al coil em bolizat ion for un r upt ured paraclinoid an eur ysm s. Neurol Res 38. Pierot L. Flow diver ter sten t s in th e t reat m en t of in t racran ial an eur ysm s:
2012;34:864–870 W here are w e? J Neuroradiol 2011;38:40–46
19. Moret J, Cogn ard C, Weill A, Cast aings L, Rey A. Th e “Rem odelling Tech - 39. Szikora I, Beren tei Z, Kulcsar Z, et al. Treat m en t of int racran ial an eur ysm s
nique” in th e Treat m en t of Wide Neck In t racran ial An eur ysm s. Angio- by fu n ct ion al recon st r u ct ion of th e paren t ar ter y: th e Bu dap est exp eri-
graph ic Result s an d Clin ical Follow -up in 56 Cases. Inter v Neuroradiol en ce w ith th e Pipelin e em bolizat ion device. AJNR Am J Neu roradiol 2010;
1997;3:21–35 31:1139–1147
20. Irie K, Kaw an ish i M, Nagao S. Balloon -assisted Guglielm i d et ach able coil 40. Frösen J, Tulam o R, Paet au A, et al. Saccular in t racran ial an eur ysm : pa-
placem en t in w ide-n ecked in tern al carot id-oph th alm ic an eu r ysm s: a re- th ology an d m ech an ism s. Act a Neu rop ath ol 2012;123:773–786
por t of fou r cases. Min im Invasive Neu rosu rg 2002;45:146–150 41. Tulam o R, Frösen J, Hern esn iem i J, Niem elä M. In flam m ator y ch anges in
21. Iih ara K, Mu rao K, Sakai N, et al. Un ru pt u red p araclin oid an eu r ysm s: a th e an eu r ysm w all: a review. J Neu roin ter v Su rg 2010;2:120–130
m an agem en t st rategy. J Neurosurg 2003;99:241–247 42. Kulcsár Z, Houdar t E, Bon afé A, et al. In t ra-aneur ysm al th rom bosis as a
22. Th orn ton J, Alet ich VA, Debrun GM, et al. Endovascular t reat m ent of para- possible cause of d elayed an eur ysm ru pt u re after flow -diversion t reat-
clin oid an eur ysm s. Surg Neurol 2000;54:288–299 m en t . AJNR Am J Neuroradiol 2011;32:20–25
23. Malek AM, Halbach VV, Ph atou ros CC, et al. Balloon -assist tech n iqu e 43. Berge J, Tourdias T, Moreau JF, Barreau X, Dousset V. Perian eur ysm al brain
for en dovascular coil em bolizat ion of geom et rically difficult in t racran ial in flam m at ion after flow -diversion t reat m en t . AJNR Am J Neuroradiol
an eu r ysm s. Neu rosu rger y 2000;46:1397–1406, d iscu ssion 1406–1407 2011;32:1930–1934
24. Spiot t a AM, W h eeler AM, Sm ith ason S, Hui F, Moskow it z S. Com parison 44. Puffer RC, Kallm es DF, Cloft HJ, Lan zin o G. Paten cy of th e oph th alm ic ar-
of tech n iqu es for sten t assisted coil em bolizat ion of aneur ysm s. J Neuro- ter y after flow diversion t reat m en t of paraclinoid aneur ysm s. J Neu rosurg
inter v Surg 2012;4:339–344 2012;116:892–896
25. Colby GP, Pau l AR, Radvany MG, et al. A single cen ter com p arison of coil- 45. Fiorella D, Albuquerque F, Gon zalez F, McDougall CG, Nelson PK. Recon -
ing versus sten t assisted coiling in 90 con secut ive paraoph th alm ic region st ruct ion of th e righ t anterior circulat ion w ith th e Pipelin e em bolizat ion
aneur ysm s. J Neu roin ter v Su rg 2012;4:116–120 device to ach ieve t reat m en t of a progressively sym ptom at ic, large carot id
26. Piot in M, Blanc R, Spelle L, et al. Sten t-assisted coiling of in t racran ial an - an eur ysm . J Neu roin ter v Su rg 2010;2:31–37
eur ysm s: clin ical an d angiograph ic result s in 216 con secut ive an eur ysm s. 46. Pian o M, Valvassori L, Quilici L, Pero G, Boccardi E. Midterm an d long-term
St roke 2010;41:110–115 follow -u p of cerebral an eu r ysm s t reated w ith flow diver ter devices: a
27. Brism an JL, Song JK, Niim i Y, Beren stein A. Treat m en t opt ion s for w ide- single-cen ter experien ce. J Neurosurg 2013;118:408–416
necked in t racran ial an eur ysm s using a self-expan dable hydroph ilic coil 47. Lan zin o G, Crobeddu E, Cloft HJ, Han el R, Kallm es DF. Efficacy an d safet y
an d a self-exp an dable sten t com bin at ion . AJNR Am J Neu roradiol 2005; of flow diversion for paraclin oid an eur ysm s: a m atch ed-pair an alysis
26:1237–1240 com pared w ith st an dard en dovascular approach es. AJNR Am J Neuro-
28. Kis B, Weber W, Berlit P, Kü h ne D. Elect ive t reat m en t of saccu lar an d radiol 2012;33:2158–2161
broad-necked in t racran ial an eur ysm s using a closed-cell n it in ol sten t 48. Food & Dr ugs Adm in ist rat ion (FDA). Ch est n ut Medical Tech n ologies. Pipe-
(Leo). Neurosurger y 2006;58:443–450, discussion 443–450 lin e Em bolizat ion Device Execut ive Sum m ar y P100018 [repor t on lin e].
29. Ogilvy CS, Nat arajan SK, Jah sh an S, et al. Sten t-assisted coiling of para- 2011 Feb 1. Accessed Augu st 31st 2011. h t t p://w w w.fda.gov/dow n loads/
clin oid aneur ysm s: risks an d effect iven ess. J Neuroin ter v Surg 2011;3: Ad viso r yCom m it t e es/ Co m m it t e e sMe et in gMat e r ia ls/ Me d ica lDevice s/
14–20 Me d ica lDe vice sAd viso r yCo m m it t e e / Ne u r o logica lDe vice sPa n el/ UCM
30. Jah sh an S, Abla AA, Nat arajan SK, et al. Result s of sten t-assisted vs non - 247160.pdf
sten t-assisted en dovascu lar th erap ies in 489 cerebral an eu r ysm s: single- 49. Vin cen t F, Weill A, Roy D, Raym on d J, Gu ilber t F. Carot id op h t h alm ic
center experien ce. Neurosu rger y 2013;72:232–239 an eu r ysm ru pt ure after paren t vessel occlusion . AJNR Am J Neu roradiol
31. Th om as JA, Wat son VE, McGrail KM. Surgical m an agem en t of a paracli- 2005;26:1372–1374
n oid an eu r ysm con t ain ing a displaced Neu roform m icrosten t: techn ical 50. Gu r ian JH, Viñ u ela F, Gobin YP, Waston VE, Du ckw iler GR, Gu lielm i G.
case rep or t . Neu rosu rger y 2008;63:E817–E818, d iscu ssion E817–E818 An eu r ysm ru pt u re after p aren t vessel sacrifice: t reat m en t w ith Guglielm i
32. Fiorella D, Albuquerque FC, Woo H, Rasm ussen PA, Masar yk TJ, McDougall det ach able coil em bolizat ion via ret rograde cath eterizat ion : case rep or t .
CG. Neuroform in -sten t stenosis: inciden ce, n at ural h istor y, an d t reat- Neurosurger y 1995;37:1216–1220, discu ssion 1220–1221
m ent st rategies. Neurosurger y 2006;59:34–42, discussion 34–42 51. Mascaren h as L, Ribeiro M, Guim araes S, Roch a J, Alegria C. Un expected
33. Saatci I, Yavu z K, Ozer C, Geyik S, Cekirge HS. Treat m en t of in t racran ial angiograph ic an d visual findings after clipping of a carot id-oph th alm ic
aneurysm s using the Pipeline flow -diverter em bolization device: a single- an eur ysm . Neurocirugia (Ast ur) 2010;21:46–49
cen ter experien ce w ith long-term follow -up result s. AJNR Am J Neuro- 52. Sch m idt GW, Oster SF, Goln ik KC, et al. Isolated progressive visual loss
radiol 2012;33:1436–1446 after coiling of p araclin oid an eu r ysm s. AJNR Am J Neu rorad iol 2007;28:
34. Fisch er S, Vajda Z, Aguilar Perez M, et al. Pipelin e em bolizat ion device 1882–1889
(PED) for neurovascular recon struction : initial experience in th e treatm ent 53. Raco A, Frat i A, San toro A, et al. Long-term surgical result s w ith aneu -
of 101 in t racran ial an eur ysm s an d dissect ion s. Neuroradiology 2012;54: r ysm s involving th e ophth alm ic segm en t of th e carot id ar ter y. J Neu ro-
369–382 surg 2008;108:1200–1210
35. Lylyk P, Miran da C, Cerat to R, et al. Curat ive en dovascular recon st ruct ion 54. Deh dash t i AR, Le Rou x A, Bacigaluppi S, Wallace MC. Long-term visual
of cerebral an eur ysm s w ith th e Pipelin e em bolizat ion device: th e Buen os outcom e an d an eur ysm obliterat ion rate for ver y large an d gian t oph th al-
Aires exp erien ce. Neu rosu rger y 2009;64:632–642, discu ssion 642–643, m ic segm ent an eur ysm s: assessm en t of su rgical t reat m en t . Act a Neuro-
quiz N6 ch ir (Wien ) 2012;154:43–52
36. Lubicz B, Collign on L, Raph aeli G, et al. Flow -diver ter sten t for th e en do-
vascu lar t reat m en t of in t racran ial an eu r ysm s: a prosp ect ive st u dy in 29
pat ien t s w ith 34 an eu r ysm s. St roke 2010;41:2247–2253

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48 Surgical Therapies for Middle
Cerebral Artery Aneurysms
Hani Malone and Robert Solom on

Mid d le cerebral ar ter y (MCA) an eu r ysm s are a com m on cau se ger y; 107 pat ien t s w ith MCA an eur ysm s w h o presen ted in good
of subarach n oid h em orrh age (SAH), accou n t ing for 20% of all n eu rologic con dit ion w ere ran dom ized to surger y or con ser va
cases.1–4 Th e exp an d in g role of en d ovascu lar t h erapy h as h ad t ive th erapy grou p s. Tw en t y th ree percen t of su rgically t reated
a p rofou n d effect on t h e t reat m en t of both r u pt u red an d u n p at ien t s died com p ared w it h 33% of con ser vat ively m an aged
r u pt ured in t racran ial an eur ysm s. How ever, due to th e an atom ic p at ien t s. W h en w om en w ere con sid ered sep arately, t h ere w as
com p lexit y of th e MCA an d th e u n favorable size an d m orph ol an overall 29% m or talit y regardless of surgical or con ser vat ive
ogy of m ost an eu r ysm s th at origin ate along its course,5 t reat- th erapy.11
m en t of MCA an eur ysm s h as largely rem ain ed th e dom ain of th e Hook an d Norlen 12 provided a m ore opt im ist ic project ion for
cerebrovascular m icrosurgeon . An eur ysm s of th e MCA represen t th e fu t u re of MCA an eu r ysm su rger y in th eir 1958 rep or t . In th is
a full range of su rgical com p lexit y, from sm all an eu r ysm s along series, 45 p at ien ts h ad direct clip ping of MCA an eu r ysm s. Fou r
su p erficial MCA bran ch es th at requ ire m in im al dissect ion of th e p at ien t s d ied p er iop erat ively, an d 30 w en t on to m ake fu ll re
sylvian fissu re, to gian t fu siform an eu r ysm s along th e p roxim al coveries w ith good n eu rologic fu n ct ion . Th ese resu lt s w ere con
M1 segm en t th at in corp orate t h e len t icu lost riates. Th is ch apter sidered excellen t for th e t im e an d en cou raged fu r th er at tem pts
review s th e an atom y, n at u ral h istor y, an d clin ical presen tat ion s at su rgical ligat ion of MCA an eu r ysm s. Robin son 13 repor ted on
of MCA an eur ysm s, an d discusses th e in dicat ion s, tech n ique, an d 84 cases of r upt ured MCA an eu r ysm s bet w een 1947 an d 1969 in
outcom es related to en dovascular an d m icrosu rgical t reat m en t . New Zealan d. In th is series, th ere w as a 9% m or t alit y in grade I
an d II pat ien ts an d 50% m or talit y in poor grade pat ien ts. How
ever, if su rger y w as d elayed u n t il at least p ost bleed day 11,
p er iop erat ive m or t alit y fell to on ly 7%. Th is st u dy fu r t h er fou n d
t h at w rapp ing of th e an eu r ysm dom e w as totally u n sat isfactor y;
■ Brief Surgical History in 32 pat ien t s w h o h ad w rapping of th e an eu r ysm as th e pri
Alth ough th e surgical m an agem en t of in t racran ial an eur ysm s, in m ar y m od e of t reat m en t , th ere w as a m or t alit y of 34% d u e to
th e form of carot id ligat ion , dates back 200 years, th e first su c rebleeding.13
cessful direct t reat m en t of a rupt ured MCA an eur ysm w as n ot Th e adaptat ion of th e operat ing m icroscop e in th e 1960s rev
rep or ted u n t il 1941, w h en , follow ing tem p orar y occlu sion of olut ion ized in t racran ial an eur ysm su rger y an d greatly ch anged
t h e MCA, Sir Nor m an Dot t 6 op en ed a large MCA an eu r ysm an d exp ect at ion s regard in g a su ccessfu l ou tcom e follow in g an eu
p acked th e fu n d u s w it h p ieces of m u scle. Th ree years later, r ysm surger y in gen eral. In popu larizing th e pterion al cran iot
Dan dy 7 first reported h is su rgical series of in t racran ial an eu om y an d advan cing m icrosurgical tech n iqu e, m ost of th e credit
r ysm s, in cluding four located in th e MCA. All fou r pat ien ts died for th e m odern n eurosurgical approach to an terior circulat ion
perioperat ively, leading Dan dy to predict th at MCA an eur ysm an eur ysm s m ust go to Yaşargil.14 He st ressed th e im portan ce of
su rger y h ad a grim su rgical fu t u re. Desp ite th is p redict ion , it w as m in im izing brain ret ract ion by com pletely rem oving th e sph e
Dan dy’s su ccessfu l adapt at ion of clip ligat ion for th e t reat m en t n oid w ing an d detailed th e cisternal approach es n ecessar y to ar
of in t racran ial an eu r ysm s th at effect ively lau n ch ed th e m odern rive at an terior circu lat ion an eu r ysm s safely w ith m in im al brain
area of an eur ysm su rger y.8 ret ract ion an d t raum a.
Th e 1940s an d 1950s saw a great expan sion in both th e n u m Drake,15 Peerless,16 Su zu ki et al,17 an d Wilson an d Sp et zler 18
ber of n eu rosurgeon s an d th eir operat ive abilit ies. Du ring th is ach ieved good results operat ing on MCA an eur ysm s by first ex
tim e, neurosurgeon s becam e w ell acquainted w ith the techniques posing th e in tern al carot id an eu r ysm in th e basal cistern s. Th eir
n ecessar y to approach an eur ysm s in any in tracran ial locat ion dissect ion th en proceeded distally along th e carot id ar ter y, split
an d to m ech an ically obliterate th e an eur ysm n eck. Soph ist icated t ing th e sylvian fissu re from p roxim al to d ist al as th e MCA w as
instrum entation and vascular clips were developed by num erous follow ed ou t to t h e locat ion of t h e bifu rcat ion . Sym on ,19 Heros
su rgeon s an d m an u fact u rers to facilitate th e clip p ing of in t racra et al,20 an d oth ers adopted a m ore direct ap p roach to th e MCA
n ial an eur ysm s.9 bifurcat ion by par t ial resect ion of th e superior tem poral gyrus
En th u siasm for in t racran ial an eu r ysm su rger y w as tem p ered an d ent r y in to th e sylvian cistern . Using advan ced m icrosurgical
by McKissock an d colleagues,10 w h o perform ed ran dom ized con tech n ique, surgeon s such as Yaşargil4 an d Su n d t 3 learn ed to split
t rolled t rials com paring su rger y to con ser vat ive t reat m en t. Th eir th e sylvian fissu re at t h e level of th e fron t al an d tem poral op er
initial study of posterior com m unicating artery aneurysm s found culum to arrive directly at th e MCA bifurcat ion w ith out cort ical
n o ben efit of su rgical t reat m en t over con ser vat ive th erapy.10 A injur y. Th is ap proach w as w idely adopted an d rem ain s st an dard
su bsequ en t an alysis of MCA an eu r ysm s on ly sligh tly favored sur pract ice in th e m icrosu rgical t reat m en t of MCA an eur ysm s.

556

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48 Surgical Therapies for Middle Cerebral Artery Aneurysms 557

cal grou p of p erforators kn ow n as th e len t icu lost riate ar teries.


■ Relevant Anatomy Th ese vessels p ierce th e an terior p erforated su bst an ce to su p ply
Th e MCA is th e m ost an atom ically com plex ar ter y of th e cerebral m ost of th e pu tam en , caudate n ucleus, an d an terior lim b of th e
vascu lat ure. It is a con t in uat ion of th e in tern al carot id ar ter y dis in tern al capsule, in addit ion to lateral port ion s of th e globus p al
tal to th e poin t w h ere th e an terior cerebral ar ter y (ACA) em erges. lid u s an d dorsal p or t ion s of t h e p oster ior lim b of th e in ter n al
Th e MCA origin is located at t h e m edial en d of th e sylvian fissu re, cap su le.27 Of n ote, in som e in stan ces recurren t bran ch es dist al to
lateral to th e opt ic ch iasm , an d in ferior to th e an terior perforated th e MCA bifu rcat ion cou rse m edially to join th e len t icu lost riate
su bstan ce. On average, th e caliber of th e MCA is 70%greater th an ar teries entering th e an terior p erforated su bstan ce.
th at of th e ACA. Th e an atom ic com p lexit y of th e MCA n ecessit ates carefu l ex
Th e ar ter y cou rses laterally p arallel to t h e sp h en oid ridge to am in at ion of preoperat ive angiography w h en MCA an eu r ysm al
en ter th e sylvian fissu re. Th is in it ial length of th e MCA is called disease is su sp ected. Obliqu e an d t ilt view s m u st be obt ain ed to
the M1 segm en t. This segm ent cont inues until reaching the lim en visualize sm all MCA an eur ysm s th at m ay be h idden am ong th e
in sula, w h ere th e MCA sh arply cu r ves rost rally to reach th e sur m yriad loop s of th e d ist al m iddle cerebral bran ch es. Recon st ru c
face of th e in sula, m arking th e begin n ing of th e M2 segm en t . At t ion of digital su bt ract ion angiograp hy data aids op erat ive p lan
th e poin t of th e lim en in su la, th e MCA u su ally bifu rcates in to n ing by revealing th e an eur ysm an d adjacen t vessels in th ree
su p erior an d in ferior t r u n ks. Th e in ferior bran ch is larger in 32% dim en sion al space (Fig. 48.2).
of cases, th e superior division is larger in 28%of cases, th e vessels
are of equal caliber in 18%of cases, and an aberrant branching pat
tern is present 22%of cases. Th e superior trunk supplies the fron
tal lobe and the inferior trunk supplies the tem poral pole, w ith the ■ Pathophysiology
dom in ant of the t w o additionally supplying the parietal lobe.21
Th e com p lex p ath ogen esis beh in d th e form at ion of saccu lar an
Dist al to th e bifurcat ion , th e t run ks t urn posteriorly an d su
eu r ysm s along th e MCA, at it s bifu rcat ion , an d th rough ou t th e
periorly to reach th e su rface of th e in su la, p rodu cing a cu r ve
intracranial circulation is in com pletely understood. The tendency
kn ow n as th e gen u . Th e in ferior or su perior t run ks often divide
for in t racran ial an eur ysm s to occur at sites of ar terial bran ch ing,
just after th e bifu rcat ion , giving th e false appearan ce of an MCA
for w h ich th e MCA bifurcat ion is a prim e exam ple, in dicates h e
t rifu rcat ion . In cadaver st u dies p erform ed by Gibo, Rh oton , an d
m odyn am ic forces as a cat alyst of elast ic m em bran e division an d
colleagu es,21 an MCA bifu rcat ion w as fou n d in 78%of sp ecim en s,
in an eur ysm al form at ion .28 Th e et iologies of fu siform an d in fec
com pared w ith t rifu rcat ion in 12%, an d 10% en d ing in fou r or
t iou s MCA an eu r ysm s are dist in ct from saccu lar an eu r ysm s, an d
m ore p r in cip al t r u n ks. Up to 90% of MCA an eu r ysm s occu r at
th ese lesion s occur w ith far less frequ en cy. Alth ough rare, fusi
t h e bifu rcat ion , often project ing laterally in th e plan e of th e M1
form an eur ysm s can present w ith im pressive size, posing a con
segm en t ,22,23 alt h ough an eu r ysm or ien t at ion at t h is locat ion
siderable th erap eu t ic ch allenge. Like saccu lar lesion s, fu siform
var ies con siderably.24
aneurysm s generally occur at the bifurcation w hen present on the
Th e MCA gen erally divides fu r th er th rough a series of bifu rca
MCA. Conversely, infect ious or m ycot ic aneur ysm s, usually occur
t ion s to p rodu ce M3 segm en t s, w h ich exten d from th e in su la to
along distal M4 segm en ts an d are gen erally th e resu lt of in fec
th e su rface of th e sylvian fissu re, cou rsing th rough th e d ivision
t iou s em boli, m ost com m only from bacterial en docardit is.29
bet w een th e fron t al an d tem poral opercu la. Dist al M4 segm en t s
th en cou rse over t h e cor t ical su rface. In all, th e t w o m ajor t r u n ks
divide to form six to 11 stem ar teries in a h igh ly variable p at tern ;
th e stem ar teries fu r th er divide in to cor t ical ar teries.
Proxim al M1 segm en t an eu r ysm s are a ch allenging th erapeu
■ Natural History
t ic en t it y; for t u n ately, th ey m ake u p on ly 2 to 12% of all MCA In early collaborative reports com bining clinical series of rupt ured
aneurysm s (Fig. 48.1).22,24–26 The M1 segm ent gives rise to a crit i in t racran ial an eur ysm s, Sah s et al,1 McKissock et al,2 Yaşargil,4

a b

Fig. 48.1a,b (a) Carotid angiogram dem onstrating an aneurysm at the the M1 aneurysm originates proxim al to the genu of the MCA at the site of
middle cerebral artery (MCA) trifurcation, as well as a proximal M1 aneurysm. an early temporal branch.
(b) Three-dimensional reconstruction of the angiogram dem onstrates that

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558 V Cerebral and Spinal Aneurysms

a b c

Fig. 48.2a–c (a) Digital subtraction angiography dem onstrating a large bilobular m iddle cerebral artery (MCA) aneurysm . (b,c) Three-dim ensional re-
constructions are studied prior to surgery to delineate the m orphology of complex MCA aneurysm s and their relationship to adjacent vessels.

an d Sun dt 3 con sisten tly fou n d th at MCA an eu r ysm s accou n ted able select ion bias.32,33 Because pat ien ts en rolled in ISUIA first
for 17 to 21% of an eur ysm al SAH. How ever, th is repor ted in ci con su lted a n eu rosu rgeon for t reat m en t of th eir an eu r ysm , pa
den ce diverged sign ifican tly from au top sy st u dies. In con du ct ing t ien ts w ith a h igh risk of rupt ure (dict ated by size, fam ily h istor y,
3,425 au topsies, McCorm ick an d Acosta Ru a 30 fou n d th at 38.9% etc.) m ay h ave been iden t ified an d t reated by experien ced n eu
(n = 73) of t h e in t racran ial an eu r ysm s occu rred in t h e MCA, rosu rgeon s an d rem oved from th e t reat m en t pool. Accordingly,
m akin g it th e m ost com m on site for an eu r ysm al d isease d e t h e overall r isk of r u pt u re rep or ted by ISUIA, p ar t icu larly for
tected at au topsy. In terest ingly, on ly 19% of th e MCA an eu r ysm s an terior circulat ion an eur ysm s, is con sidered by m any to be an
detected at au top sy h ad been clin ically sym ptom at ic, com pared u n derest im at ion .32,33
w ith a rupt u re rate of 52% in detected an terior com m un icat ing In a st udy of 142 un rupt u red in t racran ial an eur ysm pat ien ts
ar ter y an eur ysm s an d 32% in in tern al carot id ar ter y an eur ysm s, w ith m in im ized select ion bias, long term follow u p (m ean 19.7
suggesting that MCA aneur ysm s m ay be less likely to rupt ure than years), an d h igh follow u p p ercen t age, Juvela an d colleagu es 34
an eur ysm s in oth er locat ion s. Th is ph en om en on w as at t ributed rep orted an an n u al r upt ure rate of 1.3%. In th is sam ple, 131 (92%)
to th e st abilizing effect of adjacen t cor tex surroun ding MCA an pat ien ts h ad p reviou sly exp erien ced SAH, w ere fou n d to h ave
eu r ysm d om es in th e sylvian fissu re, com p ared w ith an eu r ysm s m ult iple an eur ysm s, an d h ad on ly th e offen ding lesion clipped.
in oth er in t racran ial locat ion s w ith dom es exposed freely in th e Because th e m ajorit y of th ese p at ien ts h ad m u lt iple an eu r ysm s,
su barach n oid space. a greater percen tage of th e un r upt ured an eur ysm s obser ved in
More recen t n at u ral h istor y dat a from th e ret rosp ect ive co th is st u dy w ere located in th e MCA, w h ich m igh t suggest th at th e
h or t of th e In tern at ion al St u dy of Un ru pt ured In t racran ial An eu rep orted rupt u re rates m ore accu rately reflect an eur ysm s at th is
r ysm s (ISUIA)31 foun d th at 22.7% of un rupt ured in t racran ial an locat ion . How ever, th is st udy lacks sufficien t n u m bers of t ruly
eu r ysm s in p at ien t s w ith n o h istor y of SAH occu rred in th e MCA, in ciden tal asym ptom at ic an eu r ysm s (4%), an d dat a from ISUIA
suggest ing th at au top sy st u dies m ay h ave overest im ated th e suggests th at a h istor y of SAH can h ave a st rong im pact on th e
prevalen ce of disease at th is locat ion . On e possible exp lan at ion risk of r upt u re.31 Th e st udy is fu r th er lim ited by a h om ogen eou s
for th is discrepan cy is th e in creased likelih ood of m ult iple an eu Fin ish p at ien t p op u lat ion t h at m ay gen et ically be at in creased
r ysm s occu rring in th e MCA com pared w ith oth er locat ion s.24,31 risk of r upt u re, by single cen ter bias, an d a by st udy sam ple th at
Over on e th ird (37.8%) of pat ien t s from t h e ret rosp ect ive ISUIA w as en rolled years before th e in t rod u ct ion of m odern im aging
coh or t w ith m u lt iple an eu r ysm s an d a h istor y of SAH h ad u n tech n iques.33
t reated an eur ysm s located in th e MCA. Overall, both ISUIA an d Juvela et al34 rep or t a sim ilar risk of
Th e ISUIA st u dy fou n d a cu m u lat ive ru pt u re rate of 0.05% per rupt ure (1%) for pat ien ts w ith m u lt iple an eur ysm s w h o experi
year for an eu r ysm s sm aller th an 10 m m an d 1% for th ose th at en ced a SAH an d h ad on ly th e ru pt u red an eu r ysm t reated . Risk
w ere 10 m m or larger in pat ien ts w ith n o h istor y of SAH. In pa factors consistently associated w ith aneurysm rupture include ad
t ien ts w ith p reviou s SAH an d addit ion al u n ru pt u red an eu r ysm s, vanced age, histor y of hypertension and sm oking, as w ell as aneu
th e cu m u lat ive rate of ru pt u re w as ~ 0.5% p er year for lesion s rysm size, m ultiplicit y, and location in the posterior circulation.
sm aller th an 10 m m an d 1%for th ose th at w ere 10 m m or larger.
Th e MCA w as n ot am on g an eu r ysm locat ion s, in clu d in g t h e
basilar t ip , ver tebral basilar, p osterior cerebral, an d p oster ior
com m u n icat ing ar teries, fou n d to h ave a h igh er risk for r u pt u re.
In pat ien t s w ith n o h istor y of SAH, in creasing size an d locat ion
■ Clinical Presentation
w ere related to h em or rh agic risk. In p at ien t s w it h a p reviou s Due to th e in creased ut ilizat ion of com puted tom ography (CT)
rupt u re, on ly size an d in creasing age predicted ru pt u re.31 an d m agn et ic reson an ce (MR) im aging, asym ptom at ic in t racra
Desp ite it s large m u lt i in st it u t ion al sam p le, t h e ISUIA st u dy is n ial an eu r ysm s are being d etected w it h in creasing frequ en cy.
lim ited by ret rospect ive st u dy design an d poten t ial for con sid er Never t h eless, as w it h ot h er in t racran ial an eu r ysm s, t h e m ost

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48 Surgical Therapies for Middle Cerebral Artery Aneurysms 559

com m on clin ical p resen t at ion of MCA an eu r ysm s is SAH.24 In bled. Further com plicating this scenario is a tendency for patients
t h is cr it ical scen ar io, CT gen erally d em on st rates su barach n oid w it h m u lt ip le in t racran ial an eu r ysm s to h ave an eu r ysm s on
blood or in t raparen chym al blood, w h ich m ay be laterally local t h e p roxim al M1 segm en t (Fig. 48.1),22,24 w h ich requ ire a m ore
ized in th e sylvian fissu re. CT or MR angiography can be u sed to exten sive su rgical dissect ion of th e sylvian fissu re for su rgical
localize and characterize aneurysm s, but angiography w ith three t reat m en t .
dim en sion al recon st ru ct ion is opt im al to delin eate an eu r ysm In pat ien t s w h o presen t w ith rupt ured MCA an eu r ysm s an d
m orp h ology an d ap preciate it s relat ion sh ip to adjacen t vessels SAH or ICH, early su rger y is th e st an dard of care. In p at ien t s
prior to su rger y (Fig. 48.2). In th e absen ce of blood on CT, xan w h o presen t w ith un rupt ured MCA an eur ysm s, foun d in ciden
th och rom ia on lu m bar p u n ct u re in a pat ien t w ith a h istor y sug tally or du e to n on h em orrh agic sym ptom s, m yriad factors m ust
gest ive of SAH can be used to con firm diagn osis. be considered, including the natural history of disease, aneurysm
Cerebrosp in al flu id d rain age via ven t ricu lostom y is in d icated size, m orph ology, locat ion , m u lt ip licit y, possible et iology, pa
in pat ien t s w ith acu te hydrocep h alu s follow ing SAH an d ser ves t ien t age, m edical com orbidit ies, an d fam ily h istor y. Th ese vari
as a useful m ean s of m on itoring an d relieving in tracran ial hyper ables m u st all be factored in to a calculated decision abou t th e
ten sion in th e p erioperat ive p eriod . Pat ien ts sh ou ld be adm it ted lifet im e risk associated w ith u n r u pt u red in t racran ial an eu r ysm s
to an in ten sive care u n it w it h invasive blood p ressu re m on i in com parison w ith th e risk related to t reat m en t .36
tor ing an d t reated to a systolic blood p ressu re goal of less th an
140 m m Hg w ith in t raven ous an t ihyperten sive agen t s un t il th e
an eur ysm is secured. Acute t reat m en t follow ing MCA an eur ysm
rupt ure is often com plicated by th e presen ce of in t racerebral
h em orrh age (ICH).24,35 Pat ien ts w ith sign ifican t paren chym al
■ Perioperative Evaluation
h em orrh age sh ould h ave u rgen t clot evacuat ion an d t reat m en t Th e or ien t at ion of MCA an eu r ysm s, p ar t icu larly at t h e bifu r
of t h e offen d in g an eu r ysm w h en p ossible, as t h is can h ave a cat ion w h ere t h e vast m ajor it y of t h ese an eu r ysm s resid e, can
sign ifican t im p act on ou tcom e, even in p oor grade p at ien t s.5 be h igh ly variable. Accordingly, th e use of CT angiography an d
Th e m ain cau se of disabilit y am ong p at ien t s w h o su r vive MCA th ree dim en sion al digit al su bt ract ion angiography (DSA) can be
an eur ysm rupt ure w ith ICH m ay be dam age from th e origin al in st ru m en tal in th e p reoperat ive delin eat ion of an eu r ysm orien
h em atom a.5,35 tat ion relat ive to th e an atom y of th e MCA, its bran ch es, an d per
Un like ot h er in t racran ial an eu r ysm s, MCA an eu r ysm s m ay forators (Fig. 48.2).
grow to con siderable size, at t im es 20 m m or larger, prior to clin With an eu r ysm s n ear th e MCA bifurcat ion , localizat ion of th e
ical presen t at ion . Both large (11–25 m m ) an d gian t (> 25 m m ) an eur ysm is seldom a problem . How ever, for rare an eur ysm s on
an eu r ysm s com m on ly occu r in t h e MCA (Fig. 48.3).24 Th ese dist al MCA bran ch es or for m ycot ic an eu r ysm s on th e cor t ical
gian t an eur ysm s h ave a prop en sit y to cau se seizu res, sym ptom su rface, th e su rgical an atom y m ay be con fu sing an d an eu r ysm
at ic m ass effect , an d isch em ic in su lts, du e to th rom bu s or flow localizat ion difficu lt . Th e u se of im age gu ided stereotaxis m ay
redu ct ion .22,24 be ext rem ely valuable in th ese cases an d lim it th e n um ber of
Middle cerebral ar ter y an eu r ysm s are also dist ingu ish ed by bran ch es th at h ave to be explored before iden t ifying th e an eu
th e frequ en cy w ith w h ich th ey occu r as on e of m u lt ip le in t racra r ysm .37 Th e t reat m en t of gian t an d fusiform an eur ysm s often
n ial an eur ysm s. Rin n e an d colleagues 24 foun d th at 39% of MCA requires the evaluation of m ultiple perioperative factors and con
an eur ysm s are detected in th e con text of m u lt iple in t racran ial siderable su rgical p lan n ing. Th ese ch allenging su rgical lesion s
an eur ysm s, com pared w ith 20% for aneur ysm s in oth er loca m ay n ecessit ate a m odified cran iotom y, preparat ion for vessel
t ion s.22 Follow ing SAH, th is m ult iplicit y can pose a t reat m en t recon st ru ct ion , an d , in som e in st an ces, ext racran ial in t racran ial
ch allenge, as it m ay be difficu lt to determ in e w h ich an eu r ysm bypass (see Altern at ive Treat m en t Tech n iques, below ).22

a b c

Fig. 48.3a–c (a,b) Example of a giant, partially calcified middle cerebral vessel to identify the M2 segm ents and decompress the aneurysm dom e
artery (MCA) aneurysm with both m ajor M2 trunks originating from the for effective clipping. Intraoperatively, an angiogram with indocyanine green
junction of the aneurysm and M1 segm ent. Treatm ent of this aneurysm dem onstrated aneurysm obliteration without com prom ise of the M2 ar-
required t wo separate periods of temporary occlusion of the proximal M1 teries, which was later confirm ed with conventional angiography (c).

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560 V Cerebral and Spinal Aneurysms

■ Treatment Indications: Surgical and ■ Surgical Technique


Endovascular Therapies Equipment and Instrumentation
Th is ch apter p r im ar ily focu ses on m icrosu rgical t h erap ies for Prop er equ ip m en t an d in st r u m en t at ion are cr u cial for th e su c
MCA an eu r ysm s; h ow ever, it is im p or t an t to con sid er t h e ex cess of in t racran ial an eu r ysm su rger y. Th is is par t icu larly t r ue in
p an d ing role of en d ovascu lar t h erapy in th e t reat m en t of t h ese th e su rgical t reat m en t of MCA an eu r ysm s th at requ ire com p lex
lesion s, p ar t icu larly w h en d iscu ssing ap p rop r iate in d icat ion s d issect ion of t h e sylvian fissu re to facilit ate clip ligat ion . Th e
for t h erapy. Neu rovascu lar an d en d ovascu lar su rgeon s m u st op erat ive m icroscope h as greatly en h an ced su rgeon s’ abilit y to
m ake collaborat ive t reat m en t d ecision s based on each in d i su ccessfu lly com p lete th ese com p lex dissect ion s, n ecessit at ing
vid u al p at ien t ’s clin ical st at u s an d t h e n at u ral h istor y of t h e th e develop m en t of long an d delicate m icrosu rgical in st ru m en t s.
an eu r ysm . Alth ough th ere is n o stan dardized or agreed upon list of all th e
Desp ite t h e exp an d in g role of en d ovascu lar t h erapy in t h e in st ru m en ts th at m icrosu rgeon s m ust h ave at th eir disposal for
t reat m en t of in t racran ial an eu r ysm s as a w h ole, several im an eur ysm surger y, it is im port an t th at each su rgeon develop flu
p or t an t factors h ave t rad it ion ally m ad e MCA an eu r ysm s less idit y w ith m u lt iple in st rum en t s en abling th e execu t ion of th e
am en able to en d ovascu lar t reat m en t an d m ore favorable for m any ch allenging tech n ical m an euvers in h eren t to an eu r ysm
m icrosu rgical clip p in g. Th e great m ajor it y of t h ese an eu r ysm s surger y.
occu r su p er ficially at t h e MCA bifu rcat ion , m aking t h em read An array of dissectors w ith variou s t ips of differen t sizes an d
ily accessible via a lim ited d issect ion of t h e sylvian fissu re (see angu lat ion s is m an dator y for an eu r ysm d issect ion . Sh ar p d is
Sylvian Fissu re Dissect ion , below ). Given t h e p ersisten t h em o sect ion is preferable to blu n t dissect ion aroun d an an eur ysm ,
d yn am ic st ress at t h e MCA bifu rcat ion , e n d ovascu lar t reat because sh arp dissect ion avoids t ract ion on th e precarious an eu
m e n t s at t h is locat ion m ay b e m ore likely to re qu ire ret reat r ysm dom e.
m en t or resu lt in recu r ren t SAH, a com p licat ion t h at w as fou n d Th e clip app lier is a crit ical in st ru m en t th at som e w ou ld argu e
to be m ore com m on follow ing en d ovascu lar as com p ared w it h is p erh ap s m ore im p or t an t t h an w h ich an eu r ysm clip is u sed .
su rgical in ter ven t ion in t h e In ter n at ion al Su barach n oid An eu A m yriad of an eur ysm clips h ave been developed by a h ost of
r ysm Tr ial (ISAT).38 W it h im p roved en d ovascu lar tech n iqu es, m anufacturers, m ost w ith specific advantages and disadvantages.
t h is reh em or rh age risk can be vir t u ally elim in ated , as d em on It is im por t an t th at th e set of clip appliers used en ables th e su r
st rated in t h e Bar row Ru pt u red An eu r ysm Tr ial (BRAT) 39 ; h ow - geon to apply th e clip at any angle w h ile m ain t ain ing a ver y low
ever, it is st ill im p or t an t to con sid er an atom ic feat u res t h at m ay profile at th e app lier t ip. Th is factor becom es crit ical w h en ap
lim it t h e u se of en d ovascu lar coiling in t h e t reat m en t of MCA plying clip s in to deep exp osu res an d w h en n avigat ing arou n d
an eu r ysm s. crit ical st ruct u res th at m ust be preser ved .
Morph ological feat u res of MCA an eu r ysm s, frequ en t in corpo
rat ion of m ajor bran ch es in an eu r ysm w alls, an d sm all fun du s
to n eck rat ios (< 2) often p reclu d e en d ovascu lar coiling as an
Pterional Craniotomy
effective treatm ent option. Deeper MCA an eur ysm s located along With rare except ion , all MCA an eu r ysm s can be accessed via a
th e p roxim al M1 segm en t are often sm all, m aking th e placem en t properly executed pterion al cran iotom y. Th is approach t akes fu ll
of Guglielm i d et ach able coils (GDCs) tech n ically ch allengin g.22 advan t age of n at u rally occurring plan es an d spaces th at can be
Th e sm all caliber of both crit ical p erforators from th e M1 seg u t ilized to exp ose th e base of th e brain w ith m in im al ret ract ion .
m en t an d m ore dist al bran ch es from M2 an d M3, com plicates Th e orbit al roof an d sp h en oid w in g occu py a sp ace u n d er t h e
th e u se of sten t s in m ost in st an ces. Fu r th erm ore, th e frequ en t fron t al lobe an d bet w een th e fron t al an d tem p oral lobes th at can
broad n eck of MCA an eu r ysm s proh ibit s th e use of en dovascular be used to gain access to th e blood vessels at th e base of th e brain
coils in m any cases.22,24,40 w ith in th e basal cistern s, as w ell as w ith in th e sylvian fissure.
W h en assessing th e resu lt s of th e ISAT an d BRAT t rials, it is Rem oving the sph en oid w ing and flat tening th e orbital roof opens
im por t an t to con sider th at n eith er t rial st rat ified pat ien t ou t a space th at requires on ly m in im al ret ract ion of th e fron tal lobe
com es by an eu r ysm locat ion , m aking evalu at ion s of th e best to provide access to th e parasellar region . Careful dissect ion of
t reat m en t m odalit y sp ecific to MCA an eu r ysm s difficu lt . To ad th e sylvian fissu re en ables w id en ed exp osu re of th is sp ace, in
dress th is qu est ion , Regli an d colleagu es 41 com pared en dovascu creasing access to th e p repon t in e cistern s an d MCA.
lar coiling to surgical clip ping in t h e t reat m en t of 40 con secu t ive
un ru pt u red MCA an eu r ysm s t reated bet w een 1997 an d 2000.
Patient Positioning
En dovascu lar packing w ith GDCs w as con sidered th e first lin e of
t reat m en t , w ith su rgical clip ping u sed on ly after en dovascu lar Proper positioning can facilitate surgical exposure and dissection
failure or con t rain dicat ion due to angio an atom ic feat ures. Fol by recr uit ing th e posit ive con t ribu t ion of gravit y an d m in im izing
low ing th is protocol, th e au th ors fou n d th at 93% of un ru pt u red th e det rim en t al effect s of ven ou s engorgem en t . For a st an dard
MCA an eu r ysm s requ ired su rgical clip ping, an d con clu ded th at pterion al cran iotom y, th e pat ien t is posit ion ed su pin e w ith th e
despite advan ces in en dovascu lar p rocedu res, su rgical clipp ing h ead of th e bed elevated 10 to 15 degrees to en sure th at th e h ead
sh ou ld st ill be con sidered th e st an dard of care w h en t reat ing is above th e level of th e h eart . Th ree p oin t fixat ion is used to
MCA an eu r ysm s.41 Accordingly, m ost stan dard MCA an eu r ysm s secu re th e h ead w ith a Mayfield Kees or sim ilar cran ial fixat ion
are t reated at m ajor cerebrovascular cen ters w ith m icrosu rgical system . Im por t an tly, th e fixat ion system sh ould be radiolucen t
clipp ing.40 to facilitate in t raoperat ive angiography. Th e n eck is m axim ally

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48 Surgical Therapies for Middle Cerebral Artery Aneurysms 561

a b

Fig. 48.4a,b Patient positioning for pterional craniotomy. (a) A side view showing that the neck is rotated 30 degrees contralateral to the craniot-
of the patient’s head fixed in Mayfield-Kees rigid three-point fixation with omy. (Courtesy of Barrow Neurological Institute.)
the neck m aximally extended. (b) View from the top of the patient’s head

exten d ed w ith th e h ead elevated an d rotated 30 degrees con t ra tered, th e cran iotom e is rem oved an d placed back in th e in it ial
lateral to th e side of th e cran iotom y (Fig. 48.4). Th is posit ion bur h ole. A secon d cut is th en m ade m oving in feriorly an d an te
should allow gravit y to enhance the relaxation of the frontal lobes riorly along th e tem p oral squ am osa an d exten ding su p eriorly
aw ay from th e orbital roof w ith ou t in creasing ven ous pressure. back u p to th e in ferior edge of th e sp h en oid w ing.
Th e bon e flap can th en be fract u red across th e sph en oid w ing,
an d gen tle ep id u ral d issect ion w ill free t h e flap from it s d u ral
Soft Tissue Dissection
at t ach m en t s. Using a h igh sp eed d r ill w it h a cu t t ing bu r, th e
Tradit ion ally, th e skin in cision begin s 1 cm an terior to th e exter orbit al roof sh ou ld be flat ten ed an d any m ajor bu m p s rem oved,
n al auditor y m eat us an d exten ds from th e zygom a follow ing just m aking th e bony open ing flu sh w ith th e floor of th e fron t al
posterior to th e h airlin e an d exten ding an teriorly to th e m idlin e
(Fig. 48.5). A single in cision in th e p osterior asp ect of th e tem po
ralis m u scle en ables th e m uscle an d scalp flap to be reflected
an teriorly as a single layer. Th e m uscle is th en st retch ed an teri
orly over th e zygom at ic p rocess. Th is m eth od of an terior m u scle
elevat ion m in im izes risk to th e fron t alis bran ch of th e facial
n er ve, w h ich m ay be vuln erable w h en fash ion ing th e altern at ive
in terfascial tem poralis flap pop u larized by Yaşargil.4 W h en dis-
sect ing th e tem p oralis m u scle from th e su perior tem p oral lin e,
sm all h oles can be placed in th e bon e, so th at th e m u scle m ay be
reat tach ed w ith su t u res to it s proper bony in ser t ion at th e con
clu sion of th e op erat ion .42

Craniotomy and Dural Opening


A h igh sp eed cran iotom e sh ou ld be u sed to t u rn th e cran iotom y.
A single bur hole can be placed in the tem poral squam osa under
n eath th e tem poralis m uscle in th e posterior aspect of th e bony
exp osu re. Usin g t h e cran iotom e, t h e bon e cu t begin s m ovin g
su periorly along th e posterior border of th e bony exposure, ex
ten ding across th e lin ea tem poralis an d th en gradually cur ving
an teriorly to a poin t above th e orbital rim an d 3 to 4 cm m edial Fig. 48.5 Artist’s representation of the standard skin incision (dotted line)
and the pterional craniotomy (shaded area). (Modified from Zabram ski JM,
to th e orbit al at tach m en t of th e zygom a. Turn ing in ferior, th e cut
Kiris T, Sankhla SK, Cabiol J, Spet zler RF. Orbitozygom atic craniotomy.
th en follow s th e orbit al ridge, crossing th e lin ea tem p oralis as far Technical note. J Neurosurg 1998;89:336–341. Reprinted with perm ission
an terior as possible so th at th e cut correspon ds to th e posit ion of from the American Association of Neurological Surgeons and the Journal of
th e floor of th e fron tal fossa. On ce th e sph en oid w ing is en cou n Neurosurgery.)

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562 V Cerebral and Spinal Aneurysms

fossa. Th e lateral sph en oid w ing dow n to th e superior orbit al fis


su re is th en rem oved u sing th e drill or sm all rongeu rs, as in di
cated by th e an atom y of each in dividu al case.
Th e dura is op en ed in a sem ilu n ar fash ion , creat ing a flap t h at
is reflected an teriorly. W h en secu red w ith ten t ing sut ures, th is
flap effect ively seals off th e epidural space aroun d th e sph en oid
from th e op erat ive field an d h elp s m in im ize oozing du ring th e
m icrosu rgical com p on en t of t h e op erat ion . At t h is p oin t , t h e
op erat ing m icroscop e is gen erally brough t in to t h e field, an d
m icrosu rgical tech n iqu e is em p loyed for th e rem ain der of th e
operat ion.

Brain Relaxation
Brain relaxat ion can be crit ical to th e su ccess of in t racran ial an
eur ysm surger y. This factor is particularly im portant in the treat
m en t of recen tly rupt ured an eur ysm s com plicated by SAH an d
in t racran ial hyp er ten sion . W it h ju d iciou s cerebrosp in al flu id
(CSF) d rain age, ad equ ate CSF related brain rela xat ion can be
ach ieved in m ost pat ien ts.43 CSF sh ou ld be drain ed p rior to m ak
ing th e du ral op en ing, bringing elevated in t racran ial pressu re to
n ear n orm al.
In pat ien t s w ith SAH an d hydroceph alus n ecessitat ing exter
n al ven t ricular drain (EVD) placem en t , th is can be accom plish ed
by let t ing CSF off directly from th e EVD. Oth er w ise, in ser t ion of
an in t raoperat ive spin al drain age cath eter in to th e lu m bar th ecal
sac is th e preferred m eth od. It is th e au th or’s p olicy to u se sp in al
drain age in all pat ien ts w h o are w ith in 2 w eeks of SAH at th e Fig. 48.6 Typical location of an m iddle cerebral artery (MCA) bifurcation
tim e of surger y. Follow ing the induct ion of anesthesia, th e patien t aneurysm (arrow), seen on axial T2-weighted m agnetic resonance im aging
is turned to the lateral decubitus position and a lum bar punct u re (MRI). Note the proximit y of the aneurysm to the cortical surface and the
sm all am ount of dissection required to split the fissure to arrive at the an-
using a 14 gauge spin al drain n eedle is p erform ed. A sp in al
eurysm neck.
drain age cath eter can th en be p assed in to th e th ecal sac an d
used by th e an esth esiologist to w ith draw CSF th rough out th e
procedu re based on th e obser vat ion s of th e surgeon .
Usually, bet w een 60 an d 100 m L of CSF are rem oved to p ro su re requ ires m in im al brain ret ract ion to visu alize th e area of
vide adequ ate relaxat ion during acu te an eu r ysm surger y. In t ra th e MCA bifu rcat ion . Of all in t racran ial an eu r ysm su rgeries, MCA
ven ou s m an n itol sh ould be used to augm en t brain relaxat ion in an eur ysm surger y requires th e least brain ret ract ion (Fig. 48.6),
both rupt ured an d un r upt ured cases at a dose of 1 to 2 g/kg of m aking th e t ran ssylvian approach advan tageous even in poor
body w eigh t delivered approxim ately at th e t im e of skin in cision . grade p at ien t s in w h om th ere m ay be sign ifican t brain sw elling.
Man n itol also offers som e p rotect ion from cerebral isch em ia an d Th e t ran ssylvian app roach also con fers th e advan t age of con fin
is th erefore especially u seful in cases in w h ich tem porar y clip ing th e dissect ion to th e su barach n oid space, m in im izing t raum a
applicat ion is an t icip ated. to cor t ical st ru ct ures.
A t ran scor t ical ap p roach to MCA an eu r ysm s th rough th e
tem poral lobe h as been advocated by som e surgeon s.19,20 Th is
Microsurgical Approaches ap p roach cau ses t rau m a to ot h er w ise h ealt hy tem p oral lobe
Modern su rgical ap p roach es to MCA an eu r ysm s involve sp lit t ing p aren chym a, in creasing th e risk of post t raum at ic epilepsy, an d
th e sylvian fissu re an d eith er follow ing th e MCA dist ally from it m ay be dangerou s in th e case of MCA an eu r ysm s t h at m ay be
th e carot id bifu rcat ion to th e an eu r ysm 16–18 or st art ing at th e M3 em bedded in th e tem poral lobe. Accordingly, th e t ran scort ical
bran ch es an d follow ing th em proxim ally to th e MCA bifu rca ap p roach h as been largely aban d on ed , w it h th e except ion of
t ion .3,44 Com plete sylvian fissu re dissect ion dow n to th e carot id cases w h en th e fron t al an d tem poral opercu la are so den sely ad
cistern is seldom n ecessar y for MCA bifu rcat ion an eur ysm s. Such h eren t th at n o subarach n oid space can be easily developed. In
an approach requires a considerable am ount of dissection, sylvian th ese cases, a su bpial dissect ion of th e su perior tem p oral gyru s
fissure open ing, an d fron tal/tem poral lobe ret ract ion . Th is dis dow n to th e sylvian cistern affords deep er en t r y in to th e sylvian
sect ion is also t im e con su m ing, bu t it does offer th e sign ifican t cistern an d sat isfactor y exposure of th e m iddle cerebral vessels.
advan t age of m ain tain ing p roxim al con t rol of th e MCA th rough
out th e dissect ion , an d m ay be preferable for surgeon s w ith lit tle
Sylvian Fissure Dissection
experien ce dissect ing th e sylvian fissu re.
In the au th or’s experien ce, a direct t ran ssylvian approach to Classically, th e poin t of in it ial en t r y for sylvian fissu re dissect ion
th e MCA bifu rcat ion is th e m ost efficien t plan for MCA an eu r ysm is below th e pars t riangu laris of th e in ferior fron t al gyr us, w h ere
su rger y. With p rop er brain relaxat ion , open ing th e sylvian fis th e dist al sylvian fissu re is w idest . In pract ice, th e exact poin t of

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48 Surgical Therapies for Middle Cerebral Artery Aneurysms 563

en t r y is less crit ical. Th e su rgeon sh ou ld aim for a p oin t w h ere deep er an terior circu lat ion an eu r ysm s or basilar an eu r ysm s. In
th e fron t al op ercu lu m an d tem p oral lobe are n ot in opp osit ion , m ost cases, th ere is n o n eed to disru pt th e an terior port ion of th e
sign ified by an area of t ran sp aren t arach n oid. Of n ote, th e ven ou s sylvian fissu re, w h ere th e sylvian cistern com m u n icates w ith th e
an atom y of th e surface of th e sylvian fissure is h igh ly variable. basal cisterns. MCA aneurysm s often lie fairly superficially w ithin
Th ere are often m u lt ip le large vein s th at follow th e cou rse of th e th e sylvian fissu re, adjacen t to th e lateral p ar t of th e sph en oid
sylvian fissu re drain ing in to th e sp h en op ariet al or cavern ou s si w ing. Th erefore, a relat ively sh allow dissect ion is often all th at is
n uses. Th ese large vein s gen erally drain th e fron tal an d tem poral n eeded to expose th e n eck of th e an eur ysm (Fig. 48.6).
lobes, bu t alm ost invariably en ter th e sin u ses on th e tem poral Yaşargil44 described a ver y w ide dissect ion of th e en t ire syl
side, m aking it advisable to en ter th e fissu re on th e fron tal sid e vian fissu re for MCA an eur ysm s an d exposure of th e basal cis
of th ese vein s in order to n ot h ave th ese vein s crossing th e opera tern , in cluding th e lam in a term in alis. Th is am oun t of dissect ion
t ive exp osure. appears to be excessive, except in cases of gian t an eur ysm s th at
Sh arp dissect ion is n ecessar y to com m en ce sylvian fissu re require m axim al exposure. For m ost sm all an d in term ediate
dissect ion . On ce th e cistern of th e fissu re h as been en tered, th e sized an eu r ysm s of th e MCA bifu rcat ion , a lim ited dissect ion of
dissect ion p roceed s by gen tly sp reading th e lips of th e fissu re th e sylvian fissu re th at p rovides visu alizat ion of th e dist al p or
from th e in side an d p rogressing p roxim ally by p u t t ing pressu re t ion of th e M1 ar ter y is all th at is n eeded for an eu r ysm exp osu re
on both w alls of th e fissure; th e overlying bridging t issues are an d clipping. Because th e an atom y of th e MCA is variable an d
st retch ed, an d sh arp dissect ion of t h ese bridging fibers is easily com plex w ith m any overlapping loops, m ultiple M2 branches m ay
accom plish ed. On ce th e fissu re h as been defin it ively en tered, n ot be fully appreciated w ith angiography an d th e angiogram
su bsequ en t d issect ion con t in u es from “in side ou t .” Th e goal is to can n ot replace carefu l visual in spect ion of th e MCA bifurcat ion .
keep both pial su rfaces com pletely in t act an d to separate th e t w o Sylvian fissu re dissect ion is con siderably m ore com plex w h en
lobes in th e arach n oid sp ace, alth ough th is is som et im es im pos t reat ing an eur ysm s th at origin ate on th e M1 p or t ion of th e MCA
sible to ach ieve. Occasion ally, th e orbit al fron tal gyrus m ay in in conjun ct ion w ith an early tem poral bran ch (Fig. 48.1). Th ese
den t in to th e tem p oral lobe, greatly obscu ring th e CSF cistern . In an eu r ysm s are m ore d ifficu lt to exp ose, as t h ey ar ise p roxim al
th ese cases, th ere is n o ch oice bu t to pu rsu e a subp ial dissect ion to th e lim en in sula an d gen u of th e MCA. A com plete sp lit of th e
th rough th e adh eren t p or t ion of th e fissu re. Th e on ly t ru e lan d sylvian fissure is desirable in th ese cases to gain access to th e
m arks to th e locat ion of th e fissure in th ese cases are th e dist al region of t h e carot id bifu rcat ion an d to en able t h e su rgeon to
bran ch es of th e MCA th at t ravel in th e sylvian fissure. Alth ough visu alize t h e p roxim al M1 ar ter y. Dissect ion of t h is p or t ion of
n ecessar y subpial dissect ion is gen erally n ot dangerous to fun c th e sylvian fissu re is m ore h azardou s, an d great care m u st be
t ion ing n eu ral t issu e, it can cau se bleeding th at m ay im p ede p ro taken to protect an terior tem poral bran ch es an d th e len t iculo
gression of th e dissect ion . st riate ar teries th at origin ate along th e h orizon t al segm en t of th e
Occasion ally, vein s in th e fissu re th at bridge th e fron t al an d M1 ar ter y. In som e cases, recu rren t len t iculost riate ar teries orig
tem poral lobes m ust be divided to facilitate com plete separat ion in ate from th e m ajor t ru n ks of M2 bran ch es an d ret urn back
of th e t w o lobes. Sacrifice of th ese bridging vein s is acceptable along th e M1 ar ter y to en ter th e an terior perforated substan ce.
and is not clinically significant. Conversely, cerebral arteries never In adver ten t clipping of th ese ar teries can h ave seriou s sequelae
su p ply both th e fron t al an d tem p oral lobes. Un d erstan d ing th is an d m u st be avoided.
im por t an t an atom ic con cept aids th e dissect ion , especially w h en
t w o p ial surfaces are den sely adh eren t .
Aneurysm Dissection
W h en operat ing to secu re ru pt ured MCA an eu r ysm s w ith re
sultant large tem poral or frontal hem atom as, using the subarach On ce th e M1 sect ion of th e MCA proxim al to th e an eur ysm h as
n oid approach elim in ates th e possibilit y of dist urbing th e dom e been exp osed , t h e sylvian fissu re d issect ion can be h alted an d
of th e an eur ysm before exposing its n eck, w h ich alw ays resides at ten t ion focu sed on t h e an eu r ysm it self. Great care m u st be
in th e su barach n oid sp ace. In su ch cases, th e an eu r ysm is clipp ed taken w ith recen tly rupt ured an eur ysm s to leave un dist urbed
prior to en t r y in to th e brain an d evacu at ion of th e in t racerebral th e pia, th e arach n oid, an d th e blood clot th at are adh eren t to th e
h em orrh age. W h en a large h em atom a is presen t in th e sylvian dom e of th e an eu r ysm w h ile all m ajor bran ch es of th e MCA are
fissure it self, th e volum e of th e blood clot expan ds th e sylvian iden t ified. Most MCA an eu r ysm s arise at th e t r ue bifurcat ion of
fissure separat ing th e fron tal an d tem poral lobes, often sim plify th e M1 segm en t in to th e t w o m ajor M2 bran ch es, bu t , as previ
ing dissect ion . How ever, in th ese cases, care m u st be taken n ot to ously m en t ion ed, as m any as four m ajor M2 bran ch es m ay be
dist urb th e clot w h ich is adh eren t to th e dom e of th e an eur ysm . iden t ified from th e term in us of th e M1 ar ter y. Great care m u st
A prim ar y draw back of th e t ran ssylvian approach is th at th e be taken to en su re th at a com plete in spect ion h as been m ade
n eck an d dom e of th e an eur ysm are usually en coun tered before circum feren t ially aroun d th e n eck of th e an eur ysm so th at n o
th e M1 segm en t of th e MCA can be clearly defin ed. W h en th e u n seen bran ch w ill be acciden t ally in clu ded w h en clipping th e
dom e of th e an eu r ysm is en cou n tered, th e p ath of least resis aneurysm neck (Fig. 48.7). With sm all aneur ysm s, this in spection
tan ce aroun d th e dom e is taken to advan ce th e dissect ion to th e m ay not be challenging. How ever, as aneur ysm size increases, and
base of th e an eur ysm an d to th e M1 ar ter y. On ce th e d ist al M1 cer t ain ly w ith gian t an eur ysm s, visualizat ion of ar terial bran ch es
ar ter y proxim al to th e an eur ysm is con t rolled an d prepared for on th e opposite side of th e an eur ysm dom e m ay be difficu lt .
tem porar y clipping, n o deeper dissect ion is required. How ever, Gen tle depression of th e n eck of th e an eu r ysm is usually suf
th e crit ical in it ial goal in MCA an eu r ysm su rger y is to gain con ficien t to visualize aroun d th e posterior aspect of th e an eur ysm
t rol of th e M1, before any an eur ysm dissect ion is at tem pted. an d en sure th at n o ar teries are adh eren t to th e posterior face of
Th e am ou n t of sylvian fissu re d issect ion requ ired for MCA t h e an eu r ysm d om e. How ever, w it h large, com p lex an eu r ysm s
an eur ysm s is often far less th an th at requ ired to gain exposure to an d in th ose w ith calcificat ion in th e n eck region , visu alizat ion

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564 V Cerebral and Spinal Aneurysms

a b c

Fig. 48.7a–c Large proxim al m iddle cerebral artery (MCA) aneurysm that beyond the MCA bifurcation into the region of the lenticulostriate arteries.
was clipped with resulting postoperative right leg weakness. (a) Preop - (c) Postoperative computed tom ography (CT) scan showing a sm all lacunar
erative angiogram dem onstrating a large aneurysm arising at the proxim al infarct in the left posterior internal capsular/basal ganglia (arrow). Place-
MCA bifurcation. (b) Postoperative angiogram after clipping of the aneu- m ent of the clip too deeply resulted in occlusion of a sm all striate artery
rysm , using a long straight clip. Note that the clip passes several millim eters that was m issed at the tim e of the operation.

of th e con t ralateral side m ay be im possible w ith out th e use of cau sed. In som e in st an ces, th ese vessels are so den sely adh eren t
tem porar y clips. Tem porar y occlusion of th e M1 ar ter y soften s to a th in w alled an eur ysm th at dissect ion off th e dom e is too
th e an eur ysm an d en ables gen tle ret ract ion . In som e cases, isola dangerou s to en ter t ain in th e ar terialized st ate. Again , tem p o
t ion of the an eu r ysm by clipping all of th e M2 bran ch es an d th e rar y occlusion is advan t ageou s for fin al dissect ion an d clip ap
M1 bran ch is n ecessar y to com pletely collapse th e an eur ysm an d plicat ion in th ese cases.
m ake a 360 degree circum feren tial dissection possible (Fig. 48.8).
A brief period of tem p orar y occlu sion is u su ally a safe an d effec
Clip Application
t ive w ay to gain visualizat ion to clip com plex an eur ysm s in th is
locat ion . Clip applicat ion can proceed on ce th e M1 ar ter y, all M2 bran ch es,
Middle cerebral arter y an eur ysm dissect ion is often com pli an d oth er MCA bran ch es th at m ay lie on th e u n dersurface of th e
cated by the adherence of m ajor vessels as they pass the aneurysm an eur ysm n eck h ave been iden t ified. It is im por tan t to in spect
d om e. Major M2 or M3 bran ch es h ave a propen sit y to adh ere to th e an eu r ysm n eck to determ in e th e exact depth th at th e clip
th e fu n dus of th e an eu r ysm at a locat ion w ell distal to th e origin blades n eed to pass to obliterate th e an eur ysm n eck. If too long
of th ese bran ch es. If su fficien t at ten t ion h as n ot been p aid to a clip length is selected, or if th e clip is advan ced too deeply,
th ese ar teries prior to clipping, an d th e an eur ysm clip is closed, dam age to u n su spected bran ch es m ay occu r (Fig. 48.7). As th e
t h e bran ch m ay st retch , kin k, or even r u pt u re d u e to t ract ion clip is being ap p lied, it is n ot alw ays p ossible to see bot h dist al

a b

Fig. 48.8a,b Artist’s rendition of the steps in dissecting a complicated artery. (b) To safely dissect the aneurysm , temporary clips are applied to
m iddle cerebral artery (MCA) bifurcation aneurysm . (a) View of the M1 and the M1 branch and both easily visualized M2 vessels. Suction is then placed
M2 arteries and the aneurysm dom e following initial sylvian fissure dissec- in a hole in the aneurysm to collapse it, while the posterior dissection is
tion. Inset: The true anatomy of the MCA with an M2 branch hidden behind perform ed to reveal the third m ajor M2 branch and the striate artery.
the dome of the aneurysm and giving origin to a recurrent lenticulostriate (Courtesy of Barrow Neurological Institute.)

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48 Surgical Therapies for Middle Cerebral Artery Aneurysms 565

blade tips. Therefore, before clipping, the surgeon m ust determ ine ch ecked for u n seen p er forators or u n seen recu r ren t st r iate ar
th e p roper sh ap e an d size of clip to u se an d develop a m en t al ter ies th at m ay h ave been in cluded in th e clip. If any im perfec
im age of h ow deep ly to p ass th e clip. t ion is discovered, th e clip sh ou ld be reposit ion ed . In t raoperat ive
Most MCA an eu r ysm s can be obliterated u sin g st an dard angiography is stan dard pract ice at ou r in st it ut ion , as it allow s
st raigh t or cu r ved clip s. Th e exact angle an d depth of ap plicat ion for im m ediate con firm at ion of an eur ysm obliterat ion an d m ajor
are determ in ed during in spect ion of th e an eur ysm . With an eu vessel p aten cy.46 Flu orescein angiograp hy h as also been u sefu l as
r ysm s of ~ 1 cm in size or less, it is usually safe to apply th e clip an in t raoperat ive im aging tech n ique.47 How ever, in rare cases,
directly to th e n eck follow ing ad equ ate dissect ion . With gian t th e in form at ion h as been difficu lt to in terp ret , an d it is st ill ou r
an eur ysm s, especially w h en par t of th e w all n ear th e n eck is policy to rely on in t raoperat ive DSA.
h eavily calcified, a single clip can n ot close th e en t ire n eck. Even In rare in st an ces, crit ical bran ch es em an ate from th e top of
if th e blades are long en ough , th e am ou n t of t issue or calcifica th e an eu r ysm dom e. Th is sit u at ion requires a m ore im agin at ive
t ion th at resides in th e clip w ill p reven t th e dist al blades from an d n uan ced applicat ion of clips to m aintain circulat ion to dist al
closin g com p letely. To d eal w it h t h is sit u at ion , t h e u se of a bran ch es. Som et im es it is im possible to clip an MCA an eur ysm
st raigh t fen est rated clip is recom m en ded. Th e proxim al p or t ion w ith out occluding bran ch es. Asym ptom at ic stable an eur ysm s
of th e an eur ysm n eck or th e por t ion con t ain ing calciu m is left can be left u n clip ped, invested w ith m uslin gau ze, an d referred
open in th e fen est rat ion w h ile th e blades close off th e dist al par t to an in ter ven t ion al n eu roradiologist for evaluat ion . Previously,
of th e n eck. Th e an eur ysm in th e fen est rated por t ion of th e clip rupt ured an eur ysm s gen erally m an dated clipping, w ith th e h ope
is dealt w ith separately, using sh or ter, st ronger clips to occlu de th at bran ch es from th e dom e h ad adequate collateral circu lat ion .
th is p or t ion . More recen tly, several in n ovat ive bypass procedures h ave been
Ru pt u re du ring MCA an eu r ysm su rger y is p ar t icu larly h az develop ed to address an eu r ysm s th at can n ot be safely clipp ed or
ardous because of th e com plex vascu lar an atom y of th is region . coiled.26,48–50
Bleeding obscures th e field an d greatly in creases th e likelih ood
th at n orm al vessels w ill be com prom ised. Fu r th erm ore, if th e
blade is n ot com pletely across th e n eck of th e an eur ysm w h en
Alternative Treatment Techniques
th e clip is closed, th ere is an in creased risk th at th e blade w ill Desp ite im proved tech n iqu es an d tech n ological advan ces in m i
perforate th e an eu r ysm w h en th ere is fu ll ar terial pressu re in crosu rger y, th e size, m orph ology, an d com plex vascular an atom y
side th e lu m en . For th ese reason s, tem p orar y occlu sion of M1 of certain MCA aneur ysm s precludes treatm ent w ith clip ligation.
just prior to clipping sh ou ld be used w ith large (11 to 25 m m ) Th ese lesion s ten d to be large or gian t , w ith a fu siform sh ape or
an d com plex an eur ysm s. Placing at least on e tem porar y clip on a broad calcified n eck, an d directly involve paren t or crit ical col
th e dist al M1 proxim al to t h e origin of th e an eu r ysm redu ces lateral vessels. Alternative treatm ent strategies include proxim al
ar terial pressure, soften s th e dom e, an d redu ces th e risk of rup vessel occlusion , an eur ysm t rapping, an d revascularizat ion tech
t u re du ring clip ping. n iqu es.26,48,49,51 Preop erat ive an giograp hy, augm en ted by t h ree
With gian t an eu r ysm s (> 25 m m ), m ore exten sive tem porar y d im en sion al recon st r u ct ion , m u st be carefu lly review ed before
clipp ing is u su ally n ecessar y. In addit ion to M1, all bran ch es dis deciding u pon th e appropriate t reat m en t altern at ive.
tal to th e an eu r ysm can be occlu ded, effect ively devit alizing th e If collateral circu lat ion is presen t , en dovascu lar paren t ar ter y
an eur ysm (Fig. 48.8). For n on calcified gian t an eur ysm s, 2 to 5 occlusion m ay aver t m ore invasive t rapping or revascularizat ion
m in utes of total occlusion is usu ally su fficien t to open th e dom e, tech n iques. Tem porar y balloon test occlusion sh ould be used in
collap se th e an eu r ysm , an d ap ply defin it ive clips. With calcified addit ion to angiography to bet ter delin eate collateral circulat ion
or th rom bosed an eu r ysm s, th e required occlu sion t im e m ay sig an d appreciate th e fun ct ion al con sequen ces of paren t vessel oc
n ifican tly in crease. Even if th e dom e is cut open , th e fun du s m ay clusion. Im portantly, no available diagnostic technique can predict
n ot collapse an d th e calcium an d/or th rom bus m ay h ave to be th e con sequ en ces of perm an en t vessel occlu sion w ith com plete
evacuated prior to clipping. An ult rason ic aspirat ion device (Ca fidelit y.52 An eu r ysm s con t in u e to fill th rough ret rograde collat
vit ron [Valleylab, Bou lder, CO]) m ay be n ecessar y to rem ove solid eral flow follow ing paren t ar ter y occlu sion , bu t h em odyn am ic
debris w ith in th e dom e. An en dar terectom y of th e n eck region to ch anges m ay be su fficien t to cat alyze an eu r ysm th rom bosis an d
rem ove calciu m is rarely u sed to prepare th e n eck for clip ping. resolu t ion (Fig. 48.9).53 Treat m en t effect s m ay n ot be p er m a
Historically, in ext rem ely rare cases w h en an eu r ysm size an d n en t an d spon tan eous revascularizat ion of previou sly th rom
com p lexit y dict ated th at m ore th an 10 m in u tes of occlu sion w as bosed an eur ysm s h as been repor ted.54 Surgical or en dovascular
exp ected, deep hyp oth erm ic circu lator y arrest w as at tem pted to t rapp ing of in tracran ial an eu r ysm s con sists of vessel occlu sion
decrease cerebral m etabolism an d im prove isch em ic toleran ce.45 both proxim al an d dist al to th e an eur ysm , th us elim in at ing both
Im por t an tly, evolving en dovascu lar sten t ing an d coiling tech p r im ar y filling an d ret rograd e flow . As th e t rap p ed segm en t of
n iques, m odern im aging m odalit ies, an d in n ovat ive cerebral re t h e vessels is com p letely cu t off from circu lat ion , t h is st rategy
vascu larizat ion st rategies, h ave essen t ially elim in ated th e use of is n ot applicable if im por t an t vessels or perforators are in close
deep hypoth erm ic circu lator y arrest for MCA an eu r ysm s. proxim it y to th e an eur ysm .
Revascu larizat ion tech n iqu es m ain tain dist al p erfu sion in a
vessel th at con t ain s an un clippable an eur ysm an d lacks adequate
Clip Inspection
collateral circu lat ion distally. Variou s repor ts h ave detailed dif
On ce fin al clipp ing h as been ach ieved, it is im perat ive to in spect feren t revascu lar izat ion tech n iqu es em p loyed to t reat gian t fu
th e clip or clip s carefu lly to en su re th at am ple room h as been left siform an eur ysm s of th e MCA. Alth ough th e detailed tech n ical
for blood flow th rough th e MCA bifu rcat ion an d th at n o m ajor n uan ces of each approach are beyon d the scope are of th is ch ap
bran ch h as been com p rom ised . Th e t ip s of t h e clip n eed to be ter, several key poin t s are im por t an t to con sider w h en evaluat ing

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566 V Cerebral and Spinal Aneurysms

a c e

b d f

Fig. 48.9a–f Preoperative studies of a giant fusiform right m iddle cere- bosed spontaneously following extracranial-intracranial bypass using the
bral artery (MCA) aneurysm of the M1 segm ent. (a) Coronal contrast- saphenous vein. The authors hypothesize that aneurysm throm bosis was
enhanced T1-weighted m agnetic resonance im aging (MRI) scan. (b) Axial caused by a decreased rate of blood flow in the aneurysm following bypass.
T2-weighted MRI im age. (c,d) Three-dim ensional computed tom ography More than 10 years after surgery, this patient continues to be m onitored
(CT) angiograms. (e,f) Digital subtraction angiograms. (Reprinted with per- but has not required further surgical m anagem ent.
mission of AANS from the Journal of Neurosurgery.53 ) The aneurysm throm -

com plex MCA aneur ysm s. MCA revascularization is generally per results.56,57 Sanai et al50 described an evolution from extracranial
form ed via a traditional pterional transsylvian approach, w h ich in t racran ial (EC IC) to in t racran ial in t racran ial (IC IC) bypasses
can be augm en ted by an exten ded orbitozygom at ic cran iotom y.48 for th e t reat m en t of com plex in t racran ial an eur ysm s. In th eir
If a bypass is con sid ered at all likely, th e graft m u st be prepared clin ical series, in sit u revascu larizat ion con st r u ct s based on th e
w ell before th e t im e it is n ecessar y. Com m on byp ass tech n iqu es rean astom osis an d reim plan t at ion of en t irely in t racran ial graft s
involve m obilizing a bran ch of th e extern al carot id ar ter y, m ost (IC IC) resulted in sim ilar rates of aneur ysm obliteration and graft
often th e su perficial tem p oral ar ter y (STA) or occipital ar ter y, for paten cy an d led to im proved n eu rologic ou tcom e w h en com
an astom osis w ith th e MCA.55 W h en perform ing a cran iotom y for pared w ith t radit ion al EC IC grafts.49
any MCA an eur ysm , th e STA sh ould be preser ved in th e even t
t h at an u np red icted STA MCA byp ass is called for. W h en fash
ion ing sm all caliber, low flow revascularization s, n eu rosurgeon s
sh ou ld con sider th e p ossibilit y th at flow th rough th e su rgically
con st r u cted byp ass graft w ill in adequ ately rep lace origin al per
■ Conclusion
fusion p rovided by th e sacrificed proxim al vessel. Our evolving un derst an ding of th e n at ural h istor y of in t racran ial
High er caliber con d u its, in clu ding h ar vested segm en t s of th e an eur ysm s an d th e expan ding applicat ion of en dovascu lar th er
saph en ou s vein or radial ar ter y, offer th e p oten t ial for revascu apies h as h ad a profoun d im pact on th e t reat m en t of cerebral
larizat ion w ith greater collateral flow. Th ese h igh flow graft s an eur ysm s in recen t years. In th e t reat m en t of MCA an eur ysm s,
can also be in terp osit ion ed to bypass diseased segm en t s of large m icrosurgical clip ligat ion con t in ues to be th e stan dard of care.
vessels. Direct side to side anastom osis of M2 vessels can also be Advan ces in both technology and techn ique have dram at ically im
ach ieved if on e vessel h as been occluded an d can n ot be effec proved outcom e in MCA aneur ysm surgery sin ce th e pion eering
t ively revascu larized.48 Rep or ts h ave also described th e direct w ork of Dot t 6 and Dan dy.7 Nevertheless, com plex MCA aneur ysm s
excision of gian t an eu r ysm s at th e MCA bifu rcat ion w ith m obili con t in u e to ch allenge m icrosu rgeon s to develop an d em p loy
zat ion an d rean astom oses of involved vessels w ith good clin ical som e of th e m ost com plex tech n iqu es in m odern n eurosu rger y.

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Hem orrh age. A Cooperat ive St udy. Ph iladelph ia: Lippin cot t; 1969 rupt ured in t racran ial an eur ysm s. J Neurosurg 1960;17:762–777

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3. Sun dt T. Par t I. Basic Con siderat ion s: Basic Prin ciples an d Tech n ique. Bal 29. Salgado AV, Furlan AJ, Keys TF. Mycot ic an eur ysm , subarach n oid h em or
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41–50 r ysm s. In : Le Rou x PD, Win n HR, New ell D, eds. Man agem en t of Cerebral
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r ysm s: a con t rolled t rial of con ser vat ion an d surgical t reat m en t of rup 36. Kom ot ar RJ, Mocco J, Solom on RA. Guidelin es for th e su rgical t reat m en t
t ured an eur ysm s of in ternal carot id ar ter y at or n ear th e poin t of origin of of un r upt ured in t racran ial an eur ysm s: th e first an n ual J. Law ren ce Pool
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12. Hook O, Norlen G. An eur ysm s of th e m iddle cerebral ar ter y: A repor t of sm all arteriovenous m alform ation s. J Neurosurg 1991;75:40–44
80 cases. Act a Ch ir Scan d Su p p l 1958;235:1–39 38. Molyn eu x A, Kerr R, St rat ton I, et al; In tern at ion al Subarach n oid An eu
13. Robin son RG. Rupt ured an eur ysm s of th e m iddle cerebral ar ter y. J Neuro r ysm Trial (ISAT) Collaborat ive Grou p. In ternat ion al Subarach n oid An eu
surg 1971;35:25–33 r ysm Trial (ISAT) of n eurosurgical clipping versus endovascu lar coiling in
14. Yaşargil MG, Fox JL. Th e m icrosu rgical ap p roach to in t racran ial an eu 2143 pat ien t s w ith r upt ured in t racran ial an eur ysm s: a ran dom ised t rial.
r ysm s. Surg Neu rol 1975;3:7–14 Lan cet 2002;360:1267–1274
15. Drake CG. On th e surgical t reat m en t of r upt ured in t racran ial an eur ysm s. 39. McDougall CG, Spet zler RF, Zabram ski JM, et al. Th e Barrow Ru pt u red An
Clin Neurosurg 1965;13:122–155 eur ysm Trial. J Neu rosurg 2012;116:135–144
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m un icat ing an eur ysm s. Clin Neurosurg 1974;21:151–165 n ial an eur ysm s. Neurosurg Focus 2004;17:E2
17. Su zuki J, Yosh im oto T, Kayam a T. Surgical t reat m en t of m iddle cerebral 41. Regli L, Deh dash t i AR, Uske A, de Tribolet N. En dovascu lar coiling com
ar ter y an eu r ysm s. J Neu rosu rg 1984;61:17–23 pared w ith su rgical clipp ing for th e t reat m en t of u n ru pt u red m idd le cere
18. Wilson CB, Spet zler RF. Operat ive approach es to an eur ysm s. Clin Neuro bral ar ter y an eu r ysm s: an u pdate. Act a Neu roch ir Su p pl (Wien ) 2002;82:
surg 1979;26:232–247 41–46
19. Sym on L. Surgical m an agem en t of m iddle cerebral arter y an eur ysm s. In : 42. Spet zler RF, Lee KS. Reconst ruct ion of th e tem poralis m uscle for the pteri
Sch m idek H, Sw eet W, eds. Operat ive Neurosurgical Techn iques: In dica on al cran iotom y. Tech n ical n ote. J Neurosu rg 1990;73:636–637
t ion s, Meth ods an d Result s, vol 2. Ph iladelph ia: 1982:891–908 43. Solom on RA, On est i ST, Kleban off L. Relat ion sh ip bet w een th e t im ing of
20. Heros RC, Ojem ann RG, Crow ell RM. Superior tem poral gyru s approach to an eu r ysm su rger y an d th e develop m en t of delayed cerebral isch em ia.
m iddle cerebral ar ter y an eur ysm s: tech n ique an d result s. Neu rosurger y J Neu rosurg 1991;75:56–61
1982;10:308–313 44. Yaşargil MG. Microneu rosurger y, vol 2. Clin ical con siderat ion s, Surger y of
21. Gibo H, Car ver CC, Rh oton AL Jr, Len key C, Mitch ell RJ. Microsurgical an at In t racran ial An eur ysm s, and Result s. St ut tgar t: Georg Thiem e; 1984
om y of th e m iddle cerebral ar ter y. J Neurosurg 1981;54:151–169 45. Mack W J, Ducruet AF, Angevin e PD, et al. Deep hypoth erm ic circulator y
22. Mason A, Caw ley C, Barrow D. Surgical m an agem en t of m iddle cerebral arrest for com plex cerebral an eu r ysm s: lesson s learn ed. Neurosu rger y
ar ter y an eu r ysm s. In : Win n HR, Con n olly ES, Meyer FB, Sp et zler RF, ed s. 2007;60:815–827, discussion 815–827
You m ans Neurological Su rger y, vol 4. Ph iladelph ia: Elsevier Saun ders; 46. Alexan der TD, Macdon ald RL, Weir B, Kow alczu k A. In t raoperat ive angi
2011:3862–3870 ography in cerebral aneu r ysm surger y: a prospect ive st udy of 100 cran i
23. Heros RC, Frit sch MJ. Surgical m an agem en t of m iddle cerebral arter y an otom ies. Neu rosu rger y 1996;39:10–17, discu ssion 17–18
eur ysm s. Neurosurger y 2001;48:780–785, discussion 785–786 47. Raabe A, Nakaji P, Beck J, et al. Prosp ect ive evalu at ion of su rgical
24. Rinn e J, Hern esn iem i J, Niskan en M, Vapalah t i M. An alysis of 561 pat ien t s m icroscope in tegrated int raoperat ive near in frared in docyan in e green
w it h 690 m id d le cerebral ar ter y an eu r ysm s: an atom ic an d clin ical fea videoangiography du ring an eur ysm surger y. J Neu rosurg 2005;103:982–
t u res as cor related to m an agem en t ou tcom e. Neu rosu rger y 1996;38: 989
2–11 48. San ai N, Law ton MT. Microsurgical m an agem en t of gian t in t racran ial an
25. Flam m E, Fein J. Middle cerebral ar ter y aneur ysm s. In : Fein J, Flam m E, eur ysm s. In : Youm an s Neurological Surger y, vol 4, 6th ed. Ph iladelph ia:
eds. Cerebrovascu lar Surger y. New York: Springer Verlag; 1985;861–877 Elsevier Saun ders; 2011
26. Kalan i MY, Zabram ski JM, Hu YC, Spet zler RF. Ext racran ial in t racran ial 49. Law ton MT, Spet zler RF. Surgical st rategies for gian t in t racran ial an eu
byp ass an d vessel occlusion for th e t reat m en t of un clippable gian t m iddle r ysm s. Neurosurg Clin N Am 1998;9:725–742
cerebral ar ter y an eur ysm s. Neurosurger y 2013;72:428–435, discussion 50. San ai N, Zador Z, Law ton MT. Bypass surger y for com plex brain an eu
435–436 r ysm s: an assessm en t of in t racran ial in t racran ial bypass. Neurosurger y
27. Carpen ter M, Sut in J. Hum an Neuroan atom y, 8th ed. Balt im ore: William s 2009;65:670–683, discussion 683
& Wilkin s; 1983 51. Can tore G, San toro A, Guidet t i G, Delfin is CP, Colon n ese C, Passacan t illi E.
28. Ferguson GG. Physical factors in the initiation, grow th, and rupture of hum an Surgical t reat m en t of gian t in t racran ial an eur ysm s: curren t view poin t .
in t racran ial saccu lar an eur ysm s. J Neurosurg 1972;37:666–677 Neurosurger y 2008;63(4, Suppl 2):279–289, discu ssion 289–290

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52. Standard SC, Ahuja A, Guterm an LR, et al. Balloon test occlusion of the in in ferior cerebellar ar teries for ver tebrobasilar in su fficien cy. J Neurosurg
ternal carotid artery w ith hypotensive challenge. AJNR Am J Neuroradiol 1990;72:554–558
1995;16:1453–1458 56. Ceylan S, Karakuş A, Du r u S, Baykal S, Ilbay K. Recon st ru ct ion of th e m id
53. Haqu e R, Kellner C, Solom on RA. Spon t an eous th rom bosis of a gian t fusi dle cerebral ar ter y after excision of a gian t fu siform an eu r ysm . Neu rosu rg
form aneu r ysm follow ing ext racran ial in t racran ial bypass surger y. J Neu Rev 1998;21:189–193
rosurg 2009;110:469–474 57. Hadley MN, Spet zler RF, Mar t in NA, Joh n son PC. Middle cerebral ar ter y
54. Lee KC, Joo JY, Lee KS, Shin YS. Recan alizat ion of com pletely th rom bosed an eur ysm due to Nocardia asteroides: case repor t of an eur ysm excision
gian t an eur ysm : case report . Su rg Neurol 1999;51:94–98 an d ext racran ial in t racran ial byp ass. Neu rosu rger y 1988;22:923–928
55. Ausm an JI, Diaz FG, Vacca DF, Sadasivan B. Su perficial tem poral an d oc
cipit al arter y bypass pedicles to superior, an terior in ferior, an d posterior

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49 Endovascular Therapies for Middle
Cerebral Artery Aneurysms
Jorge L. Eller, Travis M. Dum ont, Grant C. Sork in, Maxim Mok in, Kenneth V. Snyder,
L. Nelson Hopk ins, Adnan H. Siddiqui, and Elad I. Levy

En dovascu lar t reat m en t of m iddle cerebral ar ter y (MCA) an eu cases. An eu r ysm s arising in th e dist al MCA arterial t ree (beyon d
r ysm s rep resen t s a t r u e fron t ier in th e field of en d ovascu lar th e bifu rcat ion ) are u n com m on an d often associated w ith t rau
n eu rosu rger y. Desp ite in creasing accept an ce by th e n eu rosu r m at ic or in fect iou s et iologies.
gical com m u n it y of en dovascular em bolizat ion as th e preferred Th e m ost com m on MCA an eu r ysm s—th ose origin at ing at th e
t reat m en t st rategy for m ost in t racran ial an eu r ysm s sin ce th e MCA bifu rcat ion —m ay h ave a w ell d efin ed n eck th at is sepa
pu blicat ion of th e In tern at ion al Su barach n oid An eu r ysm Trial rated from th e MCA bran ch es (su perior an d in ferior t ru n ks, or
(ISAT),1 MCA an eu r ysm s rem ain t reated p rim arily by su rgical M2 bran ch es) or h ave on e or both bran ch es in corp orated in to or
clip ping. Several factors con t ribu te to th e rat ion ale for th is t reat ar ising from th e n eck. An ot h er p ossible scen ar io is to h ave on e
m en t strategy, in clu ding th e part icular an atom ic ch aracterist ics or m ore bran ch es arising from th e an eur ysm sac. Th ese an a
of th ese an eur ysm s (w h ich often h ave w ide n ecks an d bran ch es tom ic variat ion s, associated w ith th e par t icular angulat ion w ith
arising from th e n eck), a perceived long reach for en dovascular w h ich th e M2 bran ch es arise from th e M1 paren t vessel, h ave
cath eters an d devices, an d th e relat ive proxim it y of th ese an eu sign ifican t im p licat ion s w ith resp ect to th e feasibilit y an d safet y
rysm s to the cerebral surface (w hich facilitates surgical exposure). of en d ovascular in ter ven t ion s.
Moreover, MCA an eu r ysm s w ere sign ifican tly u n derrep resen ted Several an atom ic ch aracterist ics of MCA an eu r ysm s are con
in th e ISAT st u dy, w h ich u n derscores th e percept ion th at th ese sidered u n favorable for en dovascu lar in ter ven t ion , su ch as th e
lesion s do n ot offer t ru e clin ical equip oise for ran dom izat ion be presen ce of any of th e follow ing: MCA t rifu rcat ion in stead of a
t ween surgical and endovascular treatm ent and are better treated bifurcat ion , w ide n eck leading to a dom e to n eck rat io of < 2,
by su rgical ap proach es. paren t vessel (M1) sten osis, an d bran ch vessels arising from th e
As th e en dovascu lar arm am en t ariu m of devices an d tech an eur ysm n eck or sac.6 Th ese feat u res con t ribu te tow ard deter
n iqu es con t in ues to evolve at an in credible pace, som e of th ese m in ing w h at is con sidered a com p lex MCA an eu r ysm from an
assum pt ion s are being ch allenged by recen t literat ure repor ts en dovascu lar t reat m en t st rategy st an dp oin t an d, w h en presen t ,
describing safe and effective en dovascular t reatm ent strategies for favor an op en surgical approach to th ese lesion s.
MCA an eu r ysm s.2–4 Fu r th er tech n ical developm en ts in th e field
th at can be an t icipated in t h e n ear fu t u re are likely to m ake th e
case for en d ovascu lar t reat m en t even m ore com p ellin g. Th is
ch apter review s p er t in en t an atom ic, clin ical, rad iological, an d ■ Pathophysiology and Natural History
tech n ical asp ect s of con tem p orar y en d ovascu lar t reat m en t of
Invest igators h ave at tem pted to est im ate th e prevalen ce of un
MCA an eu r ysm s an d illu st rates d ifferen t en d ovascu lar tech
rupt ured in t racran ial an eur ysm s, w ith n u m bers var ying from 1
n iqu es t h at m ay be u sed to t reat eit h er M1 segm en t or bifu rca
to 2%7 to up to 5 to 10%8 of th e popu lat ion , depen ding on th e
t ion MCA an eu r ysm s th rough case p resen tat ion s.
m eth odology, st u dy design , an d populat ion st udied. Th e risk of
rupt ure of any par t icular in t racran ial an eur ysm is th e m ost cru
cial factor in determ in ing th e n eed for t reat m en t , eith er su rgical
or en dovascular. An eur ysm size an d locat ion h ave been th e t w o
■ Relevant Anatomy m ost im p or t an t d eter m in an t s of r isk of r u pt u re accord in g to
Th e MCA is th e th ird m ost com m on site of in t racran ial an eu r ys t h e In tern at ion al St u dy of Un ru pt u red In t racran ial An eu r ysm s
m al h em orrh age, an d MCA an eur ysm s accoun t for 20% of all in (ISUIA).9 More recen tly, oth er m orph ological factors, such as as
t racran ial an eu r ysm s.5 Moreover, pat ien ts w ith MCA an eur ysm s pect rat io, an eu r ysm angle, vessel angle, an d size rat io, h ave been
are m ore likely to h ave addit ion al an eu r ysm s elsew h ere in th e invest igated as poten t ial predictors of rupt u re risk.10–12 Lin et al13
in t racran ial circu lat ion . MCA an eu r ysm s m ay arise from th e h or evalu ated several geom et ric param eters in MCA an eur ysm s an d
izon t al (M1) por t ion of th e MCA (in 12% of cases), from th e MCA d eter m in ed t h at asp ect rat io (rat io of t h e m a xim u m p er p en
bifurcat ion (in 83%), from a secon dar y MCA bifurcat ion (in 3%), d icu lar h eigh t of th e an eu r ysm to t h e average an eu r ysm n eck
or from MCA bran ch es fu r th er dist ally (in 2%).5 An eur ysm s aris- d iam eter), flow an gle (an gle bet w een th e vectors of m a xim u m
ing from th e M1 port ion m ay be located at th e origin of th e tem an eur ysm h eigh t an d th e cen terlin e of th e paren t vessel) an d a
poropolar ar ter y, th e origin of th e an terior tem poral ar ter y, a new ly defined param eter, the paren t–daughter vessel angle (angle
com m on t r u n k for m ed by t h e ju n ct ion of t h ese t w o ar ter ies, for m ed bet w een vectors of flow th rough th e paren t vessel an d
or t h e or igin of t h e lateral len t icu lost r iate ar ter ies.5 MCA bifu r- daugh ter vessels) w ere associated w ith in creased rupt ure risk.
cat ion an eu r ysm s m ay h ave len t icu lost r iate bran ch es ar isin g Th e paren t–daugh ter vessel angle is a variable th at describes
in close proxim it y to th e n eck of th e an eur ysm in up to 22% of the context of the cerebral vasculat ure surroun ding th e aneurysm

569

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570 V Cerebral and Spinal Aneurysms

an d m easures th e degree of deviat ion of blood flow bet w een th e r ysm s t reated by sten t assisted coil em bolizat ion , Field s et al 2
p aren t vessel an d resp ect ive daugh ter vessel(s).13 In t h e st u dy est im ated th at 30% of MCA an eur ysm s referred for en dovascular
con d u cted by Lin et al,13 a sm aller p aren t– daugh ter an gle w as t reat m en t w ere deem ed u n su itable on th e basis of an atom ic fea
sign ifican t ly associated w it h a h igh er r isk of r u pt u re for MCA t ures fou n d on th e in it ial diagn ost ic angiogram .
an eu r ysm s. As w ill be discussed in greater detail in subsequen t We h ave fou n d th at th e abilit y to p erform en dovascu lar p ro
sect ion s, th e p aren t–daugh ter vessel(s) angle is also an im por ced u res u n d er local an est h esia an d m od erate sedat ion great ly
tan t factor in determ in ing th e feasibilit y of en dovascular t reat m in im izes t h e card iovascu lar an d p u lm on ar y r isks t h at are
m en t st rategies for MCA an eu r ysm s. p ossibly associated w ith an open surgical procedure. Both un
rupt ured an d selected low Hun t Hess grade r upt ured an eur ysm s
can be safely an d effect ively t reated en dovascu larly in th is fash
ion ,19,20 allow ing direct evalu at ion of th e pat ien t’s clin ical an d
■ Clinical Presentation n eu rologic st at us th rough out th e p rocedu re.
Th e use of self exp an ding in t racran ial sten t s h as greatly ex
Th e clin ical presen t at ion of pat ien t s w ith u n ru pt u red MCA an
ten ded th e scope of t reat m en t of an eu r ysm s th at are am en able
eu r ysm s m ay in clu de h eadach es, isch em ic even t s in th e territor y
to en dovascular coil em bolizat ion . Given th e in h eren t th rom bo
dist al to th e an eu r ysm , an d seizu res.14 Ru pt u red MCA an eu r ysm s
gen icit y associated w ith such sten ts, pat ien t s are placed on dual
are som ew h at u n ique am ong an terior circulat ion an eur ysm s be
an t iplatelet th erapy (usually aspirin an d clopidogrel) for at least
cau se t h ese p at ien t s m ay p resen t n ot on ly w it h classic d iffu se
3 m on th s p ost im plan tat ion , follow ed by lifelong aspirin th erapy.
su barach n oid h em or rh age (SAH) bu t also w it h localized in t ra
Therefore, as part of preprocedure planning, careful consideration
paren chym al or in t rasylvian h em orrh age. Ou tcom es of pat ien ts
m ust be given to any con t rain dicat ion s to an t iplatelet th erapy
w ith ru pt ured MCA an eur ysm s w ere repor ted to be w orse th an
(such as hypersen sit ivit y or gast roin test in al bleeding) to deter
th ose of p at ien t s w ith oth er an terior circu lat ion an eu r ysm s,15
m in e the feasibilit y of th e prop osed en dovascular procedure.
an d it w as post ulated th at th is differen ce m ay be accoun ted for
by th e h igh er frequen cy of ru pt ured MCA an eur ysm s associated
w ith in t raparen chym al h em atom as. Most of th ese h em atom as
are located in th e tem poral lobe, an d th e est im ated in ciden ce of
su ch MCA an eu r ysm –related in t raparen chym al h em atom as var
■ Endovascular Approaches
ies from 35 to 55%.16–18 In a ret rosp ect ive review of 92 p at ien t s and Techniques
w ith r upt u red MCA an eu r ysm s t reated su rgically, Yosh im oto et
An atom ic con siderat ion s are of th e ut m ost im por tan ce w h en
al18 fou n d th at p at ien ts p resen t ing w ith diffu se SAH h ad a less
considering endovascular treatm ent of MCA aneurysm s. We con
severe Hu n t Hess grad e at p resen t at ion an d m u ch bet ter ou t
sider t w o an atom ic feat u res of p rin cip al im por t an ce w h en de
com e t h an p at ien t s p resen t in g also w it h in t rap aren chym al or
term in ing w h eth er an MCA an eur ysm is am en able to en dovas
in t rasylvian h em or rh age. In t h ese lat ter grou p s, h igh er clin ical
cular t reat m en t an d w h ich devices are required for t reat m en t.
grade on adm ission an d larger h em atom a diam eter w ere sign ifi
Th ese t w o feat u res are th e an eu r ysm dom e to n eck rat io an d
can tly correlated w ith w orse ou tcom es.
th e angu lat ion of th e daugh ter vessels (MCA t r u n ks) com pared
W h et h er t h e in t rap aren chym al h em atom a n eed s to be su r
w ith th e paren t vessel (M1). An eur ysm s w ith un favorable (< 2:1)
gically evacu ated dep en ds on th e size of th e h em atom a an d th e
dom e to n eck rat io w ill t yp ically requ ire n eck recon st r u ct ion
severit y of th e corresp on ding m ass effect u p on deep cerebral
for t reat m en t . Un favorable (acu te angle) angulat ion bet w een th e
st r uct u res. If h em atom a evacu at ion is n ecessar y, th e associated
paren t an d daugh ter vessels m akes sten t deliver y m ore difficu lt .
MCA an eu r ysm sh ou ld be su rgically clip ped in th e sam e op era
With th ese an atom ic con siderat ion s at th e forefron t , on e can
t ion , p reclu ding en d ovascular t reat m en t .
consider five basic MCA bifurcation aneur ysm configurations that
m ay be en coun tered (Fig. 49.1), each w ith d ifferen t t reat m en t
approach es an d at ten dan t risks. Th ese five MCA bifu rcat ion an
eur ysm m orph ologies an d th e correspon ding en dovascular
■ Perioperative Evaluation st rategies used for th eir t reat m en t are described in det ail below.
Give n t h e p ar t icu lar an at om ic an d clin ical feat u res of MCA
an eu r ysm s described above, app rop riate p at ien t select ion for
en d ovascu lar t reat m en t is of p aram ou n t im por t an ce. Carefu l ap MCA Bifurcation Aneurysm Morphologies
preciat ion of th e angioarch itect u re an d u t ilizat ion of rotat ion al and Respective Endovascular Technical
t h ree d im en sion al (3D) an giograp hy are essen t ial for p recise Considerations
evalu at ion of th e an eur ysm n eck, sac, an d sh ape an d it s relat ion
Type I: Favorable Dome -to -Neck Ratio (≥ 2:1) ( Fig. 49.1 )
sh ip to th e p aren t an d daugh ter vessels p rior to ch oosing a sp e
cific t reat m en t p lan , eith er su rgical or en dovascular. For pat ien ts w ith MCA an eu r ysm s w ith a favorable dom e to
Th e feasibilit y of obt ain ing a tech n ically an d radiograph ically n eck rat io, prim ar y coil em bolizat ion is our preferred t reat m en t ,
su ccessfu l resu lt w it h en d ovascu lar em bolizat ion of an MCA p ar t icu larly in t h e set t ing of SAH.21–23 Un com p licated coil em
an eur ysm depen ds prim arily on th e abilit y to obtain an angio bolizat ion is t ypically st raigh tfor w ard, requiring sim ple cath eter
grap h ic w orkin g view t h at sh ow s t h e an eu r ysm n eck w it h ou t system s for t reat m en t . We t yp ically em ploy a 6 Fren ch (F) gu ide
su p erim p osit ion of vessels overlying th e n eck; failu re to ach ieve cath eter, w h ich is p laced in th e dist al cer vical in tern al carot id
such a view is th e m ost com m on reason for n ot p roceed ing w ith ar ter y (ICA). A 0.0165 in ch in n er diam eter m icrocath eter is th en
en d ovascu lar t reat m en t . In th eir case series of 23 MCA an eu d irected in to t h e an eu r ysm over a steerable 0.014 in ch m icro

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 571

Fig. 49.1 Five m iddle cerebral artery (MCA) bifurcation aneurysm t ypes vascular treatm ent is considered, a temporary neck reconstruction tech-
classified according to the angulation bet ween parent vessel (M1) and nique (such as balloon-assisted coiling) m ay be favored over placem ent of
daughter vessels (M2 trunks). This classification helps predict the level of a stent, as the acute angle of the daughter vessel m ay result in kinking
difficult y in performing endovascular neck reconstruction of the respective of the stent. Type IV: Wide-necked aneurysm with both daughter vessels at
MCA aneurysm s. Type I: Favorable dom e-to-neck ratio (≥ 2:1). This is an risk, branching from the M1 at an oblique angle. This configuration is also
ideal configuration for prim ary coiling, enabling placem ent of detachable favorable for clip ligation. If endovascular treatm ent is considered, neck re-
coils within the aneurysm with low risk to the daughter vessels (M2 trunks), construction with t wo stents in a Y configuration t ypically provides optimal
which com e off the parent vessel at oblique (> 90-degree) angles. Type II: protection for both at-risk daughter vessels. Type V: Wide-necked aneu-
Wide-necked aneurysm with one daughter vessel at risk, branching from rysm with t wo at-risk daughter vessels, both branching from the M1 at an
the M1 segm ent at an oblique (> 90-degree) angle. This configuration is acute angle. This configuration is favorable for clip ligation and presents the
favorable for endovascular treatm ent with a single neck reconstruction worst possible scenario for endovascular intervention. If endovascular
device (stent) in the at-risk daughter vessel. Type III: Wide-necked aneu- treatment is considered, a “waffle-cone” configuration may provide optimal
rysm with one at-risk daughter vessel branching from the M1 at an acute protection for both at-risk daughter vessels.
(< 90-degree) angle. This configuration is favorable for clip ligation. If endo-

w ire w it h road m ap tech n iqu e an d flu oroscop ic visu alizat ion t ion . We t ypically em p loy a closed cell sten t design ed for th e
th rough ou t . A fram ing coil is selected to m atch th e size of th e in t racran ial vasculat u re an d p lace th e sten t overlying th e an eu
an eur ysm diam eter an d carefully deployed in to th e an eur ysm . r ysm n eck. A 6F guide cath eter is placed in th e distal cer vical or
Prior to det ach ing th e coil, w e p erform angiography to con firm lower petrous carotid artery. A 0.021 inch (for closed cell stent) or
th e good posit ion ing of th e coil w ith in th e an eu r ysm an d th e 0.027 inch (if an open cell stent is used) inner diam eter m icro
paten cy of th e daugh ter vessels. Oth er coils (i.e., fill an d fin ish cat h eter is d irected over a steerable 0.014 in ch or 0.016 in ch
ing) are placed as n ecessar y. flow directed m icrow ire in to posit ion dist al to t h e at risk daugh
In con t rast to an eu r ysm s w ith a favorable dom e to n eck rat io, ter vessel. Th e sten t is th en delivered in to p osit ion by first bring
w id e n ecked t yp es (t yp es II to V) t yp ically requ ire n eck recon ing th e m ost distal port ion of th e n on dep loyed sten t dist al to th e
st r u ct ion , eit h er tem p orar y (balloon assisted) or p er m an en t an eur ysm an d th en u n sh eath ing th e sten t by w ith draw ing th e
(sten t im p lan tat ion ). m icrocatheter until the stent is deployed overlying the aneur ysm
n eck, w ith th e distal sten t segm en t w ith in th e at risk daugh ter
vessel an d th e proxim al sten t segm en t w ith in th e paren t vessel
Type II: Wide -Necked Aneurysm w ith One MCA Trunk at
(M1). We rem ove t h e m icrocat h eter system an d br in g a n ew
Risk, Oblique Angle ( Fig. 49.1 )
0.0165 in ch in n er d iam eter m icrocat h eter system t h rough t h e
Many MCA bifu rcat ion an eu r ysm s are w ide n ecked, an d en d o sten t an d in to th e an eur ysm over a 0.014 in ch steerable m icro
vascular t reat m en t requires n eck recon st r uct ion devices. Th is w ire. Alternatively, this m icrocatheter can be brough t up and into
su bt yp e is th e sim p lest version of a w ide n ecked MCA bifu rca th e an eu r ysm prior to dep loying th e sten t , effect ively “jailing”
t ion an eu r ysm , t ypically requ iring a single sten t for recon st ru c th e coiling m icrocath eter w ith in th e an eu r ysm . A fram ing coil is

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572 V Cerebral and Spinal Aneurysms

then selected to m atch th e an eur ysm diam eter an d delivered into vessels frequen tly en coun tered at th e MCA bifurcat ion , com
th e an eur ysm u n der flu oroscopic visu alizat ion . Addit ion al coils pared w ith presen tly available 4.5 m m closed cell sten ts.
(fill an d fin ish ing) are p laced as n eeded. With placem en t of a single sten t at a vessel bifurcat ion for
Typically, w e favor p lacem en t of a closed cell sten t becau se of t reat m en t of an an eu r ysm w ith on e vessel at risk (t yp e II), w e
th e relat ive ease of deliver y. Th e op en cell sten t presen tly avail t ypically t r y to cu stom ize deliver y of th e sten t to protect both
able for use requ ires a larger deliver y m icrocath eter, w h ich m ay daugh ter vessels. Com p ressing th e part ially deployed sten t in th e
be m ore difficult to bring in to position at th e MCA bifurcat ion . longit u d in al a xis p resses t h e sten t again st t h e bifu rcat ion , t h u s
Th e p rin cipal ben efit of th e presen tly available open cell system allow ing coverage of both daugh ter vessels w it h a single sten t .
is the availabilit y of stents w ith sm aller diam eters (up to 2.5 m m ), Th e n u an ces of th is tech n iqu e, called th e L sten t tech n iqu e, are
w h ich m ay offer a th eoret ical advan t age of a bet ter fit in sm all illu st rated in Fig. 49.2.

Fig. 49.2a–d L-stent technique. (a) The stenting m icrocatheter is in posi- m ovem ent of the m icrocatheter). Friction bet ween the partially deployed
tion in the daughter vessel at greatest risk or easiest to catheterize. The stent and the m icrocatheter causes a deform ation of the partially deployed
stent is advanced through the m icrocatheter into the ideal position over- stent, im proving stent-wall apposition at the aneurysm neck and vessel
lying the aneurysm neck. (b) The distal portion of the stent (a closed-cell bifurcation. (d) The stent is finally fully deployed by unsheathing the m icro-
stent is shown) is deployed by unsheathing the m icrocatheter (arrow). catheter (arrow shows orientation of m ovem ent of the m icrocatheter).
(c) The m icrocatheter is advanced forward (arrow shows orientation of

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 573

Type III: Wide -Necked Aneurysm w ith One MCA Trunk at Because it m ay be difficu lt to t raverse t w o sten t s w ith a m icro
Risk, Acute Angle ( Fig. 49.1 ) cath eter in ten ded for coil deliver y, w e prefer placem en t of th e
coiling m icrocath eter (0.0165 in ch in n er diam eter) in to th e an
Many MCA bifu rcat ion an eu r ysm s h ave r igh t an gle or acu te
eu r ysm an d “jailing” it in place w ith su bsequ en t deliver y of t w o
angle t u rn s bet w een th e paren t an d daugh ter vessels. Th is m or
sten t s. Y sten t con figu rat ion s w ith t w o closed cell sten ts h ave
ph ology m ay be p roblem at ic w h en a sten t is p laced, becau se th e
been described 24 ; h ow ever, w e favor use of on e open cell sten t
sten t m ay n ot p rop erly op p ose t h e vessel w all or m ay d evelop
follow ed by on e closed cell sten t . Each sten t is delivered as de
kin king, w h ich m ay be flow lim it ing or lead to in t ralu m in al
scribed for t yp e II an eu r ysm s. Th e first sten t is p laced in to th e
th rom bosis. To m in im ize sten t kin king, w e con sider em ploying
m ore difficu lt to cath eterize or m ore acu tely angled daugh ter
an open cell sten t , w h ich m ay h ave superior con form at ion to th e
vessel. Th e secon d sten t is p laced t h rough a 0.021 in ch in n er
sh arp t u rn en cou n tered bet w een th e paren t an d daugh ter vessel.
d iam eter m icrocath eter, w h ich is n avigated t h rough a free cell of
Sten t d eliver y an d coiling is p er for m ed w it h a tech n iqu e sim i
th e deployed op en cell sten t . After placem en t of both sten t s, coil
lar to th at described for t reat m en t of t ype II MCA bifurcat ion
em bolizat ion is perform ed th rough th e jailed 0.0165 in ch in n er
an eur ysm s.
diam eter m icrocath eter.
Alter n at ively, t h e r isk of sten t kin kin g m ay be avoid ed by
Balloon assisted coiling m ay be con sidered for t ype IV MCA
t h e u se of a balloon rem od eling tech n iqu e. For th is tech n iqu e, a
bifurcat ion an eur ysm s, alth ough th e fin al con st ru ct m ay be un
t w o m icrocath eter system is em ployed . Th e coiling m icrocath e
st able an d h ern iat ion of coils in to th e p aren t or daugh ter vessels
ter (0.0165 in ch in n er diam eter) is first directed in to posit ion
m ay occu r. If Y sten t in g is n ot p ossible, a “w affle con e” sten t
w it h in t h e an eu r ysm . A con for m able balloon cat h eter is t h en
con st ru ct m ay be con sidered. In th is con st ru ct , a single sten t is
p laced in p osit ion at t h e an eu r ysm n eck an d in to t h e at r isk
placed w ith th e proxim al en d w ith in th e p aren t vessel (M1) an d
daugh ter vessel (jailin g). Th e balloon is in flated u n d er flu oro
dist al en d w ith in th e an eu r ysm dom e. In ou r experien ce, th is
scop ic visu alizat ion , at w h ich p oin t t h e fram ing coil is p laced
con st r u ct is associated w ith a h igh rate of recu rren ce an d sh ou ld
w it h in t h e an eu r ysm . We t yp ically favor a coil t h at is cu be
be avoided.25
sh ap ed (rath er th an ran dom sh ap ed) to avoid h ern iat ion of th e
coil in to th e at risk vessel after th e balloon is rem oved. Balloon
occlusion sh ould last n o m ore th an 5 m in utes to aver t iat rogen ic Type V: Wide -Necked Aneurysm w ith Both MCA Trunks
isch em ic sym ptom s. We rou t in ely p er for m an eu r ysm em boli at Risk, Acute Angle (Fig. 49.1 )
zat ion p rocedu res w ith con sciou s sedat ion (as m en t ion ed) an d
h ave foun d th at pat ien t s develop sym ptom s rap idly, com p rom is En dovascular t reat m en t is essen t ially iden t ical to th at of t ype IV
ing safe an eu r ysm em bolizat ion if coils are n ot placed qu ickly. MCA an eu r ysm s, w ith th e except ion th at posit ion ing t w o sten t s
We size, select , an d p rep are on e fram ing coil an d t yp ically t w o for a Y sten t con figurat ion m ay be ext raordin arily difficult du e to
fill coils prior to balloon occlu sion as a t im e saving m easu re. th e n eed to p lace t w o sten t s w ith acu te angle t u rn s. For th is con
Given t h e com p lexit y associated w it h t reat m en t of t yp e III figurat ion , if en dovascular t reat m en t is desired, a w affle con e
an eur ysm s becau se of at risk vessel an atom y, w e st rongly con sten t con st ru ct m ay be opt im al. We st rongly con sider clipp ing of
sider clip ligat ion of th ese an eu r ysm s u n less th ere is a st rong t ype V an eur ysm s.
con t rain dicat ion to surger y (Table 49.1).

Giant and Fusiform MCA Aneurysms


Type IV: Wide -Necked Aneurysm w ith Both MCA Trunks
Th e su bset of gian t an d fu siform MCA an eu r ysm s w arran t s sp e
at Risk, Oblique Angle ( Fig. 49.1 )
cial at ten t ion . Th ese are t rem en d ou sly ch allenging lesion s to
En dovascu lar t reat m en t of th ese an eu r ysm s is possible, bu t clip t reat , eit h er su rgically or en d ovascu larly. Gian t in t racran ial an
ligat ion sh ou ld be con sidered opt im al t reat m en t u n less th ere is eu r ysm s (an eu r ysm s w ith a diam eter > 25 m m ) h ave a 5 year
a st rong con t rain dicat ion to surger y (Table 49.1). En dovascu lar cum ulat ive rupt ure rate of 40% in th e an terior circulat ion .9 Sur-
t reat m en t of t h is t yp e of an eu r ysm is sim ilar to t h e t reat m en t gical m ortalit y rates rem ain as h igh as 10%; surgical m orbidit y
of t ype II an eur ysm s, w ith th e except ion th at t w o overlapping rates ap proach 30%.26–29 Tradit ion al en dovascu lar tech n iqu es of
sten t s are p laced in a Y sten t con figu rat ion to p rotect bot h prim ar y coiling an d balloon assisted or sten t assisted coiling of
daugh ter vessels, w h ich are at risk of occlu ding if coils m igrate. gian t an eu r ysm s h ave so far been un able to provide a m uch bet
Th is con figu rat ion is t yp ically am on g t h e m ost tech n ically so ter altern at ive, w ith occlusion rates of on ly 57%30 an d an overall
p h ist icated en d ovascu lar con st r u ct s for an eu r ysm t reat m en t . m ortalit y rate var ying bet w een 7.7%30 an d 11%.31,32 Th ese lesion s

Table 49.1 Relative Indications for Endovascular or Surgical Treatment of Middle Cerebral Artery Bifurcation Aneurysms

Factor Favors Endovascular Treatment Favors Surgical Treatment

Subarachnoid hemorrhage Without mass effect With m ass effect requiring craniectomy
Aneurysm neck size Small Wide
Previous craniotomy Ipsilateral
Antiplatelet therapy Contraindication
M1 segment size (length) Short

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574 V Cerebral and Spinal Aneurysms

are often treated w ith a com bination of surgical and endovascular


tech n iques.33,34 Recen tly, flow diversion h as becom e an altern a
t ive t reat m en t m odalit y for gian t an eu r ysm s of th e ICA an d h as
been u sed off label to t reat sim ilar lesion s in t h e p oster ior cir
cu lat ion an d p roxim al MCA ter r itor y.35,36 Th is n ew tech n ology
aim s at redu cing blood flow in side th e aneu r ysm by placing a
h igh m et al con ten t , low porosit y sten t across th e an eur ysm n eck
(or th rough a diseased vessel segm en t in th e case of a fu siform
an eu r ysm ), lead ing to grad u al in t ra an eu r ysm al blood flow
st agn at ion , th rom bosis, an d even t ually at rop hy of th e an eur ysm
itself. Addit ion ally, flow diversion leads to n eoin t im al rem odel
in g of t h e p aren t vessel.37 Becau se it s m ech an ism of act ion is
in depen den t of an eu r ysm size, n eck size, dom e to n eck rat io, or
n eed for den se coil packing, flow diversion seem s w ell suited as
a tech n ique for t reat m en t of large, gian t , w ide n ecked or fusi
form an eur ysm s (Fig. 49.3). Th e m ain lim it ing factor in th e MCA
territor y is th e presen ce of th e len t icu lost riate vessels, w ith th e
associated risk of perforat ing vessel occlusion by th e flow di
ver ter an d con sequ en t st roke. Th is tech n ology is likely to evolve
an d h ave a m ore prom in en t role in th e t reat m en t of dist al bifu r
cat ion an eu r ysm s, in clu ding MCA bifurcat ion an eur ysm s.

■ Illustrative Cases Fig. 49.3 Flow diversion. The drawing depicts a flow diverter (Pipeline,
Covidien Vascular Therapies, Irvine, CA) positioned at the neck of a wide-
Case 1 necked giant m iddle cerebral artery (MCA) (M1) aneurysm . The flow di-
verter aim s at reducing blood flow inside the aneurysm , leading to gradual
A 54 year old w om an p resen ted w it h ver t igo. Evalu at ion by intra-aneurysm al blood flow stagnation and throm bosis. It is well suited for
m eans of m agnetic resonance angiography and com puted tom og large, giant, or fusiform aneurysm s, although it s use in the MCA territory
raphy angiograp hy dem on st rated bilateral MCA an eur ysm s. Th e is off-label because of the risk of comprom ising lenticulostriate perforating
vessels. (Courtesy of Covidien Vascular Therapies, Irvine CA. Pipeline is a
pat ien t w as offered cran iotom y for clip ping bu t refu sed su rger y
trademark of a Covidien Company. © 2013 Covidien.)
du e to a fam ily h istor y of death related to a p reviou s su rgical
procedure. Review of the diagnostic angiogram dem onstrated that
th e left MCA an eu r ysm , arising from th e an terior tem p oral ar
ter y an d m easuring 6 m m in it s longest diam eter, w as am en able MCA bifu rcat ion an eu r ysm (Fig. 49.5a). Treat m en t opt ion s w ere
to prim ary coil em bolization (Fig. 49.4a). The pat ient’s aneur ysm discu ssed in detail w ith th e p at ien t , in clu ding su rgical clip ping
w as su ccessfu lly cath eterized w ith a 0.0165 in ch in n er diam eter w ith or w ith out possible ext racran ial–in t racran ial bypass an d
m icrocath eter over a steerable 0.014 in ch m icrow ire. A single en d ovascu lar sten t assisted coiling. Th e pat ien t ch ose t h e en d o
coil w as deployed to com p letely obliterate t h e an eu r ysm (Fig. vascular opt ion . A 0.021 in ch in n er diam eter m icrocath eter w as
49.4b) w ith out com prom ise of th e paren t vessel. Of n ote, a distal brought up to one of the M2 branch es over a steerable 0.016 inch
access cath eter w as placed in th e proxim al MCA to provide fur m icrow ire w h ile a 0.0165 in ch in n er diam eter m icrocath eter
t h er st abilit y d u r in g m icrocat h eter izat ion an d p r im ar y coilin g w as u sed to cath eterize th e an eu r ysm over a steerable 0.014
of th is an eur ysm .38 Follow u p angiography at 6 m on th s dem on in ch m icrow ire. Th is last m icrocat h eter w as jailed w it h in t h e
st rated n o an eu r ysm residu al or regrow th . an eu r ysm as a closed cell, self expan ding sten t w as deployed,
en com passing th e an eur ysm n eck. Th e an eur ysm w as th en em
bolized using several coils of various sizes, w ith excellen t im m e
Case 2
diate radiological resu lt an d n o com prom ise of th e p aren t vessel
A 51 year old w om an presen ted w ith a n ew on set ton ic clon ic (Fig. 49.5b). Angiograp hy perform ed 3 m on th s later revealed left
seizu re. Evalu at ion revealed m u lt ip le u n r u pt u red in t racran ial M1 an eu r ysm recu rren ce, an d fu r th er recoiling of th is an eu r ysm
aneur ysm s, including a giant left M1 segm ent aneur ysm and a left w as n ecessar y.

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 575

a b

Fig . 49.4a,b Case 1. Digit al subtraction angiographic im ages, left inter- geometry favorable for prim ary coil em bolization. (b) Final angiographic
nal carotid artery (ICA) injection, anteroposterior view. (a) Middle cerebral result after deploym ent of a single coil, with complete obliteration of the
artery (MCA) aneurysm arising from the left anterior temporal artery with aneurysm and no comprom ise of the parent vessel.

a b

Fig . 49.5a,b Case 2. Digit al subtraction angiographic im ages, left inter- (b) Im mediate angiographic result of stent-assisted coiling, with excellent
nal carotid artery (ICA) injection, anteroposterior view. (a) Giant left M1 filling of the aneurysm sac and preservation of the M1 parent vessel. This
segm ent aneurysm . The patient elected to pursue endovascular treatm ent. aneurysm required further coiling because of recurrence (not shown).

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576 V Cerebral and Spinal Aneurysms

Case 3 offered . Given t h e p ar t icu lar geom et r y of t h e p aren t vessel–


an eu r ysm in ter face, balloon assisted coiling w as in d icated . A
A 60 year old w om an presen ted to th e em ergen cy room w ith a 0.0165 in ch in n er diam eter m icrocath eter w as jailed w ith in th e
tran sient ischem ic at tack consisting of righ t hem ibody num bn ess an eur ysm dom e w h ile a com plian t balloon cath eter w as brough t
an d speech difficult ies. Evalu at ion revealed a 5 m m , irregular u p to th e an eur ysm n eck an d in flated (Fig. 49.6b); th e an eu r ysm
left MCA an eu r ysm (Fig. 49.6a). Th e p at ien t ’s m ed ical com or w as th en su ccessfu lly coiled . Up on balloon deflat ion , t h e coil
bid it ies w ere exten sive an d p reclu d ed a safe su rgical ap p roach m ass w as st able w it h in t h e an eu r ysm sac an d n o com p rom ise
to t h is lesion ; m oreover, sh e h ad a p osit ive fam ily h istor y of of th e p aren t vessels w as n ot iced (Fig. 49.6c). Follow u p angiog
r u pt ured in t racran ial an eur ysm s. En dovascular t reat m en t w as raphy h as n ot been perform ed as of th is w rit ing.

a b

Fig. 49.6a–c Case 3. (a) Digital subtraction angiogram , left internal ca-
rotid artery (ICA) injection, anteroposterior (AP) view, dem onstrating an
irregular-appearing left m iddle cerebral artery (MCA) aneurysm . Because
of the patient’s medical com orbidities and positive fam ily history of rup-
tured aneurysms, endovascular treatment was offered. (b) Fluoroscopic
image, AP view, showing the balloon inflated at the aneurysm neck while
the aneurysm sac is filled with coils (balloon-assisted coiling technique).
An inflated compliant balloon is placed at the neck of the aneurysm, while
a previously jailed m icrocatheter is used to coil the aneurysm. (c) Digital
subtraction angiogram , left ICA injection, AP view showing the im m ediate
angiographic result with the coil m ass rem aining within the aneurysm sac,
c without any comprom ise of the parent vessel.

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 577

Case 4 resu scitat ion w as su ccessfu l an d th e surgical in ter ven t ion w as


abor ted. En dovascular t reat m en t at a later date w as th en in di
A 67 year old m an presen ted to th e em ergen cy room w ith acute cated. A sten t assisted coiling st rategy w as ch osen . A closed cell
m ental status changes. Noninvasive im aging studies dem onstrated self expan ding sten t w as deployed in an L sten t con figurat ion
an u n r u pt u red left MCA bifu rcat ion an eu r ysm . A d iagn ost ic (Fig. 49.2) after a 0.0165 in ch in n er diam eter m icrocath eter w as
angiogram con firm ed th e presen ce of a w ide n ecked 5 m m left jailed w ith in th e an eur ysm dom e. Th e an eur ysm w as th en coiled
MCA bifu rcat ion an eu r ysm w ith both M2 bran ch es com ing off successfully, w ith ou t com prom ise of eith er th e paren t vessel or
th e an eu r ysm n eck (t yp e V varian t) (Fig. 49.7a). Open surgical M2 bran ch es, w h ich w ere both p rop erly protected by th e single
t reat m en t w as in dicated. Un for t u n ately, on in du ct ion of gen eral sten t (Fig. 49.7b). Th e 3 m on th follow up angiogram dem on
an esth esia an d prior to t urn ing th e bon e flap, th e pat ien t devel strated no evidence of aneurysm residual or recurrence, com pro
oped severe hypoten sion , culm in at ing in cardiac arrest . Cardiac m ise of MCA bran ch es, or in sten t sten osis or th rom bosis.

a b

Fig . 49.7a,b Case 4. (a) Digit al subtraction angiogram , left internal tal subtraction angiogram, left ICA injection, AP view, dem onstrating the
carotid artery (ICA) injection, anteroposterior (AP) view, showing a wide- im m ediate angiographic results of stent-assisted coiling, using an L-stent
necked left m iddle cerebral artery (MCA) bifurcation aneurysm with both technique. Both daughter vessels were preserved, and no significant aneu-
M2 vessels com ing off the aneurysm neck. The patient was taken to the rysm residual was observed.
operating room for surgical clipping but suffered a cardiac arrest. (b) Digi-

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578 V Cerebral and Spinal Aneurysms

a b

Fig. 49.8a,b Case 5. (a) Digital subtraction angiogram, left internal carotid (b) Digital subtraction angiography, left ICA injection, AP view, showing
artery (ICA) injection, anteroposterior (AP) view, dem onstrating a large im mediate angiographic result after placing t wo stents in a Y configuration
left m iddle cerebral artery (MCA) bifurcation aneurysm with both M2 ves- to protect both M2s during stent-assisted coiling. There is m inim al aneu-
sels arising from the aneurysm neck. Endovascular treatment was offered rysm neck residual.
because of the patient’s m edical com orbidities and previous craniotomy.

Case 5 n eck residual (Fig. 49.8b). Th is resu lt w as u n ch anged at th e t im e


of 6 m on th follow u p angiography.
A 68 year old m an p resen ted w it h w orsen ing d izzin ess an d
syn cope. Evaluat ion revealed a large left MCA bifurcat ion an eu
r ysm w ith both M2s origin at ing from th e an eur ysm n eck at
Case 6
acute angles (t ype V) (Fig. 49.8a). Th is p at ien t ’s m edical h istor y A 44 year old m an w ith a kn ow n large fusiform left M1 an eu
w as rem arkable for a left sided cran iotom y w ith clip ping of an r ysm , stat u s post clipping at an out side in st it ut ion , presen ted
u n related left ICA an eur ysm , Croh n’s disease for w h ich h e h ad 4 years later w ith progressive regrow th of th is an eur ysm (Fig.
u n dergon e an ileostom y, an d coron ar y ar ter y disease w ith p oor 49.9a,b). Treat m en t opt ion s w ere discu ssed in great det ail, in
ejection fraction. Given these com orbidities, a decision w as m ade clu ding obser vat ion , ext racran ial–in t racran ial bypass follow ed
to proceed w ith en dovascular coil em bolizat ion . Due to th e un fa by t rapping of th e diseased M1 segm en t , or off label u se of flow
vorable geom et r y of th e an eur ysm n eck w ith respect to th e M2 diversion . Th e pat ien t decided to p roceed w ith flow diversion .
bran ch es, a decision w as m ade to place t w o sten ts in a Y con figu- Tw o flow diver ters w ere deployed in an overlapping fash ion , cov
rat ion . Th is w as p ar t ially su ccessfu l becau se d u r in g p lacem en t ering the diseased M1 segm ent, w ithout technical difficulties. Th e
of th e secon d sten t (closed cell sten t) th e previously deployed 3 m on th follow up angiogram revealed com plete involu t ion of
open cell sten t w as dislodged. Despite th is, th e an eur ysm w as th e an eu r ysm (Fig. 49.9c,d) an d excellen t flow diver ter p osit ion
su ccessfu lly coiled u sing cu be sh ap ed coils w ith on ly m in im al ing, w ith ou t eviden ce of in sten t sten osis (Fig. 49.9e).

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 579

a b

c d

Fig. 49.9a–e Case 6. Digital subtraction angiogram , left internal carotid


artery (ICA) injection, anteroposterior (AP) (a) and lateral (b) views, dem -
onstrating a large fusiform left M1 aneurysm , status post–surgical clipping,
now with a large recurrence. Treatm ent options were discussed in great
detail, and a decision was made to proceed with off-label flow diversion to
reconstitute the parent vessel. Three-m onth follow-up digital subtraction
angiogram , left ICA injection, AP (c) and lateral (d) views dem onstrating
complete involution of the aneurysm . The patient rem ains neurologically
intact. (e) Three-dim ensional reconstruction of previous angiographic im -
ages dem onstrating excellent flow diverter–vessel wall apposition and no
e evidence of in-stent stenosis. (Courtesy of Robert D. Ecker, MD.)

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580 V Cerebral and Spinal Aneurysms

■ Clinical Outcomes ■ Conclusion


In a system at ic review of th e literat ure describing en dovascular Endovascular treatm ent strategies and treatm en t results for MCA
t reat m en t of MCA an eu r ysm s con sist ing m ostly of ar t icles pu b an eur ysm s h ave im proved over th e past t w o decades. Never th e
lish ed p r ior to t h e availabilit y of in t racran ial sten t s, Br injikji et less, m ost cen ters st ill adopt a “clip first” policy w h en dealing
al39 described 12 studies encom passing 1,030 aneurysm s, of w hich w ith MCA bifurcat ion an eur ysm s,44,45 given th e su p erficial loca
50% presen ted w ith rupt ure. Overall m orbidit y an d m or talit y t ion of th ese lesion s an d th e relat ive ease of su rgical accessibilit y
rates were 5.1%and 6.0%for un ruptured an d ruptured aneur ysm s, w ith a stan dard pterion al cran iotom y. Moreover, th e associat ion
respect ively. Th e overall rate of com p lete or n ear com p lete oc of ruptured MCA aneur ysm s w ith intraparenchym al hem orrhage
clu sion at 3 m on th s w as 82%. By com p arison , a su m m ar y of six requiring su rgical evacu at ion m akes su rgical clip ping th e obvi
case series of surgical treat m ent of rupt ured and unrupt ured MCA ou s first ch oice in th ese cases.
an eur ysm s described m orbidit y an d m or t alit y rates approxi Th e developm en t of self expan ding in t racran ial sten t s h as ex
m ating 10%.40 pan ded th e range of in t racran ial an eur ysm s am en able to en do
Oth er st udies h ave dem on st rated excellen t resu lt s w ith surgi vascu lar in ter ven t ion . In t racran ial sten ts allow an eur ysm n eck
cal clipp ing of MCA an eu r ysm s. Regli et al41 docu m en ted good or rem odeling an d p reser vat ion of th e p aren t– daugh ter vessel rela
excellen t Glasgow Ou tcom e Scale scores in 88% of 32 pat ien t s t ion sh ip in MCA an eu r ysm s w h ile providing a m ech an ical scaf
un dergoing su rgical clip ping of u n ru pt u red MCA an eur ysm s, fold to perm it successful coil packing of th e an eur ysm sac. Th is
w ith successful occlusion in all cases. Van Dijk et al42 showed th at h as allow ed m any MCA an eu r ysm s th at w ere p reviously con sid
su rgical clipp ing resu lted in good ou tcom es in 80% of 77 ru p ered u n su it able for en dovascu lar t reat m en t to be t reated by coil
t u red an eu r ysm s an d in all 19 u n r u pt u red an eu r ysm s; com plete em bolizat ion w ith a h igh d egree of tech n ical su ccess, low p roce
an eur ysm occlu sion w as fou n d in 89% of pat ien t s. Fin ally, in a du ral risk, an d acceptable du rabilit y. Th e progressive th rom bosis
large series of 339 u n r u pt u red an eu r ysm s in 263 pat ien ts, Mor obser ved in delayed angiograph ic st udies in m any of th ese an eu
gan et al43 dem on st rated an overall surgical m orbidit y an d m or r ysm s dem on st rates th e long term durabilit y of th e sten t–coil
talit y rate of 5%, w ith 95%of pat ien ts ach ieving good or excellen t com bin at ion , an d th e use of sten ts m ay provide an an sw er to th e
outcom e at 6 w eeks after surger y. p roblem of an eu r ysm recu rren ce after prim ar y coiling.
More recen t case series of en dovascu lar t reat m en t of MCA an New devices an d tech n ologies are prom ising to revolu t ion ize
eu r ysm s in clu de resu lt s of n eck rem odeling tech n iqu es, su ch as t h e en d ovascu lar m an agem en t of in t racran ial an eu r ysm s in
stent assisted coiling. Vendrell et al4 described the results of stent gen eral, an d MCA an eu r ysm s in p ar t icu lar. Flow d iversion h as
assisted coil em bolizat ion of 50 MCA an eur ysm s in 47 pat ien ts, already ch anged t h e m an agem en t of large or gian t sid ew all or
w ith a tech n ical success rate of 96%an d m orbidit y rate of 4.3%. In fu sifor m an eu r ysm s of t h e ICA, an d is likely to evolve fu r t h er
th is case series, 20% of p at ien t s develop ed in sten t th rom bosis, w ith th e developm en t of devices th at are m ore su itable for distal
likely secon dar y to in adequ ate an t ip latelet th erapy. In th eir case bifurcat ion an eur ysm s. In addit ion , sten t s m ore ideally suited to
series of 23 con secu t ive p at ien t s un dergoing sten t assisted coil sm aller caliber vessels encountered at the MCA bifurcation, w hich
em bolizat ion for u n r u pt u red MCA an eu r ysm s, Fields et al2 de- are d elivered t h rough sm aller (0.0165 in ch in n er d iam eter)
scribed fou r p erip rocedu ral com p licat ion s (on e in t raprocedu ral m icrocath eters, h ave already sh ow n prom ise in th e t reat m en t of
rupt ure an d th ree isch em ic even t s), n on e of w h ich resu lted in com plex, difficult MCA lesion s.46
perm an en t n eu rologic deficit . Follow u p 12 m on th angiogram s An eur ysm n eck recon st r uct ion devices 47 m ay be a superior
sh ow ed com p lete an eu r ysm occlu sion in 67% of p at ien t s, th e opt ion for m any w ide n ecked MCA bifurcat ion an eur ysm s, in
presen ce of a n eck rem n an t in 17%, an d residu al an eu r ysm al fill particular w hen acute angle t urns bet w een the paren t and daugh
ing in an oth er 17%. An in terest ing fin ding h igh ligh ted by those ter vessels are en coun tered (an eur ysm s t ypes III an d V). New
au th ors is th at bet w een t h e in it ial an d last follow u p angio intra aneurysm al, endosaccular occlusion devices (Fig. 49.10) have
gram s, 50% of an eu r ysm s exh ibited progressive th rom bosis an d also sh ow n prom ise 48–50 an d m ay offer su perior en dovascu lar
on ly 11% develop ed recu rren ce w ith en largem en t at th e base. treatm en t w hen com pared w ith balloon assisted or stent assisted
In a ret rospect ive review of 100 con secu t ive MCA an eur ysm s coiling of w ide n ecked MCA bifu rcat ion an eu r ysm s (an eu r ysm s
t reated by sten t assisted coil em bolizat ion , Joh n son et al3 de- t ypes II to V). Th e p rin cipal advan t age of th ese devices is less
scribed su ccessfu l sten t deploym en t in all cases. Th ere w as on e im planted m aterial w ithin the parent artery, theoretically greatly
case of neurologic m orbidit y and on e death. Six m onth follow up redu cing th e risk associated w ith in t ralum in al th rom bosis an d
angiography in 85 an eur ysm s dem on st rated com plete an eur ysm an t iplatelet th erapy. As th ese n ew er devices becom e available,
occlusion in 90.6% of cases, residual n eck in 3.5%, an d residual MCA an eu r ysm s are likely to be m an aged en d ovascu larly in a
an eur ysm filling in 5.9%. m ajorit y of cases.

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49 Endovascular Therapies for Middle Cerebral Artery Aneurysm s 581

Fig. 49.10a–c New, intra-aneurysmal endosaccular occlusion devices hold


promise as potentially bet ter tools for endovascular management of middle
cerebral artery (MCA) bifurcation aneurysm s. Depicted are the following
devices: (a) PulseRider, (b) Luna, and (c) Web. (a: Courtesy of Pulsar Vascu-
lar, San Jose, CA; b: Courtesy of Covidien Vascular Therapies, Irvine, CA.
Luna is a tradem ark of a Covidien Company. © 2013 Covidien; c: Courtesy
of Sequent Medical, Aliso Viejo, CA.) c

sist an ce. Th e au th ors also th an k Pau l H. Dressel, B.F.A., for prep a


■ Acknow ledgments rat ion of th e illust rat ion s an d Debra J. Zim m er for editorial
Th e au th ors th an k Nell Aron off, M.L.S., at th e Kaleida Health Li assistan ce (both at Un iversit y at Bu ffalo Neu rosurger y).
braries for providing literat u re search an d referen ce ret rieval as

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cases. Surg Neurol 1986;25:6–17 t reat m en t w ith pipelin e em bolizat ion for giant dist al int racran ial an eu
18. Yosh im oto Y, Wakai S, Satoh A, Hirose Y. In t raparenchym al an d in t rasyl r ysm s w ith or w ith out coil em bolizat ion . Neurosurger y 2012;71:E509–
vian h aem atom as secon dar y to ru pt u red m iddle cerebral ar ter y an eu E513, discussion E513
r ysm s: progn ost ic factors an d th erapeu t ic con siderat ion s. Br J Neurosurg 37. D’Urso PI, Lan zin o G, Cloft HJ, Kallm es DF. Flow diversion for in t racran ial
1999;13:18–24 an eu r ysm s: a review. St roke 2011;42:2363–2368
19. Kan P, Jah sh an S, Yash ar P, et al. Feasibilit y, safet y, an d periprocedu ral 38. Hauck EF, Taw k RG, Karter NS, et al. Use of the outreach distal access catheter
com plicat ion s associated w ith en dovascular t reat m en t of selected r up as an intracranial platform facilitates coil em bolization of select intracranial
t ured an eur ysm s un der con sciou s sedat ion an d local anesth esia. Neuro aneurysm s: technical note. J Neurointerv Surg 2011;3:172–176
surger y 2013;72:216–220, discu ssion 220 39. Brinjikji W, Lan zin o G, Cloft HJ, Rabin stein A, Kallm es DF. En dovascu lar
20. Ogilvy CS, Yang X, Jam il OA, et al. Neu roin ter ven t ion al p rocedu res for t reat m en t of m iddle cerebral ar ter y an eur ysm s: a system at ic review an d
u n r u pt u red in t racran ial an eu r ysm s u n d er p rocedu ral sedat ion an d local single center series. Neurosurgery 2011;68:397–402, discussion 402
an esth esia: a large volum e, single center experien ce. J Neurosurg 2011; 40. Horow it z M, Gu pt a R, Gologorsky Y, et al. Clin ical an d an atom ic ou tcom es
114:120–128 after en dovascu lar coiling of m iddle cerebral ar ter y an eu r ysm s: rep or t on
21. Debrun GM, Alet ich VA, Keh rli P, Misra M, Ausm an JI, Ch arbel F. Select ion 30 t reated an eur ysm s an d review of the literat ure. Surg Neu rol 2006;
of cerebral an eu r ysm s for t reat m en t using Guglielm i det ach able coils: th e 66:167–171, discu ssion 171
prelim in ar y Un iversit y of Illin ois at Ch icago exp erien ce. Neu rosu rger y 41. Regli L, Uske A, de Tribolet N. En dovascu lar coil placem en t com p ared w ith
1998;43:1281–1295, discu ssion 1296–1297 surgical clipping for th e t reat m en t of un ru pt u red m iddle cerebral ar ter y
22. Fern an dez Zu billaga A, Guglielm i G, Viñ uela F, Duckw iler GR. En dovascu aneur ysm s: a consecutive series. J Neurosurg 1999;90:1025–1030
lar occlusion of in t racran ial an eur ysm s w ith elect rically det ach able coils: 42. van Dijk JM, Groen RJ, Ter Laan M, Jeltem a JR, Mooij JJ, Met zem aekers JD.
cor relat ion of an eu r ysm n eck size an d t reat m en t resu lt s. AJNR Am J Su rgical clipping as th e preferred t reat m en t for an eur ysm s of th e m iddle
Neuro radiol 1994;15:815–820 cerebral ar ter y. Act a Neuroch ir Wien ) 2011;153:2111–2117
23. Viñ uela F, Duckw iler G, Maw ad M. Guglielm i det ach able coil em bolizat ion 43. Morgan MK, Mah at t an aku l W, David son A, Reid J. Ou tcom e for m idd le
of acu te in t racran ial an eur ysm : perioperat ive an atom ical an d clin ical cerebral ar ter y an eur ysm surger y. Neurosurger y 2010;67:755–761, dis
outcom e in 403 pat ien t s. J Neurosurg 1997;86:475–482 cu ssion 761
24. Roh de S, Ben dszus M, Hart m an n M, Häh n el S. Treat m en t of a w ide n ecked 44. Abla AA, Jah sh an S, Kan P, et al. Result s of en dovascular t reat m en t of m id
an eur ysm of th e an terior cerebral arter y using t w o En terprise sten t s in dle cerebral arter y an eur ysm s after first giving con siderat ion to clipping.
“Y” con figu rat ion sten t ing tech n iqu e an d coil em bolizat ion : a tech n ical Act a Neuroch ir (Wien ) 2013;155:559–568
n ote. Neuroradiology 2010;52:231–235 45. Rodríguez Hernández A, Sughrue ME, Akhavan S, Habdank Kolaczkow ski J,
25. Dum on t TM, Sorkin GC, Snyder KV, et al. On w affle con es an d in vit ro Law ton MT. Curren t m an agem en t of m iddle cerebral ar ter y an eur ysm s:
an alysis of en dovascu lar an eu r ysm t reat m en t . World Neu rosu rg 2013; su rgical resu lt s w it h a “clip first ” p olicy. Neu rosu rger y 2013;72:415–
80:50–52 427
26. Drake CG, Peerless SJ. Giant fusiform in t racran ial an eur ysm s: review of 46. Turner RD, Turk A, Ch au dr y I. Low profile visible in t ralum in al suppor t
120 pat ien t s t reated surgically from 1965 to 1992. J Neurosu rg 1997;87: device: im m ediate ou tcom e of th e first th ree US cases. J Neu roin ter v Su rg
141–162 2013;5:157–160
27. Hau ck EF, Woh lfeld B, Welch BG, W h ite JA, Sam son D. Clipping of ver y 47. Turk A, Turn er RD, Tatesh im a S, et al. Novel an eur ysm n eck recon st ruct ion
large or giant u nrupt ured in t racran ial an eur ysm s in th e anterior circu la device: in it ial experien ce in an exp erim en t al p reclin ical bifu rcat ion an eu
t ion : an outcom e st udy. J Neurosurg 2008;109:1012–1018 r ysm m odel. J Neuroin ter v Surg 2013;5:346–350

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48. Klisch J, Sych ra V, St rasilla C, Liebig T, Fiorella D. Th e Woven En doBridge new in t rasaccular an eur ysm occlusion device. AJNR Am J Neuroradiol
cerebral an eur ysm em bolizat ion device (W EB II): in it ial clin ical experi 2011;32:602–606
en ce. Neuroradiology 2011;53:599–607 50. Tu rk AS, Turn er RD, Ch audr y MI. Evaluat ion of th e Nfocus LUNA, a n ew
49. Kw on SC, Ding YH, Dai D, Kadir vel R, Lew is DA, Kallm es DF. Prelim inar y parent vessel occlu sion device: a com parat ive st udy in a can in e m odel.
resu lt s of th e Lun a an eur ysm em bolizat ion system in a rabbit m odel: a Neurosurger y 2011;69(1, Suppl Operat ive):on s20–on s26

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50 Surgical Therapies for Anterior
Communicating Artery Aneurysms
Salah G. Aoun, Bernard R. Bendok , Tarek Y. El Ahm adieh, Najib E. El Tecle, and H. Hunt Bat jer

Th e an ter ior com m u n icat in g com p lex is d efin ed as t h e com bi- gives birth to a m edian prim it ive ACA th at usually regresses in
n at ion of th e distal port ion of th e A1 segm en ts of th e an terior h um an s, an d is referred to as th e m edian ar ter y of th e corpus
cerebral ar teries (ACAs), th e an terior com m un icat ing ar ter y callosu m . Failu re of th is arter y to regress can resu lt in eith er a
(ACoA), an d th e proxim al segm en t s of th e A2 segm en t of th e t r ip le an ter ior con figu rat ion w it h t h ree A2 bran ch es (2 to 13%
ACAs. Th is com plex h as been repeatedly sh ow n th rough ou t of in dividu als), or th e regression of n orm ally developing lateral
lan dm ark clin ical st u dies to be a com m on site for in t racran ial A2s w it h com p en sator y en largem en t of t h e m ed ian ar ter y of
an eur ysm s form at ion , an d it h osts u p to 39% of in t racran ial an - t h e corpu s callosu m , w h ich is th en referred to as an “azygos” A2
eu r ysm s.1–5 An eur ysm s at th is locat ion display an in creased ten - (< 1 to 9.7% of th e populat ion ).1 An azygos arter y frequ en tly re-
den cy to r upt u re an d are respon sible for debilitat ing m orbid it y su lts in form at ion of an an eu r ysm . Th e A1 segm en ts of th e ACA
an d h igh rates of m or talit y in a relat ively young p op ulat ion .1,5 In also exh ibit frequen t an atom ic variat ion s w ith hypoplasia, apla-
addit ion to th e previously cited epidem iological factors, ACoA sia, du p licat ion , fen est rat ion , or at yp ical cou rse of th e vessels. A
an eur ysm s are located st rategically bet w een m ajor in t racranial hypoplastic (em pirically defined by som e authors as having a di-
vessels, th e opt ic ch iasm an d opt ic n er ves, an d a m u lt it ude of am eter sm aller th an 1.5 m m )10 or aplast ic A1 t r u n k can be fou n d
ext rem ely fragile perforat ing bran ch es th at cou ld resu lt in a w ide in 10% an d 0.26% of th e popu lat ion , resp ect ively.
array of in capacitat ing n eurologic sequ elae, if injured directly by
th e su rgeon or in directly by postop erat ive edem a or vasospasm .
To add to th e com plexit y of ACoA an eu r ysm m an agem en t , th e
an atom y surroun ding th e an terior com m un icat ing com plex can
var y greatly am ong in dividu als 6 an d t h u s requ ires th e t reat ing
■ Surgically Oriented Anatomy of the
su rgeon to be w ell versed in th e su rgical in terp retat ion of diag- Anterior Cerebral Artery Complex
n ost ic im ages, as w ell as surgically experien ced an d m an ually
A1 Segment of the Anterior Cerebral Artery
dexterou s. Th is ch apter p rovides an over view of key factors re-
lat ing to th e em br yology, an atom y, an d ep idem iology of ACoA Th e A1 segm en t of t h e ACA is d efin ed as t h e bran ch t h at for m s
an eur ysm s, an d review s th e basics of th eir preoperat ive, opera- at th e bifurcat ion of th e in tern al carot id ar ter y in th e carot id cis-
t ive, an d en dovascu lar m an agem en t . We also offer su rgical t ip s tern an d en ds at th e ju n ct ion bet w een th e ACA an d th e ACoA.1,6
an d p earls. Th e A1 segm en t direct s an teriorly an d m edially an d en ters th e
cistern of th e lam in a term in alis often en cased by th ick arach n oid
t issu e, w ith p ossible variat ion s in its cou rse u n t il it reach es th e
ACoA. Th e A1-ACoA jun ct ion occurs at th e level of th e opt ic ch i-
■ Surgically Oriented Embryology of asm in approxim ately t w o-th irds of cases an d above th e opt ic
n er ves in on e-th ird of cases. Th e diam eter of th e A1 is usu ally
Anterior Communicating Aneurysms h alf of th at of th e m iddle cerebral ar ter y (MCA). Both A1s are of
Develop m en tal an om alies du ring th e early em br yological st ages th e sam e size in h alf th e cases, an d h ave a differen ce of ≥ 5 m m
of form at ion of th e an terior com m un icat ing com plex can h elp in th e oth er h alf.1,2 Th is is of clin ical an d surgical relevan ce be-
accou n t for th e m u lt iple an atom ic varian ts th at are en cou n tered cau se a discrep an cy is fou n d in th e diam eter of th e A1 segm en ts
in th at region .6 An an om aly of th e an terior com m u n icat ing com - in 85% of ACoA an eu r ysm s. An eur ysm al form at ion m ay be th e
plex h as been fou n d in u p to 60% of cases in au topsy series.1 At result of h em odyn am ic st ress cau sed by u n even flow in th e A1s,
35 days of age, a prim it ive ACA stem s from each in tern al carot id w h ich w ould accoun t for th e fact th at m ost ACoA an eur ysm s
ar ter y laterally. Five days later (day 40), th e t w o prim itive ACAs ar ise from t h e d om in an t A1 an d grow in t h e direct ion of t h e
elongate tow ard th e m id lin e, an d each bran ch sen ds a m u ltit ude sm aller or hyp op last ic con t ralateral A1 segm en t (i.e., from t h e
of bridging an astom oses tow ard th e oth er. Four days later (day area of h igh h em odyn am ic st ress an d pressure, tow ard areas of
44), th e bridging plexus coalesces to form th e ACoA. At th is poin t , low er in t ravascular p ressure).
an om alies of th e form at ion of th e ACoA can be listed as follow s: Th e A1 segm en t s each give bir th to t w o to 15 m edial len t icu -
(1) t h e com p lete absen ce of t h e ACoA ar ter y, t h e in cid en ce of lost riate perforat ing arteries (MLAs) th at sh ould be dist inguish ed
w h ich w as repor ted to range from 0.2%in a series of 1,803 speci- from th e lateral len t icu lost riate ar teries th at arise from th e m id-
m en s to 22% in a series of 87 silicon -casted brain s 7 ; (2) th e fen - dle cerebral ar teries, an d th e recu rren t ar ter y of Heu bn er (RAH)
est rat ion of th e ACoA; an d (3) th e presen ce of m u lt ip le ACoAs, th at bran ch es ou t of th e A2 segm en t an d u su ally cou rses an teri-
w ith double or t riple ACoAs foun d in up to 30% an d up to 10% of orly to th em . Th e m ajorit y of MLAs (86%) arise from th e poste-
cases, resp ect ively.6,8,9 On ce th e em br yon ic ACoA is form ed, it rior or su perior aspect of th e A1, w ith approxim ately t w o-th irds

584

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50 Surgical Therapies for Anterior Com m unicating Artery Aneurysm s 585

fou n d at it s p roxim al h alf; 41 to 50% of MLAs bran ch ou t in to A2 Segment of the Anterior Cerebral Artery
sm aller p er forators t h at can n u m ber u p to 50, an d en ter t h e
Th e A2 segm en t s st ar t at th e ACoA an d exten d in terh em isph eri-
brain at th e m edial asp ect of th e an terior perforated su bstan ce 10
cally u n t il th ey reach th e gen u of th e corp u s callosu m , w h ere
to su pply m ult iple key cen ters in clu ding th e an terior lim b of th e
th ey con t in u e u pw ard as th e A3s. Th ree m ain bran ch es origin ate
in tern al capsu le, th e an terior hypoth alam u s, th e an terior st ria-
from each A2 segm en t 1 : th e first is located im m ediately dist al to
t um , th e in ferior cau date n ucleus, th e an terior globus pallidus,
th e ju n ct ion w ith th e ACoA an d is referred to as th e m edial st ri-
an d th e pillars of th e forn ix.1,5 An MLA inju r y can th u s result in
ate ar ter y or m ore com m on ly th e RAH after th e Germ an pedia-
a pan oply of m otor, sen sor y, an d cogn it ive deficit s. MLAs th at
trician Johan n Ot to Leonhard Heub ner (1843–1926) w ho init ially
do n ot en ter th e an terior p erforated su bst an ce irrigate th e dorsal
described it . Th e secon d bran ch con sist s of th e orbitofron tal ar-
opt ic ch iasm an d opt ic n er ves, th e opt ic t ract , th e suprach ias-
ter y, w h ich cou rses for w ard an d dow nw ard to sup ply th e gyr u s
m at ic hypoth alam u s, th e sylvian an d in terh em isph eric fissure,
rect us an d th e olfactor y t ract . Th e th ird bran ch is referred to as
an d/or th e in ferior fron t al lobe.
th e fron topolar ar ter y an d is th e m ost dist al of th e th ree, an d
directs an teriorly, crossing th e su bfron tal sulcus. Kn ow ing th ese
Anterior Communicating Artery an atom ic feat ures h elps th e surgeon differen t iate th e orbitofron -
tal an d fron topolar ar teries from th e RAH th at directs backw ard
Measu ring 2 to 3 cm in length an d h alf th e size of th e A1 in diam -
an d parallel to th e A1 an d usually origin ates w ith in a few m illi-
eter, th e ACoA is described as an an astom ot ic form at ion created
m eters of th e A2–ACoA ju n ct ion . How ever th e RAH can be fou n d
by th e u n ion of th e t w o A1s w ith in th e lam in a term in alis cistern
on th e distal A1 t run k in 10 to 14% of cases 1 an d on th e ACoA in
at th e ju n ct ion of th e coron al an d t ran sverse p lan es, an d con -
u p to 8% of cases.10 An oth er differen t iat ing feat u re is th at th e or-
n ected to t w o sym m et rical A2 segm en ts th at course side by side
bitofron t al arter y origin ates at th e bou n daries of th e lam in a ter-
tow ard th e in terh em isph eric fissure.1 Th is classic set up, h ow -
m in alis an d th e callosal cistern s. Th e diam eter of th e RAH ranges
ever, is foun d in on ly 20% of cases, as the A2s are u sually form ed
from 0.2 to 2.9 m m , an d it s length is app roxim ately d ou ble th at
by th e division of a dom in an t A1 branch w ith an asym m et rical
of t h e A1, ranging from 12 to 38 m m , t h u s p lacing it at an in -
sm aller con t ralateral cou n terp ar t . A relat ion sh ip h as been fou n d
creased risk of inju r y d u r ing su rger y.1,6,10 Alt h ough t h e RAH is
bet w een the difference in the size of the A1 segm ents and the size
at t ach ed to t h e A1 at it s or igin by t h ick arach n oid ban d s, it
of th e ACoA, w ith greater differen ces in size accoun t ing for in -
cou rses freely dist ally in th e su barach n oid sp ace an d p en et rates
creasingly larger ACoAs, m ost likely to com pensate for the reduced
th e brain to su p ply th e cau date n u cleu s, pu t am en , ou ter globu s
flow to th e A2 segm en t supplied by the sm aller/hypoplast ic A1.
pallidu s, an d th e an terior lim b of th e in tern al cap su le. Inju r y to
Th is fin ding suggest s th at becau se an terior com m u n icat ing com -
th is perforat ing bran ch can be clin ically silen t or cau se a h em i-
plex an eu r ysm s u su ally arise in th e set t ing of n on sym m et rical
paresis th at is m ost prom in en t in th e face an d upper ext rem it y,
A1s, a p aten t ACoA sh ou ld be con st an tly fou n d in th e presen ce of
as w ell as h em ich orea, dysfun ct ion of th e tongue an d palate, an d
ACoA an eur ysm s.6 In addit ion , th e ACAs at th e level of t h e ACoA
dysar th ria w ith expressive aph asia if th e dom in an t side is in -
en ter t h e in terh em isp h eric fissu re sym m et rically in on ly 20% of
volved. Sym ptom s can occasion ally regress an d even n orm alize
cases, resu lt ing in an ACoA th at is u su ally orien ted in an obliqu e
w ith in a few m on th s. Bilateral occlusion of th is ar ter y can be a
or sagit t al plan e.1,6,11 Th ese fin dings are im por tan t because th ey
cau se of akin et ic m u t ism .12
affect th e in t raoperat ive presen t at ion of th e ACoA an d of ACoA
an eur ysm s, th e orient at ion of th e an eur ysm dom e as w ell as th e
h eigh t of th e ACoA and of ACoA an eur ysm s from th e floor of th e
sku ll base, an d th eir relat ion sh ip to perforat ing ar teries em erg-
ing from th e ACoA.11 Th ree-dim en sion al (3D) ren dering of com -
■ Clinical Relevance of Anterior
puted tom ography (CT) angiography or m agnetic resonance (MR) Communicating Aneurysms
angiograp hy u sin g 3D m od elin g soft w are or CT an giograp hy
recon st r u ct ion s can be u sefu l in an t icip at ing t h ese var iat ion s
Epidemiology
p reop erat ively an d plan n ing for a safe su rgical ap proach . St u dies u sing large h istorical coh or t s h ave rep eated ly fou n d th e
Repor t s on th e n u m ber an d size of p erforators origin at ing ACoA to be a frequ en t , an d even th e m ost frequen t , site of in t ra-
from t h e ACoA var y greatly w ith a range of 0 to 11 ar teries an d a cran ial an eur ysm form at ion as w ell as an eur ysm rupt u re. Th e
d iam eter of 0.1 to 2.1 m m . Most p er forators ar ise from t h e su - origin al Cooperat ive st udy (2,695 an eur ysm s) publish ed in 1966
p erior an d posterior aspect (perpen dicular to th e origin of th e reported an in ciden ce of 28% of ACoA an eur ysm s am ong r up -
A2) of th e ACoA an d are th us sh aded from th e surgeon’s lin e of t u red an eu r ysm s.2 A st u dy of t h e Ku op io Cerebral An eu r ysm
sigh t . Th ey are often fou n d eccen t rically on th e side of th e dom i- Database (1977–2005), involving 4,253 an eur ysm s, foun d th at
n an t A1, or m edially in case of sym m et rical A1s.1 Th ese perfora- an eur ysm s w ere located at th e an terior com m un icat ing com plex
tors are excessively fragile an d suscept ible to inju r y from dissec- 23% of th e t im e.1 Th e In tern at ion al Cooperat ive St udy on th e
t ion an d elect rocoagu lat ion , an d m ay ten d to ir reversibly kin k Tim ing of An eur ysm Surger y foun d th e an terior com m un icat ing
or spasm if crush ed by a clip—even tem porarily—or if m obilized com plex region to h arbor u p to 39% of ru pt u red in t racran ial an -
rough ly. Th ey su pp ly vit al cen ters su ch as th e st alk of th e pit u - eu r ysm s.3 In a p opu lat ion -based series of 2,365 p at ien t s w ith
itar y glan d, th e opt ic ch iasm , th e an terior hyp oth alam us, th e for- p r im ar y an eu r ysm al su barach n oid h em or rh age, ACoAs w ere
n ix, areas of th e lim bic system , an d th e gyri of th e in ferior fron tal t h e site of ru pt u re in 30% of cases (as frequ en t as an eu r ysm s of
lobe. Th eir inju r y can lead to great n eu rologic m orbid it y t h at th e bifu rcat ion of t h e m iddle cerebral ar ter y).1 Th e recen t In ter-
in clu d es m em or y d eficit s an d p erson alit y ch an ges, as w ell as n at ion al St udy of Un r upt ured In t racran ial An eur ysm s (ISUIA) in
elect rolyt ic im balan ces.1,11 4,060 pat ien t s w ith u n rupt ured an eur ysm s iden t ified an ACoA

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586 V Cerebral and Spinal Aneurysms

aneurysm in 12.3%.4 In a sim ilar fashion, the Japanese Unruptured brain , an d th eir proxim it y to 11 key ar terial bran ch es in cluding
Cerebral An eu r ysm St u dy (UCAS) repor ted th at 15.5% of all an - t w o A1s an d t w o A2s t h at p rovid e bilateral an terograde an d
eu r ysm s w ere ACoA an eu r ysm s in a large series of 6,697 u n ru p - ret rograde flow to th e ACoA, to t w o RAHs, an d to t w o orbitofron -
t u red an eu r ysm s.5 Moreover, ACoA an eu r ysm s seem to r u pt u re tal an d t w o fron topolar ar teries.6 Th e p reoperat ive evalu at ion of
at a sm aller size com pared w ith oth er an eu r ysm s, w ith u p to 50% th e an eu r ysm dict ates th e ch oice of th e su rgical ap proach an d
of th e rupt u red aneur ysm s being sm aller th an 7 m m in size. sh ou ld be perform ed on a case-by-case basis an d t ake in to ac-
Th ese fin dings are corroborated by th e n ew ly pu blish ed UCAS cou n t both clin ical an d an atom ic factors.
st u dy, w h ich foun d th at ACoA h as th e h igh est an n ual rate of ru p - Clin ical factors of relevan ce in clu d e (1) t h e r u pt u red or u n -
ture both overall (hazard ratio, 2.02; 95% confidence inter val [CI], rupt ured stat us of th e an eur ysm ; (2) th e am oun t of t im e elapsed
1.13–3.58) an d specifically am ong an eur ysm s m easu ring 3 to after t h e h em or rh agic ep isod e or after a p reviou s su rger y (in
4 m m (ru pt u re risk per year of 0.9%; 95% CI, 0.45–1.80).5 an eur ysm s requiring surgical ret reat m en t), w h ich provides th e
su rgeon w ith im p or tan t in form at ion regarding th e degree of
arachnoid scarring and interfering inflam m atory adhesions; and,
m ost im por t an tly, (3) th e clin ical stat us of th e pat ien t an d th e
■ Clinical and Radiological Presentation n eed to evacuate life-th reaten ing in t raparen chym al or in t raven -
Alth ough th e clin ical presen tat ion of m ost pat ien t s w ith ru p - t ricu lar h em atom as.1 An atom ic factors th at can affect th e ch oice
t u red ACoA an eu r ysm s is fairly sim ilar to th at of oth er in t racra- of th e surgical approach in clude, bu t are n ot lim ited to, th e dom -
n ial an eur ysm s, th ere are specific im aging-related criteria th at in an ce of th e A1 segm en t , th e size of th e an eu r ysm , th e direct ion
w arran t discussion . First , p at ien ts w ith ACoA an eu r ysm s ten d to of t h e an eu r ysm d om e, t h e h eigh t of t h e an ter ior com m u n icat -
presen t frequ en tly w ith in su lts to th e brain p aren chym a an d ing com p lex from the cran ial base, th e 3D orien t at ion of th e
ven t ricles eith er in addit ion to subarach n oid h em orrh age or in ACoA in t h e sagit t al an d coron al p lan es, t h e p resen ce of calcifi-
an isolated fash ion ; a presen t ing in t raven t ricular h em orrh age cat ion s at th e an eu r ysm n eck, an d th e presen ce of associated an -
h as been repor ted in up to 29% of cases of an eur ysm al ru pt ure,1 eu r ysm s. Met icu lou s st u dy of h igh -qu alit y preop erat ive im ages
an d an in t raparen chym al h em atom a h as been repor ted in up to sh ou ld en able th e su rgeon to recogn ize an d accou n t for m ost of
32% of cases,13 w ith th e p os sibilit y of a com bin at ion of both oc- th ese factors, an d to redu ce th e n u m ber of u n expected in t raop -
curring 10% of th e t im e. Th e presen ce of in t raven t ricular or of erat ive even ts to a m in im u m .
in t raparen chym al h em atom as w orsen s th e clin ical progn osis
an d m ay prom pt surgical evacuat ion . In addit ion , pat ien t s w ith
rupt ured ACoA an eur ysm s ten d to presen t frequen tly w ith acute
hydroceph alu s (44% in th e Kuopio series), w h ich m ay w arran t ■ Selecting the Side of
im m ediate ven t ricu lar drain age.
Secon d , radiological iden t ificat ion of t h e cau sat ive lesion can
Surgical Approach
usually be m ade using CT im ages, w ith subarachnoid hem orrhage Th is sect ion ap p lies to n on -in terh em isp h eric ap p roach es su ch as
located predom inantly or in isolation w ithin the interhem ispheric the pterion al, supraorbital, an d orbitozygom atic exposures, w hich
fissure. More specific to ru pt ured ACoA an eur ysm s is th e fin ding are discussed later in th is ch apter. Th e ch oice of th e side of surgi-
of an in t racerebral h em atom a w ith in th e gyrus rect u s. cal ap p roach h as t w o m ain goals: (1) in flict th e m in im al am ou n t
Th ird, becau se of in com ing p ressurized ar terial blood bilater- of t rau m a on th e dom in an t h em isph ere, an d (2) spare th e perfo-
ally from both A1s, th e act ual flow w ith in th e ACoA can be m in i- rat ing arteries th at m ay be located at th e an eur ysm n eck an d can
m al, an d t h u s accou n t for th e fact t h at ACoA an eu r ysm s h ave be in adver ten tly caugh t bet w een th e blades of th e clip. As a rule
t h e h igh est false-n egat ive angiography rate com p ared w ith oth er of th um b, h em odyn am ic st ress factors cause th e an eur ysm to
in t racran ial an eu r ysm s. Man ual com p ression of th e con t ralateral grow in th e direct ion of th e sm aller/hypop last ic A1. Th e an eu-
in tern al carot id arter y du ring th e angiograp hy procedure can r ysm n eck can be foun d on th e side of th e dom in an t A1, w ith th e
h elp in crease flow w ith in th e ACoA an d assess th e qualit y of col- dom e p oin t ing tow ard th e con t ralateral side. Becau se a 3D exp o-
lateral flow, alth ough m any au th ors advocate CT angiography as su re of th e n eck is n ecessar y to avoid inju ring p erforat ing ar ter-
th eir diagn ost ic im aging test of ch oice.1,6,14 ies du ring th e clipping p rocedu re, accessing th e an eur ysm from
Large an d gian t ACoA an eu r ysm s h ave been repor ted to cau se t h e sid e of t h e d om in an t A1 p rovid es t h e su rgeon w it h a t act i-
hydroceph alu s, cogn it ive im pairm en t eith er th rough direct an - cal advan t age by exp osin g t h e an eu r ysm n eck before it s dom e.
eu r ysm al com p ression or th e resu lt ing hydrocep h alu s, as w ell as In rare cases w h ere th e t w o A1 segm en t s are of equal size an d
visu al sym ptom s by d ist u rbin g t h e opt ic ap p arat u s in in fer ior- th e an eu r ysm is t r u ly m idlin e w ith in th e sagit t al p lan e, an ap -
p oin t in g an eu r ysm s.1,15 Dem en t ia w as also rep or ted in gian t proach from th e n on dom in an t h em isph ere is w arran ted.
an eu r ysm s larger th an 3.5 cm .15

Anatomic Configurations of Anterior


Communicating Artery Aneurysms
■ Preoperative Evaluation of Anterior
Th e im por t an ce of th e spat ial orien t at ion of th e dom e an d n eck
Communicating Artery Aneurysms of ACoA an eur ysm s an d its im pact on th e ch oice of th e surgical
Th e su rgical ch allenge presen ted by ACoA an eu r ysm s resides approach an d th e tech n ique of brain ret ract ion an d dissect ion ,
m ain ly in th eir crit ical locat ion deep w ith in th e m idlin e of th e culm in at ing in an eur ysm clipping, w ere recogn ized by Yaşar

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50 Surgical Therapies for Anterior Com m unicating Artery Aneurysm s 587

gil16–18 in th e 1970s, w h o classified ACoA in to five categories. Superior or Upw ard-Facing Aneurysms
Each of th ese categories p resen t s th e su rgeon w ith sp ecific an a-
tom ic p ar t icu lar it ies an d w it h su rgical op p or t u n it ies an d d is- Th ese an eu r ysm s con st it u te 34.4% of all ACoA an eu r ysm s.18
advan tages th at sh ould be closely exam in ed before th e surger y Su perior p oin t ing an eu r ysm s are located w ith in th e in terh em i-
to opt im ize th e approach an d avoid preven t able operat ive com - sph eric fissu re bet w een th e t w o A2 segm en t s, w ith th e dom e
plicat ion s (Fig. 50.1). Th e m ajorit y (71.2%) of ACoA an eu r ysm s project ing in th e sam e direct ion as th e A2s. Th ey offer th e advan -
project w ith in th e in terh em isph eric fissu re, an d on ly a m in orit y tage of gen erally n ot being adh eren t to relat ively fixed st r uct ures
project in feriorly tow ard th e opt ic ch iasm (16%). An oth er 16% of of th e cran ial base such as th e opt ic n er ves or th e opt ic ch iasm ,
th ese an eu r ysm s h ave com plex m u lt ilobu lated m u lt idirect ion al an d th us presen t a m in im al risk of rupt ure during fron t al lobe
projection s. Th e m ain ch aracterist ics of th e m ajor categories of ret ract ion an d during ret ractor placem en t across th e in terh em i-
ACoA an eu r ysm s are d iscu ssed in th e follow ing subsect ion s. sp h eric fissu re to reveal key sect ion s of t h e an terior com m u n i-

Fig. 50.1 Artist illustration displaying the four m ain variations of anterior ond, and third segm ents of the anterior cerebral artery, respectively; AChA,
com m unicating artery (ACoA) aneurysm s, and their relationship to the sur- anterior choroidal artery; FPA, frontopolar artery; ICA, internal carotid ar-
rounding vascular and nervous anatomy, as seen through a right pterional tery; LLA, lateral lenticulostriate artery; MCA, m iddle cerebral artery; MLA,
craniotomy. The different aneurysm colors represent the four possible ori- m edial lenticulostriate artery; OC, optic chiasm ; OFA, orbitofrontal artery;
entations as follows: blue aneurysm , inferior or downward facing; green ON, optic nerve; PCoA, posterior com m unicating artery; RAH, recurrent
aneurysm , superior or upward facing; brown aneurysm , anterior or forward artery of Heubner.
facing; black aneurysm , posterior or backward facing. A1, A2, A3, first, sec-

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588 V Cerebral and Spinal Aneurysms

cat ing com p lex, specifically th e an atom y of th e con t ralateral A1 clu ding th e opt ic ch iasm , th e opt ic n er ves, an d th e du ra of th e
segm en t. On th e oth er h an d, th e posterior asp ect of th e an eu - in teropt ic space. Early m an euvers aim ed at ret ract ing t h e fron t al
r ysm n eck an d dom e is often in t im ately adh eren t to in fun dibular lobe m ay th u s avu lse th e dom e of an eu r ysm off of its sites of
an d hypoth alam ic perforators, w h ich h ave to be dissected aw ay adh eren ce, cau sing a brisk bleed th at w ill be difficult to con t rol.
to clear sp ace for t h e ap p licat ion of a clip . In ad d it ion , on e or Releasing t h e fron t al lobe by ap p roach ing t h e an ter ior com m u -
bot h A2 segm en t s can be den sely adh eren t to th e dom e of th e n icat ing com p lex t h rough th e sylvian fissu re, an d resect ing t h e
an eur ysm an d h ave to be dissected off before clipping. If th is gyrus rect us w ill bring th ese an eur ysm s in view of th e surgeon
procedu re is deem ed too difficu lt or h azardou s, fen est rated clips in m ost cases alm ost w ith out t h e n eed for m uch fron t al ret rac-
can be of u se to circu m ven t th e ad h eren t A2 segm en t . Becau se t ion . On ce th e an eu r ysm dom e is visu alized, it sh ou ld be care-
th ese an eu r ysm s are fou n d w ith in th e plan e defin ed by th e t w o fully detach ed an d exam in ed circu m feren t ially, as it w ill often
A2 segm en t s an d w ith in th e in terh em isph eric fissu re, an in ter- h ave in fun dibular an d hypoth alam ic perforators adh eren t to its
h em ispheric approach can be useful in cases of h igh -riding ACoA posterior aspect .1,6 On ce th ese perforators are dissected aw ay, a
an eur ysm s. st raigh t clip p arallel to th e direct ion of th e ACoA usually secures
th e an eu r ysm w h ile avoiding perforator injur y.

Anterior or Forw ard-Facing Aneurysms


An terior poin t ing an eur ysm s project fron tally alm ost perpen - Surgical Complications Specific to Anterior
dicu lar to th e p lan e set by th e A2 segm en ts. Th ese an eu r ysm s Communicating Artery Aneurysm Surgery
con st it u te 22.7% of an eu r ysm s of th e ACoA.18 Th e st ruct ure of
Com p licat ion s relat in g to sp ecific tech n ical vascu lar inju ries
th e an eu r ysm is directed in th e op p osite direct ion of th e in fu n -
d u r ing ACoA an eu r ysm surger y h ave already been discussed in
dibu lar an d hyp oth alam ic p erforators, an d th ese an eu r ysm s are
p reviou s sect ion s of t h is ch apter. How ever, t w o m ajor gen eral
th erefore som e of th e easiest to clip on ce th ey are exposed, an d
com p licat ion s t h at are com m on ly fou n d after ACoA an eu r ysm
th ey can be n eu t ralized by a st raigh t clip app lied p arallel to th e
rupt u re or repair are w or th discussing.
ACoA to avoid inju r y to t h e p erforators. How ever, becau se of
t h e or ien t at ion of th eir d om e, t h ese an eu r ysm s can ad h ere to
th e orbitofron t al or less frequen tly th e fron topolar ar ter y, w h ich Electrolytic Abnormalities
w ill h ave to be dissected off, or scarified to clear th e an eu r ysm
Mu lt ip le elect rolyt ic d ist u rban ces can be fou n d after ACoA an -
n eck. More im por t an tly, an terior-facing ACoA an eur ysm s h ave
eu r ysm r u pt u re or su rger y, bu t t h e m ost frequ en t rem ain s hy-
t h e h igh est rate of p rem at u re in t raop erat ive r u pt u re.1 Becau se
p on at rem ia. It w as previously at t ribu ted to th e syn drom e of in -
of th eir direct ion , th e dom e often adh eres to th e fron tal lobe at
appropriate an t idiuret ic h orm on e secret ion , but is n ow believed
th e level of th e gyru s rect u s an d m ay ru pt u re at any step of th e
to be due to th e cerebral salt-w ast ing syn drom e. It s occurren ce
dissect ion , bu t esp ecially du ring su bfron t al ret ract ion . Ret ract-
w as fou n d in 18% of p at ien t s p reop erat ively an d 40.5% of p a-
ing th e fron t al lobe sh ou ld be avoided an d th e exposure of th e
t ien ts p ostop erat ively in a series of 371 r u pt u red an eu r ysm s
an eur ysm –A1-A2 com plex can be obt ain ed by a careful st rategic
pu blish ed by Yaşargil,18 an d lasted 1 to 5 days.
resect ion of th e gyru s rect u s.

Cognitive Dysfunction
Posterior or Backw ard-Facing Aneurysms
In it ial repor ts of ACoA an eur ysm surger y ou tcom es described
Posterior projecting ACoA aneur ysm s are located beh ind the plane
th e occu rren ce of a syn d rom e follow ing an eu r ysm r u pt u re or
form ed by th e t w o A2s an d face tow ard th e occiput . Th ey con st i-
su rger y an d con sist ing of severe am n esia, person alit y ch anges,
t u te 14.1% of all ACoA an eu r ysm s.18 Th ey are con tain ed w ith in
an d con fabu lat ion . Th is disorder w as at t ributed to lesion s of th e
th e in terh em isph eric fissu re. Alt h ough th e an eu r ysm dom e does
basal fron t al lobe, an d clin ically com p ared w it h t h e Wer n icke-
n ot involve t h e A2s, t h ese an eu r ysm s are con sid ered t h e m ost
Korsakoff syn drom e an d th us w as term ed ACoA an eur ysm syn -
com p lex to clip becau se th eir n eck an d th e low er p or t ion of th e
drom e.19 How ever, advan ces in th e fields of m icrosurger y, crit i-
dom e are located in th e m idst of ACoA p erforators. In fu n dibu lar
cal care, an d an esth esia h ave led to th e occu rren ce of m ilder
an d hyp ot h alam ic p er forators are often ad h eren t to t h e n eck
form s of th is syn drom e an d even par t ial or com plete recover y in
an d th e body of th e an eur ysm (com m on ly over its in ferior or less
som e patien ts. Th e cogn it ive dysfu n ct ion is n o longer con sidered
com m on ly it s su p erior asp ect) an d n eed to be carefu lly dissected
to be a com p lete am n est ic syn d rom e bu t rat h er en t ails sym p -
off before clip applicat ion . On ce th e perforators h ave been se-
tom s ranging from m ild to severe th at sh ou ld be t reated on a
curely iden t ified, a st raigh t clip placed parallel to th e ACoA can
case-by-case basis.19
usu ally secure th e an eur ysm , alth ough m ore com plex clip com -
bin at ion s can som et im es be n ecessar y.2,3
Surgical Approaches to the Anterior
Inferior or Dow nw ard-Facing Aneurysms Communicating Complex
Th ese an eu r ysm s con st it u te 12.8% of all ACoA an eu r ysm s.18 An - Fou r cran iotom ies h ave been described to access th e region of
eu r ysm s project ing in feriorly are alm ost com p letely ou t side of th e an terior com m u n icat ing com plex: pterion al, lateral su p ra-
th e in terh em isp h eric fissu re, an d are u su ally t igh tly adh eren t to orbit al, in terh em isph eric, an d orbitozygom at ic. Issues specific to
relat ively st at ic st r u ct u res (com p ared w ith th e fron tal lobes) in - each of th ese approach es are described below, as w ell as th e par-

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50 Surgical Therapies for Anterior Com m unicating Artery Aneurysm s 589

t icu larit ies an d advan tages offered by each regarding sp ecific com plex w ith lit tle to n o ret ract ion . On ce th e du ra is exp osed, it
t ypes of ACoA an eu r ysm s. Th e gen eral preop erat ive an d in t ra- should be opened in a cur vilinear fashion and reflected an teriorly
op erat ive n eu rosu rgical an d n eu roan est h esiologic p r in cip les, over th e bon e in a m an n er th at avoids dural folds to m axim ize
in clu ding brain relaxat ion , n avigat ion th rough th e cistern s w ith t h e exp osu re t h rough t h e su bfron t al cor r id or. Th e op erat in g
cerebrospin al flu id drain age w h en n ecessar y, th e use of n euro- m icroscope is th en brough t in to th e su rgical field. It is ou r pref-
m onitoring, and the use of burst suppression w hen needed, apply eren ce to u se t h e m ou t h p iece, as it en ables t h e m icroscop e to
regardless of th e cran iotom y t yp e. be refocused at var ying depth s w ith out t aking th e h an ds off th e
m icro-in st ru m en t s.

Pterional Approach
Microsurgical Technique
Macrosurgical Technique
Th e m icrosu rgeon sh ou ld w ork in a seated p osit ion in a post u re
Th e det ails of th e pterion al ap proach h ave been exten sively p u b - sim ilar to th at of a p ian ist . It is ou r p referen ce to u se sh arp dis-
lish ed in th e literat u re.1,6,17,20 Th e pat ien t’s h ead is first elevated sect ion w ith an arach n oid kn ife for m ost of th e dissect ion . Blun t
above sh ou lder level an d th en rotated aw ay from th e side of th e dissect ion can be u sed to st retch bu t n ot tear arach n oid adh e-
an eur ysm by 45 to 60 degrees an d exten ded to place th e zygo- sion s, w h ich can facilit ate th eir su bsequ en t division w ith a sh arp
m at ic em in en ce at th e h igh est poin t of th e h ead as seen in an op h t h alm ic kn ife. Relevan t cister n s sh ou ld be op en ed , w h ich
axial plan e. Th is posit ion allow s gravit y to “ret ract” th e fron tal m akes th e procedure m ore of a t ran scistern al operat ion th an a
lobe aw ay from t h e base of t h e an ter ior fossa an d m in im izes “brain op erat ion .” Occasion ally, open ing th e sylvian fissure can
t h e n eed for in t raop erat ive ret ract ion . Th e h ead is th en sligh tly be advan tageous par t icularly for large an d gian t an eur ysm s as
t urn ed to th e opposite side to keep th e plan e of th e fron tal base w ell as for an eur ysm s th at are h igh relat ive to th e cran ial base. A
parallel w ith th e sh ou lders. A cu r vilin ear in cision is plan n ed ret ractor is placed along th e fron t al border of t h e m edial sylvian
from w ith in 1 cm of th e t ragus at th e level of th e zygom at ic root fissure w ith th e t ip of th e ret ractor just superficial to th e opt ic-
(to avoid fron t alis m uscle injur y) to th e m idlin e, staying beh in d carot id cistern . Th is cistern sh ou ld be open ed to release cerebro-
th e h airlin e (Fig. 50.1). A st raigh t lin e draw n bet w een th e star t- spin al fluid. Th e cistern of th e opt ic n er ve is th en open ed w ith
ing an d en ding poin t of th is p lan n ed in cision sh ou ld ap proxi- special care to avoid inju r y to th e blood su pply to th e opt ic n er ve.
m ate th e keyh ole. For in dividuals w ith w ide foreh eads it m ay be Th e ret ractor is th en gradu ally t ran sit ion ed posteriorly an d m e-
n ecessar y to cross th e m idlin e to provide opt im al supraorbital dially to elevate th e fron tal lobe off th e opt ic n er ve an d fron t al
exp osu re, as th e cran iotom y w ill n eed to exten d to th e level of base. Care is taken to avoid tearing vessels an d arach n oid adh e-
th e su p raorbit al n er ve m ed ially. For u n ru pt u red an eur ysm s, w e sion s. Sh arp d issect ion is essen t ial to keep th e dissect ion gen tle
t ypically clip en ough h air to keep th e closu re lin e clear at th e en d an d at raum at ic. Th e dissect ion is con t in u ed un t il th e ipsilateral
of th e procedure. We t ypically clip m ore h air in pat ien ts w ith A1 is seen , an d a place for a tem porar y clip is iden t ified sh ould it
rupt ured an eur ysm s. We prefer to secure th e skin flap to a re- be n eeded. Care is taken h ere to avoid inju r y to th e RAH.
t ractor bar th at elevates th e flap at abou t a 45-degree angle to Th e ret ractor is n ow rot ated tow ard th e A1/A2 ju n ct ion , an d
th e cran ial base, h en ce avoiding pressu re on th e orbit al con ten t s. its t ip is p laced ju st lateral to th e olfactor y t ract . Th e cistern al
It is our preferen ce to h ar vest pericran ium an d keep it on its vas- dissect ion is th en carried across th e m idlin e to iden t ify th e con -
cular pedicle for later use in th e case if n eeded . t ralateral A1, th u s yielding com p lete p roxim al con t rol. If n eed ed,
We th en in cise th e tem p oralis fascia in a lin e 1 cm below th e a subpial part ial gyrus rect us resect ion is th en perform ed. It is
su p erior tem p oral lin e from th e keyh ole back to th e p osterior im port an t for th is dissect ion to rem ain su bpial un t il th e origin of
edge of th e in cision . From th is p oin t a secon d cu t is carried dow n th e RAH is clearly defin ed. Th e p ia can be en tered m ore dist ally
to th e level of th e zygom at ic root . Th e tem poralis m uscle is th en along th e ipsilateral A2 to approach th e in terh em isph eric fissure
m obilized an teriorly w ith blun t dissect ion an d secured to th e re- an d iden t ify th e con t ralateral A2. Iden t ifying th e t w o A2s be-
t ractor bar. We t yp ically th en place th ree bu r h oles, bu t occa- yon d th e an eu r ysm (or th ree A2s w h en presen t) establish es dis-
sion ally a fou r th is n eed in elderly pat ien ts w ith ver y adh eren t tal con t rol. Th e ipsilateral A2 is th en follow ed back carefu lly to
du ra. Th e bu r h oles are located (1) at th e keyh ole, (2) ju st above th e an eu r ysm w h ere gen tle sh arp dissect ion w ill reveal th e 3D
th e zygom at ic root , an d (3) 1 cm below t h e su p erior tem p oral feat ures of th e n eck. It is im por tan t for th e su rgeon to w ork in a
lin e an d in fron t of th e posterior in cision . Th ese th ree bu r h oles com for t able p osit ion an d to h ave th e an atom y com pletely u n rav-
are covered by m uscle at th e en d of th e procedure, w h ich results eled . Not seeing en ough of th e an atom y is a com m on cau se for
in bet ter cosm esis. A fou r th bu r h ole m ay be n eeded in lin e w ith errors du ring clipp ing. Dissect ing deep to th e A1/A2 ju n ct ion en -
th e su p raorbit al n otch 2 cm above th e cran ial base. W h en creat- ables the anterior com m unicating com plex to be seen from below,
ing th e bon e flap w ith th e craniotom e it is im p ort an t to m ake th e w h ich is crit ical for protect ing perforators an d for un derstan ding
su p raorbit al cu t as low as possible on th e cran ial base. Th e m e- th e 3D con figu rat ion of th e an eu r ysm an d of th e an terior com -
dial exten t of th is cu t is th e lateral border of th e su praorbital m un icat ing com plex. Clipping sh ould n ot com m en ce un t il ade-
n otch . On ce th e cran ial flap is elevated, tacking sut ures can be qu ate visualizat ion an d surgeon com for t h ave been ach ieved.
placed circu m feren t ially. Th e sph en oid ridge is th en drilled un t il
flat an d th e superior orbital fissu re is exposed. Th e m en ingo-
Surgical Clipping
orbit al ban d can be divided to facilit ate adequate flat ten ing of
th e sp h en oid ridge. Drilling th e in n er t able of th e fron t al bon e W h en clip p ing an ACoA an eu r ysm , it is h elp fu l to keep in m in d
allow s subfrontal exposure of the anterior com m unicating artery th e appearan ce of th e an eur ysm -free an atom y, as clipping th e

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590 V Cerebral and Spinal Aneurysms

aneurysm entails reconstructing the functional anatom y and t ak- the corpus callosum until the anterior com m unicating com plex is
in g t h e an eu r ysm ou t of t h e circu lat ion . Th is view of t h e p roce- reached. The neck of the aneurysm is then prepared for clipping.
du re en ables th e su rgeon to recon st r u ct th e A1/A2 ju n ct ion an d
th e ACoA w ith ou t com p rom ising th e con t ralateral A2 caliber.
Tem porar y occlusion can be a safe step, par t icu larly for fragile Orbitozygomatic Approach
rupt ured lesion s an d for com plex lesion s. Trapping w ith defla-
Th e orbitozygom at ic app roach is ver y u sefu l for gian t an eu r ysm s
t ion can facilitate th e clipp ing of large, gian t , an d w ide-n ecked
an d for an eu r ysm s t h at are located h igh relat ive to t h e cran ial
an eur ysm s. On occasion w e h ave foun d aden osin e flow arrest
base.6,25 Gon zalez et al 26 u sed cadaver ic h ead s to com p are t h e
h elpful to soften large an eur ysm s en ough to see th e con t ralat-
su rgical exposu re to th e cran ial base p rovid ed by th e pterion al
eral A1/A2 ju n ct ion an d facilit ate clip ap plicat ion .21,22 It is im -
approach , th e stan dard orbitozygom at ic approach , an d a m odifi-
por t an t to avoid catch ing p osterior hypoth alam ic p erforators in
cat ion of th e orbitozygom at ic app roach in clu ding m axillar y ex-
th e blade. On ce th e clip s are p laced, carefu l in spect ion sh ou ld
ten sion . Th e m a xim um angle of at t ack obt ain ed w as sign ifican tly
com m en ce to en su re th at n o im p or t an t vascu lar an atom y w as
greater w ith th e orbitozygom at ic approach com pared w ith th e
com prom ised an d th at th e an eu r ysm is secu re. In t raop erat ive
pterion al (37.2 ± 4.7 degrees vs 27.1 ± 4.3 degrees; p < 0.001),
in docyan in e green (ICG) angiograp hy w h en u sed approp riately
an d in creased even m ore n ot iceably w ith m a xillar y exten sion
can h elp en su re p aren t ar ter y p aten cy an d an eu r ysm closu re.
(42 ± 4.9 degrees; p < 0.001). Th e su rgeon’s w orking area also
in creased w h en com paring th e pterion al cran iotom y (281 m m 3 )
Lateral Supraorbital Approach to th e orbitozygom at ic cran iotom y (343 m m 3 ). Th e orbitozygo-
m at ic ap p roach can t h u s im p rove t h e an gle of at t ack to t h e an -
Alth ough th is approach is favored by som e surgeon s, w e h ave
terior com m un icat ing com plex w h ile m in im izing th e n eed for
n ot adopted it in ou r pract ice.1 Th is approach is perform ed as
brain ret ract ion .26
follow s: th e pat ien t’s h ead is posit ion ed so as to place th e ACoA
region at th e t ip of th e su rgeon’s t riangle of exposu re, an d can be
m odified perioperat ively by rotat ing th e h ead fram e or th e op -
erat ive t able. After a fron totem poral skin in cision is m ade beh in d
th e h airlin e, an d th e tem poralis m u scle sp lit , th e skin is ret racted ■ Clinical Outcome After Anterior
an teriorly un t il th e edge of th e orbit al rim . A bur h ole is placed Communicating Artery Aneurysm
directly m edially to th e tem p oral lin e, an d a sm all cran iotom y is
m ade. Th e dura is open ed an d sh arp dissect ion is used to n avi-
Surgery
gate un der th e fron tal lobe un t il th e lam in a term in alis cistern is Pat ien t ou tcom es after th e surgical m an agem en t of ACoA an eu-
open ed. Th e rest of th e m icrosurgical procedure is sim ilar to th at r ysm s h ave im p roved great ly sin ce t h e in it ial coh or t rep or t s
described in th e pterion al app roach . gen erated before th e in t rodu ct ion of th e su rgical m icroscop e in
th e n eu rosu rgical specialt y in th e 1970s. In a p rosp ect ive ran -
dom ized t rial in clu ding 300 p at ien ts t reated bet w een 1958 an d
Anterior Interhemispheric Approach
1963 for a r upt ured ACoA an eu r ysm an d com paring surgical to
Th is ap p roach can be h elpfu l in cases w h ere th e an terior com - clin ical m anagem en t, surgical m ortalit y rates exceeded conserva-
m un icat ing com plex is sit u ated h igh above th e floor of th e an te- tive m anagem ent m ortalit y rates, and w ere as high as 44%, w ith
rior fossa, par t icu larly at a dist an ce of m ore th an 13 m m , an d on ly 37% of surgical pat ien ts able to resum e th eir n orm al w ork
w h ere sign ifican t ret ract ion of th e fron tal lobe w ould be re- act ivit ies.6 With th e im plem en t at ion of m odern n eurosurgical
qu ired to access th e an eu r ysm .1,6,17,18,23,24 Min im al brain t issue tech n iqu es, Yaşargil decreased t h is m or t alit y rate to 5.9% in a
ret ract ion is required, an d th e olfactor y tract an d gyru s rect us series of 371 cases of r upt ured ACoA an eur ysm s pu blish ed in th e
are preser ved. Th e h ead is elevated above th e level of th e h ear t m id -1970s, alth ough m ost of th e su rgical p at ien t s in th is series
an d placed in a n eut ral posit ion , w ith th e nose at th e m idlin e an d w ere preoperat ively in good clin ical con dit ion (80%Fish er grades
poin t ing u pw ard to provide a p erp en dicu lar view at th e an terior I an d II).17,18 It is n ow kn ow n th at in it ial clin ical presen tat ion is a
com m u n icat ing com p lex. Th e in cision is m ade beh in d th e h air- predict ive factor of surgical outcom e in an eur ysm surger y. More
lin e in a cu r vilin ear fash ion an d crosses th e m idlin e. Hook re- recen t large su rgical series report in term ediate figures; th e sur-
t ract ion provides exp osu re of th e fron tal bon e w ith ou t th e n eed gical m ortalit y rate in th e In tern at ion al Cooperat ive St u dy w as
for a bicoron al in cision , an d a bu r h ole is placed m idlin e above 16.8%3 for an terior com m un icat ing com plex an eur ysm s w ith an
th e su perior sagit t al sin u s. Th e du ra is dissected carefu lly off th e overall m ortalit y rate of 30.1%. Proust et al27 com pared 83 pa-
bon e, w ith special care taken in en tering the bridging vein s. After tients treated m icrosurgically for ACoA aneurysm s bet w een 1990
th e cran iotom y, th e d u ra is in cised in a cur vilin ear fash ion an d an d 1995, an d 103 pat ien ts t reated m icrosurgically bet w een
reflected tow ard th e m idlin e. Th e edges of th e su rgical exp osu re 1996 an d 2000. Th ey foun d th at th e rate of death an d perm an en t
are t h en covered to p reven t air em boli. Th e in terh em isp h er ic m orbidit y related to su rger y decreased dram at ically bet w een
fissu re is en tered, an d sh arp dissect ion is used to rem ove arach - the t w o periods, w ith 16.9%for the earlier period and 3.9%for the
n oidal adh esion s to th e falx w h ile n avigat ing tow ard its in ferior later p er iod (p = 0.011). Fu r t h er advan ces in t h e field , su ch as
border bet w een th e cingulate gyri, un t il the pericallosal cistern t h e u se of aden osin e for in t raop erat ive tem p orar y flow arrest 21,22
is reach ed. Th e corp u s callosu m an d th e p ericallosal arteries are an d th e availabilit y of in t raoperat ive ICG angiography are cer tain
visu alized. Th e arteries are follow ed w ithin th e fissure arou n d to im p rove th ese n um bers even m ore.

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50 Surgical Therapies for Anterior Com m unicating Artery Aneurysm s 591

dates for both su rgical clipp ing an d en dovascu lar coiling (Fig.
■ Treatment Decision for Anterior 50.2). It is th is par t icu lar categor y of an eu r ysm s th at is evaluated
Communicating Artery Aneurysms: in m ost clin ical t rials. Th is evalu at ion rem ain s h igh ly su bject ive
Clip or Coil? because th e eligibilit y of th e an eur ysm as a good can didate for
eith er coiling or clip p ing is p erceived differen tly depen ding on
Alth ough som e st udies h ave sh ow n m ore favorable sh or t-term th e t rain ing, exp erien ce, an d biases of t h e t reat ing team m em -
outcom e for coiling w h en com pared w ith clipping for ru pt ured bers. In addit ion , th ere are n o ran dom ized data for un rupt u red
an eur ysm s, several issues n eed to be kept in m in d. Com parat ive an eur ysm s. Clearly th ere are pros an d con s to both approach es,
st u dies rely on experien ced team s to iden t ify a su bset of an eu - an d ideally th e tech n ique th at gives th at pat ien t th e best sh or t-
r ysm s th at are at equipoise, an d are th us con sidered good can di- an d long-term result sh ould be th e on e u t ilized. Gen eral factors

Fig . 50.2a– g (a) A 43-year-old m an presented with clinical signs of


m eningeal irritation (Hunt-Hess Grade I) and a front al interhem ispheric
subarachnoid hem orrhage seen on brain com puted tom ography scan.
(b) Angiogram revealed the presence of a wide-necked 3- to 4-mm anteriorly
projecting anterior com m unicating artery (ACoA) aneurysm . (c) The pa-
tient underwent balloon-assisted coiling of the aneurysm with com plete
initial aneurysm occlusion. (continued on page 592)

b c

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592 V Cerebral and Spinal Aneurysms

d e

f g

Fig. 50.2a–g (continued ) (d,e) Follow-up angiography 2 weeks later from the aneurysm and contained by a pseudom embrane. An incidental
prompted by a significant headache reported by the patient showed m ajor right M1 aneurysm was also surgically clipped during the sam e procedure.
recurrence of the aneurysm . The patient underwent surgical clipping via a (f,g ) The postoperative angiogram showed com plete obliteration of the
right pterional craniotomy. The coils were seen intraoperatively extruding lesions. The patient woke up neurologically intact.

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50 Surgical Therapies for Anterior Com m unicating Artery Aneurysm s 593

th at m ay sw ay th e operat ive decision tow ard clip ping in clu de bid it y.27 On t h e ot h er h an d , an eu r ysm s w it h a d om e sm aller
young pat ient age, w here en suring the durabilit y of the t reatm ent th an 10 m m th at p roject an teriorly an d h ave a sm all n eck m ay
is con sidered essen tial; th e p resen ce of a large or gian t-sized an - disp lay h igh rates of in it ial com p lete em bolizat ion .29 In a recen t
eu r ysm ; th e presen ce of a large h em atom a requ iring evacu at ion series by Guglielm i et al,30 rep or t ing on 306 p at ien t s w ith ACoA
in th e con text of a ru pt u red an eur ysm ; an d a sign ifican t an eu- an eur ysm s, com plete an eur ysm occlusion w as obtain ed in 45%
r ysm n eck-to-dom e rat io (> 0.5), w h ich could be problem at ic for of cases, w h ile a rem n an t w as detected in 47% of cases, w ith
coilin g. On t h e ot h er h an d , gen eral factors t h at m ay favor t h e m orbidit y an d m or talit y rates of 3.5% an d 1%, respect ively, an d
en dovascu lar opt ion in clu de older p at ien t age, w h ere th e du ra- 91.5% of pat ien t s rem ain ing n eurologically in t act or im proving
bilit y of th e t reat m en t is less of a con cern , especially in th e pres- clin ically. Th e auth ors con cluded th at w ith th e in creasing safet y
en ce of m u lt iple com orbidit ies th at in crease th e su rgical risk; an d efficacy of en dovascular tech n iques an d con t in u ously im -
sm aller an eu r ysm size, esp ecially in th e p resen ce of a sm all n eck; proving m icrocath eter techn ology, en dovascu lar t reat m en t is a
an d th e presen ce of vascular spasm , w h ere in t ravascu lar ch em i- viable altern at ive for ACoA an eu r ysm s especially in cases w ith a
cal an d m ech an ical angiop last y cou ld be p erform ed sim u lt an e- h igh ch an ce of perforator injur y. Th e fin al th erapeut ic decision ,
ou sly if n eed ed. h ow ever, depen ds on th e pat ien t’s clin ical an d an atom ic factors,
In addit ion to th e in flu en ce of th ese gen eral factors, an eu- th e p at ien t’s w ish es, an d the exp er t ise of th e su rgeon .
rysm s of the anterior com m unicating com plex m ay be m ore prone
to recu r com pared w ith oth er in t racran ial locat ion s becau se of
th e h em odyn am ic forces at play.6 Moret et al28 fou n d a 12-m on th
recu rren ce rate of 25% at follow -up angiograp hy. Coil com pac-
t ion or ext ru sion ou tside of th e an eu r ysm w all d u e to th e in -
■ Conclusion
creased h em odyn am ic st ress an d th e w ater h am m er effect of th e An eu r ysm s ar ising from t h e ACoA com p lex are com m on le-
blood flow in th is region m ay accoun t for som e of th ese recur- sion s. Alth ough both m icrosurgical tech n ique an d en dovascular
ren ces. En d ovascular access to th e ACoA m ay be especially prob - th erapies h ave sh ow n to be effect ive in t reat ing th ese lesion s, th e
lem at ic in th e p resen ce of a severely hyp oplast ic or absen t A1 decision to t reat sh ou ld be in dividu alized based on th e ch arac-
segm en t . Posteriorly facing an eu r ysm s m ay be difficu lt to access terist ics of th e an eur ysm , th e clin ical stat us of th e pat ien t , an d
du e to th e acu te angle of th eir project ion ,28 alth ough th eir en do- th e exper t ise of t h e p ract it ion er. Master y of m icrosu rgical tech -
vascu lar t reat m en t is recom m en d ed by som e au t h ors becau se n iques rem ain s essen t ial for th e t reat m en t of a su bgroup of th ese
of th e associated h igh rate of p erforator injur y an d su rgical m or- lesion s.

References
1. Hern esn iem i J, Dash t i R, Leh ecka M, et al. Micron eurosurgical m an age- 12. Toyoda K. An terior cerebral ar ter y an d Heubn er’s ar ter y territor y in farc-
m en t of an terior com m un icat ing ar ter y an eur ysm s. Surg Neurol 2008;70: t ion . Fron t Neurol Neu rosci 2012;30:120–122
8–28, discussion 29 13. Pasqualin A, Bazzan A, Cavazzan i P, Scien za R, Licat a C, Da Pian R. In t racra-
2. Locksley HB. Nat ural h istor y of subarach n oid hem orrh age, int racranial n ial h em atom as follow ing an eur ysm al rupt ure: experience w ith 309
an eu r ysm s an d ar terioven ou s m alform at ion s. Based on 6368 cases in th e cases. Su rg Neurol 1986;25:6–17
cooperat ive st udy. J Neurosurg 1966;25:219–239 14. Iw an aga H, Wakai S, Och iai C, Narit a J, In oh S, Nagai M. Ru pt u red cerebral
3. Kassell NF, Torn er JC, Haley EC Jr, Jan e JA, Adam s HP, Kongable GL. The In - an eur ysm s m issed by in it ial angiograph ic st udy. Neurosurger y 1990;27:
ternat ion al Cooperat ive St udy on th e Tim ing of An eu r ysm Surger y. Par t 1: 45–51
Overall m an agem en t result s. J Neurosurg 1990;73:18–36 15. Low n ie SP, Drake CG, Peerless SJ, Fergu son GG, Pelz DM. Clin ical p resen -
4. W iebers DO, W h isn an t JP, Hu ston J III, et al; In ter n at ion al St u dy of Un - t at ion an d m an agem en t of gian t an terior com m u n icat ing ar ter y region
r u pt ured Int racranial An eur ysm s Invest igators. Un rupt u red in t racran ial an eur ysm s. J Neurosurg 2000;92:267–277
an eur ysm s: n at ural h istor y, clin ical ou tcom e, an d risks of su rgical an d 16. Rom an i R, Laakso A, Nie m elä M, et al. Microsu rgical p r in cip les for an -
en dovascular t reat m en t . Lan cet 2003;362:103–110 te r ior circu lat ion an e u r ysm s. Act a Ne u roch ir Su p p l (W ie n ) 2 01 0 ;10 7 :
5. Morit a A, Kirin o T, Hash i K, et al; UCAS Japan Invest igators. Th e n at ural 3– 7
course of u nr upt ured cerebral an eur ysm s in a Japan ese coh or t . N Engl J 17. Yaşargil MG, Fox JL. Th e m icrosurgical approach to in t racran ial an eu-
Med 2012;366:2474–2482 r ysm s. Surg Neu rol 1975;3:7–14
6. Hu ang J, Ger m anw ala AV, Tam argo RJ. An ter ior com m u n icat ing ar ter y 18. Yaşargil MGF, Ray MW. Th e operat ive approach to aneu r ysm s of th e ante-
an eur ysm s. In : Winn HR, ed. Youm an s Neurological Surger y, 6th ed. Ph il- rior com m unicating arter y. In: Krayenbuhl HA, ed. Advan ces an d Technical
adelph ia: W B Sau n ders; 2011:3841–3852 Standards in Neurosurger y. New York: Springer-Verlag; 1975:113–170
7. Merkkola P, Tulla H, Ron kain en A, et al. Incom plete circle of Willis an d 19. Böt tger S, Prosiegel M, Steiger HJ, Yassouridis A. Neurobeh aviou ral dist ur-
righ t axillar y ar ter y perfusion . An n Th orac Surg 2006;82:74–79 ban ces, reh abilit at ion outcom e, an d lesion site in pat ien t s after r upt ure
8. Perlm ut ter D, Rh oton AL Jr. Microsurgical an atom y of th e dist al an terior an d repair of an terior com m u n icat ing ar ter y aneu r ysm . J Neu rol Neuro-
cerebral arter y. J Neurosu rg 1978;49:204–228 surg Psychiat r y 1998;65:93–102
9. Agraw al A, Kato Y, Chen L, et al. An terior com m un icat ing ar ter y an eu- 20. Solom on RA. An terior com m un icat ing ar ter y an eur ysm s. Neurosurger y
r ysm s: an over view. Min im Invasive Neurosurg 2008;51:131–135 2001;48:119–123
10. Perlm ut ter D, Rhoton AL Jr. Microsurgical an atom y of an terior cerebral 21. Bebaw y JF, Gupt a DK, Ben dok BR, et al. Aden osin e-in du ced flow arrest to
an terior com m u n icat ing recu rren t ar ter y com p lex. Su rg For u m 1976;27: facilitate in t racran ial an eu r ysm clip ligat ion : dose-resp on se dat a an d
464–465 safet y profile. An esth An alg 2010;110:1406–1411
11. Serizaw a T, Saeki N, Yam aura A. Microsurgical anatom y and clinical signifi- 22. Ben dok BR, Gu pt a DK, Rah m e RJ, et al. Aden osin e for tem porar y flow ar-
cance of the anterior com m unicating artery and its perforating branches. rest du ring in t racran ial an eur ysm surger y: a single-cen ter ret rospect ive
Neurosurger y 1997;40:1211–1216, discussion 1216–1218 review. Neurosurger y 2011;69:815–820, discu ssion 820–821

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23. Lough eed W M. Select ion , t im ing, an d tech n ique of an eur ysm surger y of 27. Proust F, Debon o B, Han n equin D, et al. Treat m en t of an terior com m u ni-
th e an terior circle of Willis. Clin Neu rosu rg 1969;16:95–113 cat ing ar ter y an eur ysm s: com plem en t ar y aspect s of m icrosurgical an d
24. Ito Z. Th e m icrosurgical an terior in terh em isph eric approach suit ably ap - en dovascular procedures. J Neurosurg 2003;99:3–14
plied to r u pt u red an eu r ysm s of th e an terior com m u n icat ing ar ter y in th e 28. Moret J, Pierot L, Bou lin A, Cast aings L, Rey A. En dovascular t reat m en t of
acu te st age. Act a Neu roch ir (Wien ) 1982;63:85–99 an terior com m u n icat ing ar ter y an eu r ysm s u sing Guglielm i d et ach able
25. Zabram ski JM, Kiriş T, San kh la SK, Cabiol J, Spet zler RF. Orbitozygom at ic coils. Neuroradiology 1996;38:800–805
cran iotom y. Tech n ical n ote. J Neurosurg 1998;89:336–341 29. Gon zalez N, Sed rak M, Mar t in N, Vin u ela F. Im p act of an atom ic feat u res
26. Gon zalez LF, Craw ford NR, Horgan MA, Desh m u kh P, Zabram ski JM, in th e en dovascu lar em bolizat ion of 181 an terior com m u n icat ing ar ter y
Sp et zler RF. Working area an d angle of at t ack in th ree cran ial base ap - an eur ysm s. St roke 2008;39:2776–2782
p roach es: pter ion al, orbitozygom at ic, an d m a xillar y exten sion of t h e 30. Guglielm i G, Viñ u ela F, Du ckw iler G, Jah an R, Cot ron eo E, Gigli R. En dovas-
orbitozygom at ic ap p roach . Neu rosu rger y 2002;50:550–555, d iscu ssion cular t reat m en t of 306 an terior com m un icat ing ar ter y an eu r ysm s: over-
555–557 all, perioperat ive result s. J Neu rosurg 2009;110:874–879

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51 Endovascular Therapies for Anterior
Communicating Artery Aneurysms
Douglas L. Stofko, Zakaria Hakm a, and Erol Veznedaroglu

Th e an ter ior com m u n icat in g ar ter y (ACoA) is t h e m ost com - In 2002, th e acceptan ce of en dovascu lar t reat m en t of in t ra-
m on site of in t racran ial an eu r ysm s an d th e single m ost frequ en t cran ial an eur ysm s w as boosted by th e results of th e In tern a-
site for an eu r ysm r u pt u re, accou n t ing for 40% of an eu r ysm al tion al Subarachnoid Aneurysm Trial (ISAT),13 w hich dem onstrated
su barach n oid h em orrh age (SAH).1–3 Historically, th e preferred a sign ifican t reduct ion in depen den cy an d death at 1 year for
m eth od of t reat m en t of ACoA an eu r ysm s h as been m icrosurgical pat ien ts t reated w ith en dovascu lar p rocedures versu s clip liga-
clip ligat ion .4–6 How ever, com p lex an atom y, frequen tly en coun - t ion , w ith an absolu te valu e of 7.4% few er poor ou tcom es in th e
tered anatom ic variants, vital perforat ing arteries, and close prox- en d ovascu lar coilin g grou p . Sim ilarly, t h e In ter n at ion al St u dy
im it y to th e opt ic apparat us can m ake an eur ysm s arising from of Un ru pt u red In t racran ial An eur ysm s (ISUIA), first publish ed in
th is locat ion ch allenging to t reat m icrosu rgically.7 More recen tly, 1998, aim ed to evaluate th e n at ural h istor y of un ru pt ured in t ra-
due to th e advan ces in en dovascu lar devices an d occlusion tech - cran ial an eur ysm s an d determ ine th eir risk of repair.8 Th is st udy
n iques, en dovascular t reat m en t of ACoA h as becom e a safe an d also por t rayed, in a p rospect ive fash ion , dat a from m ult iple cen -
effect ive t reat m en t opt ion for th e prop erly selected pat ien ts.8–15 ters regarding th e m orbidit y an d m or t alit y of an eur ysm t reat-
As w ith m icrosurgical clipping, there are significant challenges m en t . In it ial resu lt s revealed h igh er rates of su rgical m orbidit y
to en dovascular t reat m en t of ACoA an eur ysm s. Th e an eur ysm an d m or t alit y at 1 year th an previou sly publish ed, ranging from
dom e an d n eck orien tat ion , dom e-to-n eck rat io, an d overall size 13.1% to 15.7%. In 2003, an u pdate to th e ISUIA sh ow ed th at
p ose sign ifican t ch allenges for en d ovascu lar t reat m en t . Fu r- t reat m en t-related m orbidit y an d m or t alit y rem ain ed h igh er at
t h er m ore, th e h igh p revalen ce of adjacen t ACoA an om alies an d 1 year in th e clipping grou p at 12.6%, w h ereas th e en dovascular-
com plex h em odyn am ic flow p at tern s across th e ACoA fu r th er treated group rem ained low er at 9.8%.21 More recently, the Barrow
com plicate successfu l en dovascu lar t reat m en t . Rupt u red An eu r ysm Trial (BRAT), a single-cen ter, p rospect ive,
ran dom ized t rial evalu at ing en dovascular t reat m en t versus sur-
gical clip p ing, fou n d t h at en d ovascu lar t reat m en t resu lted in
10.5% absolu te few er p oor ou tcom es at 1 year.22 Th e resu lt s at
■ History 3 years, w h ich w ere recen tly pu blish ed, dem on st rated equ ipoise
En dovascu lar t reat m en t of in t racran ial an eu r ysm s began in th e bet w een m icrosurger y an d en dovascu lar th erapy for an eur ysm s
1970s w it h t h e u se of d et ach able latex balloon s.15 Alt h ough of th e an terior circu lat ion .23
t h ese balloon s w ere p r im ar ily u sed for p aren t vessel occlu sion , Th ese st u dies dem on st rated th e advan t ages of en dovascu lar
t h ere w ere select cases rep or ted of an eu r ysm occlu sion w it h t reat m en t (or at least equ ip oise) over su rgical clip p in g for a se-
preser vat ion of th e p aren t ar ter y. Fur th er effor ts u sing “push - lect grou p of p at ien t s. Th e on ly in for m at ion sp ecific to ACoA
able” det ach able coils w ere em ployed, bu t th eir unpredictable an eu r ysm s t h at cou ld be ext rap olated from t h e p reviou sly d is-
and uncontrollable nature led to uncertain outcom es.16 It was not cu ssed st udies w as th at ACoA an d an terior cerebral ar ter y an eu-
un t il th e adven t of th e Guglielm i detach able coil (GDC), w h ich r ysm s accou n ted for 12.3% of an eu r ysm s in ISUIA an d 45.4% of
m ay be rep osit ion ed or w ith draw n prior to fin al deploym en t , an eu r ysm s in ISAT.
th at coil em bolizat ion of in t racran ial an eu r ysm s becam e m ore Alth ough several st u dies h ave repor ted successful en dovascu -
predictable an d safer.10,17 lar occlusion of ACoA an eu r ysm s, few st udies h ave addressed th e
Th e rou t in e u se of coil em bolizat ion for t reat m en t of both com plex hem odynam ic flow, vessel anatom y, and aneur ysm m or-
rupt ured an d un r upt ured an eur ysm s h as been expan ding an d ph ology th at m ake su ccessfu l en dosaccu lar occlu sion of ACoA so
m any reports h ave cited th e safet y an d efficacy of en dovascular ch allenging. Birkn es et al9 w ere th e first to rep or t m orp h ological
tech n iqu es. Un for t un ately, m ost of th e early st u dies w ere ret ro- criteria for su ccessful en dovascular t reat m en t . Th is w as fur th er
spect ive, single-cen ter experien ces.18,19 Koivisto et al20 w ere th e exp an ded in 2008 by Gon zalez et al,24 w h o publish ed th e largest
first to publish a prospect ive, ran dom ized st udy com paring en - case series an alyzing t h e an atom ic ch aracterist ics resp on sible
dovascu lar versu s su rgical t reat m en t of ru pt u red in tracran ial for eith er com plete em bolizat ion or aneur ysm recan alizat ion .
an eur ysm s by assessing overall 1-year outcom es via th e Glasgow
Outcom e Scale (GOS). Even th ough th ere w as n o st at istically sig-
n ifican t differen ce in overall ou tcom es at 1 year bet w een th e en -
dovascu lar an d su rgically t reated p at ien ts, a good recover y w as
■ Incidence and Natural History
repor ted in 40 of th e 52 (76.9%) en dovascu lar pat ien t s com pared Alt h ough t h e t r u e in cid en ce of in t racran ial an eu r ysm s is u n -
w ith on ly 38 of th e 57 (66.7%) su rgical pat ien ts. Alth ough th is kn ow n , it is est im ated t h at 1% to 6% of t h e p op u lat ion h arbor
outcom e did n ot reach stat ist ical sign ifican ce, it did suggest th at t h ese lesion s, w ith an ter ior circu lat ion an eu r ysm s accou n t in g
favorable outcom es w ere possible using endovascular treatm ent. for up to 91% of all cases.3,21,24,25 St u dies h ave revealed th at th e

595

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596 V Cerebral and Spinal Aneurysms

m ost com m on site of in t racran ial an eu r ysm s an d m ost com m on diam eter th an th e A1 segm en t w ith m u lt ip le sm all p erforat ing
locat ion of an eu r ysm ru pt u re is th e ACoA. Th e origin al Coop era- bran ch es origin at ing from th e su perior an d posterior surface to
t ive St u dy of In t racran ial An eu r ysm s an d Su barach n oid Hem or- su p ply th e su prach iasm at ic area of th e hypoth alam u s, an terior
rh age repor ted th at 30.3% of th e 2,349 an eu r ysm s w ere ACoA perforate su bst an ce, an d opt ic ch iasm .31 Variat ion s can be fou n d
an eur ysm s.2 Sim ilarly, th e in cid en ce of ACoA an eu r ysm s in th e in th e ACoA arter y in 8 to 20% of cases.3 Not u n com m on ly th ese
In tern at ion al Cooperat ive St udy on th e Tim ing of An eur ysm Sur- variat ion s are duplicat ion s (30%), t riplicat ion s (10%), aplasia, hy-
ger y w as 39%.1 pop lasia, or fen est rat ion s of th e ACoA arter y.29
Th e n at u ral h istor y of ACoA an eu r ysm r u pt u re ten ds to be Th e ACA con t in u es rost rally from th e ACoA in t h e in terh em i-
poor. In 1966, Locksley,2 in th e Coop erat ive St u dy, rep or ted a spheric fissure un t il term in at ing at th e jun ct ion of th e rost r um
15.2% death rate for r upt ured ACoA an eur ysm s, com pared w ith an d gen u of th e corpus callosum , w h ich is called th e A2 segm en t .
less th an 10% for oth er an terior circulat ion r u pt u red an eur ysm s. Th e m ost im p or t an t of th e p erforat ing ar teries origin at ing from
Also, th e risk of reru pt u re of ACoA an eur ysm s in w eeks 5 th rough t h e d ist al A1 (78%), p roxim al A2 (14%), or ACoA (8%) segm en t
12 w as 2.6%per w eek, t w ice as high as that of other anterior circu- is th e m edial st riate ar ter y, also kn ow n as th e recurren t ar ter y
lation aneurysm s. Sim ilarly, the International Cooperative Study of Heubn er.29 W h en arising from A2, th e m edial st riate ar ter y is
repor ted p oorer ou tcom es after ru pt u re of ACoA an eur ysm s. t ypically t h e largest vessel. It origin ates from t h e superolateral
Alth ough th ere is con siderable disparit y bet w een th e data on aspect of th e ACA an d courses parallel to th e A1 segm en t tow ard
th e rep or ted p revalen ce of u n ru pt u red in t racran ial an eu r ysm s, t h e carot id bifu rcat ion before su p p lyin g t h e p u t am en , cau date
th ere is som e evid en ce suggest ing th at an eu r ysm s of th e ACoA n u cleu s, exter n al segm en t of t h e globu s p allid u s, an d an ter ior
h ave a h igh er risk of rupt ure.1,13,26 Mira et al27 con du cted a m eta- lim b of in ter n al cap su le.31 Dam age to t h is vessel can resu lt in
an alysis of over 1,400 un r upt ured ACoA an eur ysm s. Th ey foun d con t ralateral h em ip aresis of th e u p p er ext rem it y an d face, an d
th at alth ough th e ISUIA did n ot recogn ize ACoA an eu r ysm s as exp ressive aph asia if inju red on th e dom in an t h em isp h ere. Th e
h aving a h igh er risk of r upt ure, th eir an alysis sh ow ed th at th e orbitofron tal ar ter y also arises from A2 bu t courses perpen dicu-
risk of ru pt u re of ACoA an eu r ysm s is at least t w ice as h igh as th at larly over the gyrus rectus and across the olfactory tract. The next
of oth er in t racran ial an eur ysm s. Fur th erm ore, 94.5%of ACoA an - m ajor bran ch arising from A2 is th e fron top olar ar ter y, w h ich
eu r ysm s cau sing ru pt u re are less th an 10 m m , 46% are less th an t ravels along th e m edial surface of th e fron t al lobe an d crosses
6 m m , an d u p to 32% are less t h an 4 m m . Moreover, Okuyam a th e subfron t al sulcu s.
et al28 com p ared rates of an eu r ysm al ru pt u re in differen t loca-
t ion s an d fou n d th at ACoA an eu r ysm s reach ed 55% of th eir r u p -
t u re in ciden ce rate at 3 m m , suggest ing th at ACoA an eu r ysm s
h ave an in creased risk of ru pt u re regardless of size.
■ Clinical and Radiographic Presentations
As w it h ot h er in t racran ial an eu r ysm s, p at ien t s w it h an eu r ysm s
of t h e ACoA ten d to presen t w ith spon tan eous h em orrh age, in ci-
dentally, or less often as a result from m ass effect. Although spon -
■ Anatomy taneous hem orrhage caused by ACoA is prim arily aneurysm al
Th e com p licated ar terial an atom y of th e ACoA com p lex can p re- SAH, oth er t ypes of h em orrh age can occur. In t racerebral h em or-
sen t a tech n ical ch allenge w h en t reat ing an eu r ysm s in th is loca- rhage, interhem ispheric clot, and intraventricular hem orrhage are
t ion . Su ccessfu l en dovascu lar em bolizat ion of ACoA an eu r ysm s all frequ en tly en coun tered, fou n d to be presen t in 79%of cases.32
dem an ds a th orough th ree-dim en sion al (3D) u n derstan d ing of Th e clin ical presen t at ion of an eu r ysm al SAH is review ed in
th is com plex an atom y, as w ell as kn ow ledge of th e frequ en t vas- Ch apter 39; h ow ever, a few key poin t s w ill be addressed h ere.
cu lar an atom ic variat ion s en coun tered. Hypon at rem ia occurs m ore com m on ly in pat ien ts w ith ru pt ured
Th e an terior cerebral ar ter y (ACA) is bilateral an d arises at th e ACoA an eur ysm s w h en com pared w ith rupt ured an eur ysm s in
term in at ion of th e in tern al carot id ar ter y (ICA), t ypically as th e ot h er locat ion s, likely secon dar y to t h e close p roxim it y of t h e
sm aller an d m ore m ed ial ICA ter m in at ion . From it s or igin to ACoA to t h e hyp ot h alam u s.33 Also, r u pt u red ACoA an eu r ysm s
t h e ACoA, th e A1 segm en t , it cou rses an terom ed ially in a h ori- com m on ly are associated w ith cogn it ive dysfu n ct ion , referred to
zon tal plan e bet w een th e opt ic ch iasm an d olfactor y t rigon e. as th e ACom syn drom e.11 Feat ures of th is syn drom e are at t rib -
Perlm u t ter an d Rh oton 29 describe th e A1 segm en t on average as u ted to injur y to th e basal forebrain an d con sist of person alit y
being 13 m m in length , but it can range from 7 to 18 m m . Th ey ch an ges, sh or t -ter m m em or y im p air m en t , an d a ten d en cy to
also defin ed a hypoplastic A1 segm en t , w h ich can be en cou n - con fabu late. Un com m on ly, gian t ACoA an eu r ysm s can cau se bi-
tered in 10%of cases, as less th an 1.5 m m in diam eter. In addit ion , tem poral h em ian opsia from com pression of th e opt ic ch iasm .
a du plicate A1 segm en t can occur in 2% of cases. Because th e Radiograph ically, ACoA an eu r ysm s can h ave dist in ct ive blood
base of ACoA an eur ysm s t ypically occurs on th e side of th e dom - pat tern s on com p u ted tom ograp hy (CT) th at can be h igh ly sug-
in an t A1, w ith th e dom e poin t ing tow ard t h e hypoplast ic seg- gest ive of th e diagn osis. Isolated clot or su barach n oid blood in
m en t , it is im port an t to un derstan d th at in th e presen ce of ACoA the interhem ispheric fissure or an intraparenchym al hem orrhage
an eur ysm s th e paired A1 segm en t s are of un equal diam eter m ore in th e region of th e gyru s rect us is predict ive of an ACoA ru pt ure
th an 85% of th e t im e.29,30 (Fig. 51.1).
Th e ACoA ar ter y is su rrou n ded in feriorly by th e ch iasm at ic An oth er radiograph ic ch aracterist ic of ACoA an eur ysm s is
cistern, superiorly by the lam ina term inalis, posteriorly by the pial th at th ey h ave th e h igh est false-n egat ive rate angiograp h ically
su rface of th e lam in a term in alis, an d laterally by th e p ial su rface w h en subarach n oid blood is presen t . Iw an aga et al34 fou n d th at
of th e m edial fron tal lobe. Th e ACoA ar ter y is t ypically sm aller in out of 469 pat ien ts w ith SAH, 38 w ere n egat ive for an eur ysm .

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51 Endovascular Therapies for Anterior Communicating Artery Aneurysms 597

(w orking view ) secon dar y to m ult iple ar terial bran ch es arising


n ear th e an eur ysm . Visualizat ion of both ICAs is n ecessar y to de-
term in e th e side filling th e an eur ysm an d th u s th e side for en do-
vascu lar t reat m en t , as w ell as to recogn ize any absen ce of t h e
A1 segm en t. Th e absen ce of an A1 segm en t n eeds to be assessed
before em bolizat ion of th e an eu r ysm is perform ed, as preser va-
t ion of th e ACoA is vit al to filling of th e con t ralateral A2 segm en t .
Alth ough an absen t A1 segm en t is n ot a con t rain dicat ion to en -
d ovascu lar t reat m en t , it n eed s to be ap p roach ed w it h cau t ion ,
as any com prom ise to th e ACoA ar ter y m ay result in deleterious
effects.
Along w ith m ult iple clin ical an d pat ien t variables, an alysis of
ACoA an eur ysm m orph ology is vital w h en determ in ing th e best
t reat m en t for th e pat ien t . Even w ith m u lt iple ap p roach es to t reat
w ide-n ecked an eu r ysm s, it h as long been determ in ed th at th e
m ain lim it ing factor for successfu l en dovascu lar em bolizat ion of
in t racran ial an eu r ysm s is th e an eur ysm n eck size.21 Alth ough
aneurysm m orphology and the success of endovascular treatm ent
h ad been discussed in th e literat ure, it w as n ot un t il Birkn es et
al9 an d later Gon zalez et al24 est ablish ed th e an atom ic variables
to guide in est im at ing th e probabilit y of successfu l en dovascu lar
t reat m en t of ACoA an eu r ysm s. Birkn es et al ret rospect ively an a-
lyzed 123 ACoA an eu r ysm s an d classified an eu r ysm m orp h ology
based on th e project ion of the an eur ysm an d th e n eck size. Th ey
con clu ded th at a sm all n eck (< 4 m m ) an d an terior p roject ing
an eur ysm s w h ere am en able to en dovascular coil em bolizat ion
Fig. 51.1 Computed tom ography (CT) scan dem onstrating acute sub 90% of th e t im e w ith 0% recan alizat ion , w ith a m ean follow -up
arachnoid hem orrhage (SAH) within the interhem ispheric fissure, intra of 8.6 m on th s. Altern at ively, in ferior p roject ing an eu r ysm s w ith
parenchym al hem orrhage in the gyrus rectus, and a flam e hemorrhage in
w ide n ecks (≥ 4 m m ) h ad a low rate of successful em bolizat ion
the right frontal lobe.
(40%) an d a 100% recan alizat ion rate. Th e successful em boliza-
t ion an d recan alizat ion rates of th e oth er m orp h ological classifi-
Repeat angiogram s on th e 38 pat ien ts fou n d th at eigh t (21%) an - cations fell in bet w een. Com plete or near-com plete occlusion w as
giogram s w ere posit ive for an eur ysm , seven of w h ich w ere foun d at tain ed in 87.8% of p at ien ts, w h ereas su ccessfu l em bolizat ion
to be ACoA an eu r ysm s. Sim ilarly, van Rooij et al35 foun d th at re- w as ach ieved in 69.9% of p at ien t s.
peat angiography in 18 of 23 p at ien ts, w ith in it ial n egat ive d igi- Sim ilarly, Gon zalez et al24 perform ed a ret rospect ive review
tal su bt ract ion angiograp hy, dem on st rated th at 11 (61%) of th e of 181 ACoA an eur ysm s t reated w ith en dovascular coil em boli-
18 w ere ACoA an eur ysm s. ACoA an eu r ysm s m ay n ot be visual- zat ion . An eu r ysm s w ere an alyzed for th e direct ion of th e dom e,
ized on angiography becau se of flow com p et it ion p h en om en a th e locat ion of th e n eck, th e associat ion w ith hyp op lasia or ap la-
from th e con t ralateral A1 segm en t , an d in th ese in st an ces com - sia of th e ACoA com plex, an d th e dom e an d n eck size to p redict
pression of th e con t ralateral ICA du ring inject ion m ay be h elpfu l. su ccessfu l en dovascu lar t reat m en t . Th e au th ors fou n d th at an
Due to th e h igh prevalen ce of ACoA an eur ysm s foun d on repeat an eur ysm size < 10 m m , a sm all n eck size (< 4 m m ), an d an terior
angiography after an in it ial n egat ive digit al subt ract ion angio- d om e p roject ion w ere p redictors of com p lete em bolizat ion .
gram , on e n eeds to h ave a h igh level of su sp icion for ACoA an eu - Conversely, th ey foun d th at dom e size ≥ 10 m m , posterior dom e
r ysm s, especially in th e presen ce of it s dist in ct ive blood pat tern or ien t at ion , n eck locat ion on t h e ACoA, an d in com p lete in it ial
on CT. em bolizat ion w ere all associated w ith an eu r ysm recan alizat ion .
Even w ith th e tech n ological advan cem en t in en dovascu lar
devices an d tech n iqu es, su ch as com plian t m icroballoon s, em -
bolic agen ts, flow diver ters, an d n eu rodedicated self-expan ding
sten t s, th ere are lim it at ion s in th e en dovascu lar t reat m en t of
■ Anatomic and Morphological ACoA an eu r ysm s, an d an eur ysm m orph ology sh ould be con sid-
Considerations for Endovascular ered in pred ict ing th e su ccess of t reat m en t .
Treatment
In addit ion to th e frequen t vascular an om alies previously dis-
cussed, th ere are oth er an atom ic ch allenges ren dering cath eter-
izat ion an d u lt im ately en dovascu lar em bolizat ion of ACoA an eu -
■ Endovascular Techniques
r ysm s difficult . Such factors th at can arise are difficult cath eter Alth ough coil em bolizat ion is th e prim ar y m eth od of en dovascu-
access due to th e acute angle form ed by th e ICA an d A1 segm en t , lar t reat m en t of ACoA an eu r ysm s, th ere are oth er en dovascu lar
tor t uosit y of th e A1-A2 segm en ts, th e relat ive sm all size of m any devices an d tech n iqu es th at aid in th e t reat m en t of ACoA an eu -
ACoA an eur ysm s, an d difficult y in acquiring adequate im aging r ysm s. Th e differen t m orph ologies of ACoA an eu r ysm som etim es

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598 V Cerebral and Spinal Aneurysms

require m u lt ip le en dovascu lar tech n iqu es for successfu l t reat- Stent-Assisted Coil Embolization
m en t . This sect ion discu sses th e differen t devices, st rategies, an d
tech n iques used to t reat th e variet y of an atom ically an d m or- Mu lt ip le st rategies h ave been devised to t reat w ide-n ecked an -
ph ologically d ifferen t ACoA an eu r ysm s, as w ell as t h e p oten t ial eu r ysm s of th e ACoA ar ter y, on e of w h ich is sten t-assisted coil
com plicat ion s. em bolizat ion .36,37 Despite th e evolu t ion of n avigat ion frien dly
Su ccessfu l en dovascu lar em bolizat ion of ACoA an eu r ysm s, as sten t s, sten t placem en t can be p ar t icu larly difficu lt an d of lim -
w ith all aneurysm s, begins w ith qualit y visualization of the neck, ited use in ACoA an eur ysm s, par t ially d ue to th e sh or t length of
dom e, an d su rrou n ding vascu lat ure. As previou sly discussed, bi- th e ACoA.38 Fur th erm ore, in th e presen ce of r upt ured ACoA an -
lateral ICA inject ion s n ot on ly en able iden t ifying th e absen ce of eu r ysm s, sten t p lacem en t becom es less p ract ical as du al an t i-
an A1 segm en t but also determ in e th e side filling th e an eu r ysm platelet agen t s are requ ired. Sten t-assisted coil em bolizat ion of
an d th us th e side for en dovascular t reat m en t . In it ial assessm en t rupt ured ACoA an eur ysm s sh ould be prim arily reser ved for use
of th e diam eters of th e A1, A2, an d ACoA sh ou ld be con sidered if as a rescu e tech n ique. On e in dicat ion for u sing sten t-assisted
th e p oten t ial exist s for sten t-assisted coiling, as diam eters n eed coiling in th e set t ing of an eu r ysm r u pt u re is w h en coil m asses
to be > 2 m m to accom m odate sten t p lacem en t . h ern iate in to th e paren t vessel or vessel th rom bosis occurs an d
sten t placem en t is u sed to ach ieve vessel paten cy.
Th ere are m u lt iple tech n ical n u an ces to sten t deploym en t for
Primary Coil Embolization ACoA an eu r ysm s. As discussed, an atom ic variat ion s n eed to be
Coil em bolizat ion of ACoA an eu r ysm s rem ain s th e m ost com - taken in to accoun t as w ell as th e locat ion of th e an eur ysm n eck,
m on en dovascular t reat m en t for m ult iple reason s (Fig. 51.2).10 as th is affect s th e st rategy an d success of sten t placem en t . Sizing
Alth ough sten t in g an d rem od elin g tech n iqu es are feasible, t h ey of th e sten t is of ut m ost im por tan ce, as oversized sten ts can pro-
can be d ifficu lt to n avigate t h rough t h e p oten t ially tor t u ou s A1 m ote sten osis or th rom bosis w ith in th e sten t . In th e rare occur-
segm en t . Fu r th erm ore, in th e p resen ce of SAH, th e risks of long- ren ce of sten t dep loym en t for rupt u red ACoA an eu r ysm s, th e
term an t iplatelet th erapy after sten t deploym en t m ust be taken probabilit y of u n dersizing th e sten t is h igh er du e to poten t ial
in to con siderat ion . vessel spasm .38 An oth er variable th at n eeds to be accoun ted for
At m ost cen ters, th e t reat m en t of cerebral an eur ysm s is don e is sten t d esign . Self-exp an dable closed -cell sten t s (En ter p r ise,
under general anesthesia, w hich ensures m ore controlled patient Cord is, Miam i, FL) con form bet ter to tor t u ou s vascu lat u re an d
m an agem en t an d bet ter im aging qu alit y, p ar t icu larly im por tan t m ain t ain a con st an t cell op en in g at t h e convexit y of a vessel
w h en n avigat ing tor t uous an atom y of sm all-caliber vessels an d cur ve, so th at th e risk of prot rusion out side th e paren t vessel
catheterizing sm all rupt ured aneur ysm s. Neurom on itoring is fre- lu m en or in to an an eu r ysm n eck is low er; also, th e sten t can be
qu en tly u sed w h en p at ien t s are u n der gen eral an esth esia to en - recapt ured in to th e cath eter for reposit ion ing. Conversely, open -
h an ce th e safet y of th e en d ovascu lar t reat m en t of an eur ysm s. cell sten ts (Neuroform , Boston Scien t ific, Nat ick, MA) are less
At ou r in st it ut ion , an eur ysm s are t ypically em bolized th rough n avigable, en tail th e risk of in -sten t sten osis due to possible pro-
a 6-Fren ch gu ide cath eter using con t in uous flush an d a hydro- t ru sion of sten t st r u ts in to th e an eu r ysm , an d can n ot be recap -
p h ilic gu id ew ire. W h en t h e gu id e cat h eter is w it h in t h e ICA, t u red for reposit ion ing.
a soft -t ip p ed m icro-gu idew ire is u sed to steer a m icrocat h eter On ce t h e sten t is d ep loyed across t h e an eu r ysm n eck, t h e
in to t h e an eu r ysm . Th e m icro -gu id ew ire, an d u lt im ately t h e an eur ysm is coiled by n avigat ing th e m icrocath eter th rough th e
cath eter, is slow ly advan ced in to th e an eu r ysm u n der “roadm ap” sten t an d in to th e an eu r ysm . An oth er tech n iqu e th at can be im -
set t ings. Coils are th en dep loyed in to th e an eu r ysm u n der direct plem en ted is referred to as “jailing,” w h ich en t ails p in n ing th e
real-t im e fluoroscopic gu idan ce. Depen ding on th e an eur ysm m icrocath eter bet w een t h e vessel w all an d sten t to en h an ce
sh ap e an d size, w e start w ith com p lex fram ing coils follow ed by t h e stabilizat ion of th e m icrocath eter du ring coil deliver y. How -
softer packing coils to ach ieve an eu r ysm occlu sion . Th e first coil ever, th e n ew ly deployed sten t m ay n ot be fully im plan ted in th e
selected sh ou ld be th e largest coil dep loyed, an d it ser ves to paren t vessel; coil loop s m ay be in ciden t ally pu sh ed bet w een
fram e th e th eoret ical bou n daries of th e an eu r ysm . Ap p rop riately th e vessel w all an d th e sten t . Som e au t h ors, th erefore, prefer
sized sm aller an d softer coils are th en delivered to fill th e in ter- su bsequ en t coiling in a secon d session for elect ive u n ru pt u red
st ices of th e an eur ysm u n der m ask angiography. Th e progressive an eur ysm s. Also, n ew ly deployed sten ts can st ill m ove, an d cau -
coiling of th e an eu r ysm dom e lead s to st agn at ion of flow, pro- t ion m u st be taken w h en th e sten t is reen tered w ith a m icro-
m otes th rom bosis, an d isolates th e an eur ysm from th e arterial cath eter.
circulat ion . Waffle-con ing is a tech n ique used for em bolizat ion of w ide-
W h en a tor t u ou s A1 segm en t is en cou n tered, th e m icrocath - n ecked an eur ysm s. Th is tech n ique con sist s of deploym en t of th e
eter t ip can be steam sh ap ed for easier n egot iat ion or it can be dist al segm en t of th e sten t w ith in th e an eu r ysm sac.37,38 Dis-
exch anged for a differen t angled m icrocath eter. Oth er devices, advan t ages of th is procedure are r upt ure of th e an eur ysm upon
su ch as th e DAC (d ist al access cat h eter, Con cen t r ic Med ical, deploym en t of th e sten t an d poten t ial flow d iversion in to th e
Mou n t ain View, CA), can add ext ra st abilit y to th e m icrocath eter an eur ysm , th u s cau sing in creased rates of recan alizat ion .
for im proved n avigat ion an d added suppor t to h elp redu ce m i- Oth er tech n iques h ave been recen tly publish ed in th e litera-
crocath eter “kickback” during coiling. t ure. Saatci et al39 repor ted a n ovel tech n iqu e of an X-con figu red
Given th at throm boem bolic com plications constitute th e m ajor sten t-assisted coiling in a series of five w ide-n ecked ACoA an eu-
risk to p at ien t s u n dergoing en dovascu lar coil em bolizat ion of in - rysm s. Their technique consisted of jailing a m icrocatheter w ithin
t racran ial an eu r ysm s, an t icoagu lat ion du ring t reat m en t is em - th e an eu r ysm by deploying on e sten t from th e con t ralateral A2
ployed at m ost cen ters w ith in t raven ou s h ep arin w ith var ying to th e ipsilateral A1. Th e secon d sten t w as th en deployed, via th e
regim en across in st it ut ion s. con t ralateral ICA, from th e con t ralateral A2 to th e ipsilateral A1.

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51 Endovascular Therapies for Anterior Communicating Artery Aneurysms 599

a b

Fig. 51.2a,b Ruptured anterior com m unicating artery (ACoA) aneurysm aneurysm with m icrocatheter navigated through the left A1 and catheter
treated with coil em bolization. (a) Anteroposterior (AP) projection of left izing the aneurysm . (b) Postcoiling AP angiography dem onstrating com
internal carotid artery (ICA) injection angiography dem onstrating an ACoA plete occlusion of the aneurysm with good packing densit y.

They had no technical failures or adverse events using this m ethod difficu lt y is en cou n tered as w ith sten t deploym en t—n avigat ing a
of d u al sten t p lacem en t . Th ey also d em on st rated com p lete an - relat ively rigid device in to tor t u ou s vessels—an d system ic an t i-
eu r ysm occlu sion w ith a m in im u m of 6 m on th s of follow -u p. coagulat ion du ring balloon in flat ion is required.
Com plex aneur ysm s requiring these tech nically challenging endo- Variat ion s of balloon -assisted coil em bolizat ion , specific to
vascu lar procedures, w ith poten t ially devast at ing com plicat ion s, ACoA an eur ysm s, in clu de driving a m icrocath eter in to on e A1
should be strongly evaluated by the neurosurgeon for craniotom y segm en t w h ile th e balloon cath eter is gu ided in to th e con t ralat-
an d clip ligat ion . eral A1 segm en t . Addit ion ally, th e “kissing” balloon tech n iqu e
All of t h e aforem en t ion ed tech n iqu es are n ot w it h ou t r isk. en t ails cath eterizat ion of both A1 segm en t s w ith balloon s w h ile
In addit ion to accept ing th e risks of cath eterizat ion an d long- a th ird m icrocath eter is used to coil th e an eu r ysm .42
term dual an t ip latelet th erapy, sten t ing h as its ow n in h eren t Again , alth ough th ese tech n iqu es are n ovel an d tech n ically
risks. Navigat ing t h e tor t u ou s vessels w ith st iff sten t system s can ch allenging, th eir risks n eed to be assessed again st th e risk of
in crease th e risk of an eu r ysm ru pt ure as m icro-guid ew ires or cran iotom y an d clip ligat ion . Th is is esp ecially im p or t an t in
m icrocath eters m ay en d up w ith in th e an eu r ysm . Also, because w ide- n ecked an eu r ysm s in w h ich th e poin t of ru pt u re, defin ed
of vessel tor t uosit y, sten t s m ay ret ract an d in adver ten tly be de- by a bleb or a daugh ter an eur ysm , is close to th e an eur ysm n eck.
ployed w ith in th e an eu r ysm , direct ing flow in to th e an eu r ysm In flat ion of th e balloon m ay reru pt u re th e an eu r ysm w ith lit t le
sac. Fu r th erm ore, som e sten ts, su ch as th e Neu roform , are d e- con t rol or p rotect ion by en dovascu lar tech n iqu es. How ever, du e
sign ed to be t racked over an exch ange-length m icrow ire, an d to im provem en ts in coil tech n ology an d th e in t roduct ion of th e
th ese exch anges can be tech n ically difficu lt , in creasing th e risk 3D com plex fram ing coil, th is tech n iqu e is u sed less frequen tly.
of an eur ysm ru pt u re.

Double Catheter Technique


Balloon-Assisted Coil Embolization Th e double cath eter tech nique con sists of using t w o m icrocathe-
Balloon-assisted coil em bolization or rem odeling is a new er tech- ters to sim ultaneously place coils in to a w ide-n ecked an eur ysm .43
n ique first described in 1997 by Moret’s group 40 an d discu ssed Th is tech n iqu e is based on th e con cept of secu rely bracing coils
fu r t h er in 2009,41 w h ich h as sh ow n to be ben eficial in occlu sion besid e on e an ot h er to ach ieve a st able con figu rat ion . Placing
of w ide-n ecked aneu r ysm s. Th e prem ise is to create suppor t in t w o m icrocath eters w ith in th e an eu r ysm en ables t w o coils to be
th e p aren t ar ter y via a balloon w h ile fram ing coils are deployed posit ion ed an d th eir stabilit y assessed before eith er coil is de-
w ithin the aneurysm . This w ill create stable “scaffolding” for w hich tach ed. A side-by-side con figu rat ion of coils is fash ion ed across
fu t u re coils can be in ser ted in to th e an eu r ysm . Again , th e sam e th e n eck of th e an eu r ysm , ad ding addit ion al su pp or t , w h ich pre-

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600 V Cerebral and Spinal Aneurysms

ven t s th e coils from h ern iat ing in to th e paren t vessel. Th is tech -


n ique again requ ires n avigat ion of t w o cath eters sim ultan eou sly
in to sm all an d tor t u ou s vessels or con cu rren t cath eterizat ion of
bilateral A1 segm en ts. Again , th e in creased tech n ical dem an ds
an d potent ial for com plicat ion s n ecessitate con siderat ion of oth er
altern at ives in cluding m icrosu rgical clipp ing.

Partial Coiling
Part ial coiling is a st rategy u sed to t reat com plex ru pt ured cere-
bral an eur ysm s th at are n ot am en able to clipping an d can n ot be
coiled p rim arily (Fig. 51.3). Th e prem ise of par t ial coiling is to
protect again st reh em orrh age in th e acu te set t ing an d offer fu r-
th er t reat m en t, if n ecessar y, in th e fu t u re. As p reviou sly stated,
som e ru pt u red an eu r ysm s are n ot am en able to en dovascu lar
t reat m en t becau se of th e n eed for sten t p lacem en t an d an t i-
platelet agen t s. Also, su rgical t reat m en t in th e set t ing of SAH is
difficu lt du e to brain sw elling an d in creased in t racran ial p res-
su re, as w ell as th e p at ien t’s p oor n eu rologic st at u s. Waldau et
al44 p u blish ed data from th ree cen ters on 15 p at ien ts w ith ru p -
t u red an eu r ysm s (53% w ere ACoA or p osterior com m u n icat ing
ar ter y an eur ysm s), w ith th e in ten t ion of t reat m en t being par t ial Fig. 51.3 An anteroposterior digital subtraction angiography (DSA) image
coiling for dom e p rotect ion . Th e 15 an eu r ysm s th at w ere in ten - of a right internal carotid artery (ICA) injection showing partially coiled
t ion ally p ar t ially coiled w ere ch osen from 428 con secu t ive ru p - sm all anterior com m unicating artery (ACoA) aneurysm with migrated coil
(arrow) lodged in the distal pericallosal artery. Fortunately, the patient had
t u red an eu r ysm s over a 4½-year t im e p eriod. In tot al, six of th e
excellent collateral circulation and did not suffer any neurologic sequela
15 an eur ysm s (40%) h ad a daugh ter sack w ith an average n eck from coil dislodgm ent.
size of 4.88 m m . An average of 92 days p assed bet w een in it ial
coiling an d defin it ive t reat m en t . Fift y-th ree percen t of th e an eu -
r ysm s w ere clipped after in ten t ion al part ial coiling, 33% un der- m on . Guglielm i et al11 foun d th at of 306 con secut ive ACoA an eu-
w en t sten t-assisted coiling, an d 7% u n der w en t fu r th er coiling or r ysm s t reated, on ly eigh t (2.6%) w ere gian t an eur ysm s. Th e
Onyx (Covidien ev3 Neurovascular, Ir vin e, CA) em bolizat ion . Th e reason for th eir rarit y is un kn ow n bu t it h as been post ulated th at
authors repor ted n o cases of rebleeding in 6 m on th s to 3 years of it m ay be due to th e h igh er rate of rupt u re of sm aller ACoA an eu-
follow -up after th e defin it ive t reat m en t . As th e auth ors ackn ow l- r ysm s.46 How ever, th e risk of an n u al r u pt u re of ACoA an eu r ysm s
edged, there are a few potential concerns using this technique, one is subst an t ial, w ith th e ISUIA assessing a risk of 8% ru pt u re per
being that aneur ysm s can still rupture after partial coiling, and year for gian t ACoA an eu r ysm s. As previou sly d iscu ssed, w h en
protect ing th e dom e does n ot alw ays p rotect again st reru pt u re. an ACoA an eur ysm reach es a gian t size th ere m ay be resultan t
com p ression of opt ic app arat u s an d or basal forebrain . Un for t u -
nately, endovascular treatm ent relieves the sym ptom s from m ass
Complications effect in only half of the cases and can frequently worsen the
Potential com plications of ACoA aneurysm coil em bolization have sym ptom s.19,47
been discussed relat ive to th e specific en dovascular tech n iques Regardless of t reat m en t m odalit y, gian t an eu r ysm s are ch al-
an d devices used. Oth er poten t ial com plicat ion s of en dovascular lenging to t reat . W h en en dovascu lar t reat m en t s are ut ilized th ey
t reat m en t of ACoA an eu r ysm s are briefly discu ssed h ere, as th e often require m ult iple procedures, w ith m ore th an h alf of gian t
com p licat ion s are sim ilar to th ose of oth er locat ion s. An eu r ysm an eu r ysm s t h at u n d ergo en d ovascu lar em bolizat ion sh ow ing
or vessel perforat ion w ith th e m icrow ire, m icrocath eter, or coil is recu rren ce an d n eeding su bsequ en t recoiling.19,48 En dovascu lar
a com m on com plicat ion th at is m ore prevalen t w h en using de- ap p roach es for gian t ACoA an eu r ysm s con sist of p r im ar y coil-
vices such as balloon s or sten ts. Sym ptom at ic th rom boem bolism ing, paren t-vessel sacrifice, sten t-assisted coiling, em bolic agen ts,
is en coun tered in 3.8 to 9% of cases, m ore com m on ly in w ide- covered sten ts, an d flow diver ters.
n ecked an eur ysm s, w h en balloon -assisted coiling tech n iques are Giant aneurysm s have a high prevalence of intralum inal throm -
u sed, or w h en th ere is h ern iat ion of coils in to th e paren t vessel.45 bus, an d gian t ACoA an eur ysm s are n o differen t . In t ralu m in al
Oth er poten t ial com plicat ion s are vessel dissect ion , coil dislodg- th rom bu s can be p roblem at ic for p rim ar y coil em bolizat ion du e
m en t , an d coil st retch ing. to th e coil m ass frequen tly “set tling” in to th e in t ralum in al clot ,
requiring a large n u m ber of coils as w ell as h aving a h igh preva-
len ce of recanalization.14,49 Also, em boli from in trasaccular throm -
bosis or progressive th rom bosis from th e sac can exten d beyon d
■ Endovascular Treatment of th e an eur ysm in to th e paren t ar ter y, result ing in vessel occlu-
sion . Fu r th erm ore, som e pu blish ed series h ave fou n d , u sing th e
Giant Aneurysms GDC m et h od , t h at su fficien t an eu r ysm occlu sion w as reach ed
Even th ough ACoA an eur ysm s are th e m ost frequen tly en coun - in on ly 50% of gian t an eu r ysm s along w ith p ost- GDC t reat m en t
tered an eur ysm s, gian t (> 2.5 cm ) ACoA an eur ysm s are un com - h em orrh age rates of 6.5% to 33%.19 Mu rayam a et al14 foun d th at

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51 Endovascular Therapies for Anterior Communicating Artery Aneurysms 601

in 916 aneurysm s treated over 11 years, com plete occlusion could creases an d th e literat ure suppor t ing th ese devices grow s, likely
be achieved in only 26%of giant aneur ysm s, com pared w ith com - so w ill th eir usage.51
plete occlu sion in 75.4% of sm all an eu r ysm s (4 to 10 m m , n eck
< 4 m m ). Jah rom i an d colleagu es 49 pu blish ed long-term clin ical
an d radiological follow -up on 39 gian t an eu r ysm s t reated by en -
dovascu lar em bolizat ion . At 21 m on th s, com plete occlu sion w as ■ Endovascular Treatment of
seen in 36%, w ith 64% sh ow ing greater th an 95% occlu sion .
Paren t vessel sacrifice is an establish ed app roach for th e t reat-
Small Aneurysms
m ent of giant aneur ysm s w hen the aneurysm neck is arising from Endovascular coil em bolization of sm all (< 3 m m ) an eur ysm s, in -
t h e ACoA com p lex, or after byp ass su rger y. Cu r ren t ly, flow d i- cluding ACoA aneurysm s, is dem anding and entails a higher risk of
version devices are being u sed m ore frequ en t ly w ith su ccess for aneurysm perforation than does larger aneurysm s (Fig. 51.4). Due
th e t reat m en t of gian t ACoA an eu r ysm s.49,50 As operator use in - to the potentially high com plication rate, endovascular t reat m en t

a b

Fig . 51.4a–c Sm all anterior com m unicating artery (ACoA) aneurysm .


(a) Three dim ensional (3D) rotational angiography from a left internal ca
rotid artery (ICA) injection helps determ ine the relationship of this sm all
(2.4 m m) ruptured ACoA aneurysm to the parent vessel. (b) Anteroposte-
rior projection showing the m icrocatheter position inside the aneurysm .
c (c) Postcoiling injection showing complete occlusion of the aneurysm .

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602 V Cerebral and Spinal Aneurysms

of ACoA an eur ysm s sm aller th an 3 m m h as been con t roversial.52 clin ical resu lt s as th e m ost favored resu lt s pu blish ed in th e lit-
Slu zew ski et al53 w ere t h e first to d em on st rate t h at sm all an eu - erat ure (0% m or talit y, 1.7% m orbidit y, an d 95% tot al occlusion ).
r ysm size w as a risk factor for p roced u re-related r u pt u re. How -
ever, Su zu ki et al52 t reated 21 pat ien ts w ith sm all (< 3 m m ) r u p -
t ured an eur ysm s, 11 of w h ich w h ere ACoA an eu r ysm s. Th ey
sh ow ed com plete an eu r ysm obliterat ion w ith ou t subsequent ■ Endovascular Treatment of Aneurysms
procedural rupture. Tsutsum i et al54 reported a series of 19 rup -
t u red sm all (< 3 m m ) ACoA an eu r ysm s an d fou n d n o an eur ysm After Hemorrhage
perforat ions or procedure-related com plication s. Com plete an d Th e efficacy of en d ovascu lar em bolizat ion of r u pt u red in t ra-
n ear-com plete occlusion w as obser ved in 16 pat ien t s (84.2%) cran ial an eu r ysm s w as p reviou sly ad d ressed by t h e ISAT an d
an d th ree pat ien ts (15.8%), respect ively. Th is h elped con fir m BRAT. Sp ecific to ru pt u red ACoA an eu r ysm s, st u dies h ave sh ow n
t h at alt h ough sm all an eu r ysm s are ch allen gin g to t reat , t h ey th at en d ovascu lar t reat m en t of r u pt u red ACoA an eu r ysm s is ef-
can be t reated safely an d ad equ ately via en d ovascu lar occlu - fective.3,9,11,12,24,38,39 Th e con troversy arises w hen aneur ysm m or-
sion . Th is is of u t m ost im p or tan ce becau se ACoA an eu r ysm s phology n ecessitates en dovascu lar procedures requ iring an t i-
reach 55% of th eir r upt u re in ciden ce rate at 3 m m . coagu lat ion or an t iplatelet agen t s. In th is scen ario, th e au th ors
believe th at surgical clip ligat ion is th e preferred m eth od. Al-
th ough th e effect of th ese m edicat ion s h as n ot been th orough ly
st u died in th is su bset of p at ien t s, Rin kel et al56 st u died 15 pa-
■ Endovascular Treatment of t ien ts presen t ing w ith SAH on an t icoagu lan t th erapy an d 126
Unruptured Aneurysms pat ien ts w ith SAH an d n o an t icoagu lat ion . Th ey fou n d dep en -
den cy or death occu rred after SAH in 14 of 15 pat ien t s on an t i-
Both m icrosu rgical an d en dovascu lar tech n iqu es h ave been vali- coagu lan t t reat m en t com p ared w ith 62 of 126 n ot being t reated
dated for th e t reat m en t of m any in t racran ial an eu r ysm s. Mu l- w ith an t icoagulan t s, con cluding th at t reat m en t w ith an t icoagu-
t iple pat ien t-specific factors, th e su rgeon’s com fort in m an aging lan t drugs doubles th e already h igh risk of poor ou tcom e in pa-
part icu lar cases, an d an eu r ysm m orph ology h elp determ in e th e t ien ts w ith SAH.
best t reat m en t opt ion . Treat m en t of u n r u pt u red in t racran ial W h en an eu r ysm ru pt u re is associated w ith in t racran ial h e-
an eu r ysm s in you ng, m ed ically low -r isk p at ien t s m ay be best m atom a, pat ien t s ten d to h ave w orse ou tcom es.57 Not on ly is th e
p er for m ed by su rgical clip ligat ion du e to low er en d ovascu lar pat ien t’s clin ical con d it ion affected by th e u n derlying brain in -
com p lete an eu r ysm occlu sion rates an d recan alizat ion rates jur y from th e h em orrh age, but it is also affected by th e m ass ef-
st ill ran gin g u p to 20.9%, d esp ite tech n ical an d d evice im - fect an d resultan t in creased in t racran ial pressu re (ICP). Alth ough
p rovem en t s.14 su rger y both alleviates th e h igh ICP an d secu res th e an eu r ysm to
In 2010, Pierot et al55 pu blish ed th e An alysis of Treat m en t p reven t rebleed ing, it can often be tech n ically ch allenging d u e
by En dovascular Approach of Non r upt ured An eur ysm (ATENA) to diffuse edem a. In 2010, Taw k et al57 p u blish ed a series of 30
st u dy, w h ich w as a p rosp ect ive, m u lticen ter st udy evalu at ing th e pat ien ts w ith an eu r ysm al SAH w h o u n der w en t coil em boliza-
im m ed iate p ostop erat ive an atom ic resu lt s in a large ser ies of t ion of ru pt u red in t racran ial an eu r ysm follow ed by im m ediate
u n r u pt u red in t racran ial an eu r ysm s t reated by en dovascu lar open decom pression an d evacuat ion of clot . Of th e 30 pat ien ts,
tech n iques. Of 694 un r upt ured an eur ysm s evaluated, 200 w ere seven h ad an ACoA an eu r ysm . Th e au th ors rep or ted th at 60.7%of
located in th e ACA or ACoA. Of th e 200 ACA/ACoA an eu r ysm s th e pat ien t s h ad favorable ou tcom es (GOS score of 4 or 5). Th ey
t reated, an atom ic resu lts in d icated total occlu sion in 110 (55%), con clu ded th at in selected pat ien t s w ith an eu r ysm al SAH an d
n eck rem n an t in 53 (26.5%), an d an eu r ysm rem n an t in 37 associated in t racran ial h em orrh age, com bin ed en dovascular an d
(18.5%). Alth ough postoperat ive an atom ic result s w ere in flu- open surgical tech n iques can be used to both secure th e an eu-
en ced by an eu r ysm size an d n eck size, th ere w ere n o sign ifican t r ysm an d con t rol h igh ICP w ith reason able outcom es.
differen ces bet w een an eur ysm locat ion s. W h en in clu ding an eu -
rysm s from all locations, postoperative occlusion rates were 85.4%,
in clu ding both com p lete occlusion an d n eck rem n an t . Th is resu lt
w as sim ilar to p reviou sly p u blish ed sat isfactor y occlu sion rates
for un r u pt u red in t racran ial an eu r ysm s.
■ Long -Term Angiographic Results
Alth ough un r upt ured an eur ysm s in young, relat ively h ealthy At ou r in st it u t ion , in it ial angiograp h ic follow -u p is t yp ically
pat ien ts are often t reated by su rgical clip ligat ion , m any cen ters obtain ed at 6 m on th s after em bolizat ion if com plete or n ear-
treat all in tracran ial aneur ysm s, w ith favorable m orphology w ith com p lete em bolizat ion w as accom p lish ed. Pat ien t s w ith par t ial
en dovascu lar tech n iqu es. On ly w h en an eu r ysm s are n ot am en a- an eur ysm occlusion t ypically h ave repeat follow -up angiogram at
ble to en dovascular t reat m en t are th ey t reated via surgical clip 3 m on th s after t reat m en t . Also, pat ien t s at risk for coil com pac-
obliterat ion . Agh akh an i and colleagues 7 t reated 440 u n ru pt u red tion , such as th ose w ith partially throm bosed or giant aneur ysm s,
an eu r ysm s, all of w h ich w ere being con sid ered for t h eir first u n dergo 3-m on th follow -u p angiogram s. If on a follow -up angio-
en dovascu lar t reat m en t . Of t h e 440 u n rupt u red an eu r ysm s eval- gram th ere is com p lete occlu sion , th en th e pat ien t is follow ed
uated, 202 an eu r ysm s w ere selected for en dovascu lar t reat m en t w it h m agn et ic reson an ce angiograp hy ever y 6 m on t h s. If in -
an d 238 an eu r ysm s w ere t reated via op en su rger y. For t y-fou r com p lete occlu sion occu rs, t h en rep eat an giogram is d on e at 3
(18.5%) of t h e u n r u pt u red an eu r ysm s w ere ACoA an eu r ysm s. to 6 m on th s an d a fin al angiogram at 5 years, at th e discret ion of
Using th is st rategy th e au th ors sh ow ed sim ilar angiograph ic an d th e su rgeon .

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51 Endovascular Therapies for Anterior Communicating Artery Aneurysms 603

As already d iscu ssed, th e com p lete occlu sion rate is variable m ain ly in large, w ide-n ecked an eu r ysm s. Sim ilarly, Gon zalez et
depen ding on th e m orph ology of th e an eu r ysm .3,21 Sp ecific to al24 obt ain ed angiograp h ic follow u p in 79 of 181 ACoA an eu -
ACoA an eur ysm s, Kazekaw a an d colleagues 12 evalu ated 19 con - r ysm s, ranging from 1 to 60 m on th s, an d foun d th at 12 h ad re-
secu t ive ACoA an eu r ysm s t reated via GDC coils an d rep or ted can alized (15.2%).
com p lete obliterat ion in 68% of cases, an d a n eck rem n an t in
32% of cases. Gon zalez et al24 rep or ted com p lete em bolizat ion
in 96 of 181 cases (53%), a n eck rem n an t in 71 cases (39.2%),
an d in com plete em bolizat ion in eigh t cases (4.4%). Sim ilarly,
■ Conclusion
Guglielm i et al11 ach ieved com p lete occlu sion in 139 (45.5%) Alth ough n o single t reat m en t m odalit y can be successfu l for all
cases, n eck rem n an t in 145 (47.5%) cases, an d residu al filling of an eur ysm s in a single locat ion , it is clear th at en dovascu lar th er-
th e an eu r ysm in 7% of cases. apy for both r upt ured an d un r upt ured ACoA an eur ysm s is be-
Recu rren ce rates h ave been d ocu m en ted from 0% to 20.9%.9,14 com ing m ore read ily ap plied in th e properly selected p at ien t . A
Sp ecific to ACoA an eu r ysm s Birkn es et al9 fou n d th e recan aliza- detailed u n derst an ding of th e m orp h ology an d an atom y of th e
t ion rates ranged from 0% for an terior project ing an eur ysm w ith an eur ysm is n ecessar y to h elp p redict th e success of en dovascu-
sm all n eck (< 4 m m ), to 100% for in ferior p roject ing w ith large lar t reat m en t .
n eck (≥ 4 m m ), w ith m ean follow -up of 8.6 m on th s. Moret an d Even w ith th e tech n ological advan cem en t in en dovascu lar
associates 3 follow ed 24 ACoA an eu r ysm s t reated w ith GDC de- devices an d tech n iqu es, su ch as com plian t m icroballoon s, em -
tach able coils, ranging from 3 to 28 m on th s, an d repor ted th at 21 bolic agen ts, flow diver ters, an d n eurodedicated self-expan ding
(87.5%) sh ow ed com p lete occlu sion on follow -u p angiograp hy. In sten t s, th ere are lim it at ion s in th e en dovascu lar t reat m en t of
2009, Guglielm i et al11 repor ted th eir experien ce of en dovascular ACoA an eur ysm s. Experien ced en dovascu lar as w ell as open n eu -
t reat m en t of 306 con secu t ive ACoA an eu r ysm s. Th ey obser ved rosurgeon s n eed to part icipate in th e decision -m aking process to
a 16% recan alizat ion of th e an eu r ysm s on follow -up angiogram , determ in e th e opt im al t reat m en t of ACoA an eu r ysm s.

References
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r ysm s: m orph ological con siderat ion s. Neurosurger y 2006;59:43–52, dis- r u pt ured In t racran ial An eur ysm s Invest igators. Un rupt ured in t racran ial
cu ssion 43–52 an eur ysm s: n at ural h istor y, clin ical outcom e, an d risks of surgical an d
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cu lar t reat m en t of 306 an terior com m u n icat ing ar ter y an eu r ysm s: over- 23. Spet zler RF, McDougall CG, Albuquerque FC, et al. The Barrow Rupt ured
all, perioperat ive result s. J Neurosurg 2009;110:874–879 An eur ysm Trial: 3-year result s. J Neurosu rg 2013;119:146–157
12. Kazekaw a K, Tsut sum i M, Aikaw a H, et al. En dovascu lar t reat m ent of an - 24. Gon zalez N, Sed rak M, Mar t in N, Viñ u ela F. Im p act of an atom ic feat u res
terior cerebral arter y an eur ysm s using Guglielm i det ach able coils: m id- in th e en d ovascu lar em bolizat ion of 181 an terior com m u n icat ing ar ter y
term clin ical evalu at ion . Radiat Med 2002;20:291–297 an eur ysm s. St roke 2008;39:2776–2782

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25. Kassell NF, Torn er JC. Th e In tern at ion al Cooperat ive St udy on Tim ing of 42. Kelly ME, Gon ugun t a V, Woo HH, Turn er R IV, Fiorella D. Dou ble-balloon
An eur ysm Surger y—an up date. St roke 1984;15:566–570 t rapping tech n ique for em bolizat ion of a large w ide-n ecked su perior cer-
26. Juvela S, Porras M, Poussa K. Nat ural h istor y of un rupt ured in t racran ial ebellar ar ter y an eu r ysm : case report . Neurosurger y 2008;63(4, Su ppl 2):
an eu r ysm s: p robabilit y of an d risk factors for an eu r ysm ru pt u re. J Neu ro- 291–292, discussion 292
surg 2000;93:379–387 43. Baxter BW, Rosso D, Low n ie SP. Double m icrocath eter tech nique for de-
27. Mira JM, Cost a FA, Hor t a BL, Fabião OM. Risk of rupt ure in un r upt ured t ach able coil t reat m en t of large, w ide-n ecked in t racran ial an eu r ysm s.
an ter ior com m u n icat ing ar ter y an eu r ysm s: m et a-an alysis of n at u ral AJNR Am J Neuroradiol 1998;19:1176–1178
h istor y st u dies. Su rg Neu rol 2006;66(Su p pl 3):S12–S19, d iscu ssion S19 44. Waldau B, Reavey- Can t w ell JF, Law son MF, et al. In ten t ion al par t ial coiling
28. Okuyam a T, Sasam ori Y, Takah ash i H, Fukuyam a K, Saito K. [St u dy of m ul- dom e protect ion of com plex r u pt u red cerebral an eu r ysm s p reven t s acu te
t iple cerebral an eur ysm s com prised of both rupt ured an d un rupt ured rebleeding and produces favorable clin ical ou tcom es. Act a Neurochir
an eu r ysm -an an alysis of in ciden ce rate w ith respect to site an d size] No (Wien ) 2012;154:27–31
Sh in kei Geka 2004;32:121–125 45. Hen kes H, Fisch er S, Weber W, et al. En dovascu lar coil occlusion of 1811
29. Perlm ut ter D, Rh oton AL Jr. Microsurgical an atom y of an terior cerebral in t racran ial an eur ysm s: early angiograph ic an d clin ical resu lt s. Neuro-
an terior com m u n icat ing recu rren t arter y com plex. Su rg Foru m 1976;27: surger y 2004;54:268–280, discussion 280–285
464–465 46. Low n ie SP, Drake CG, Peerless SJ, Fergu son GG, Pelz DM. Clin ical p resen -
30. Wilson G, Riggs HE, Rupp C. Th e path ologic an atom y of r upt u red cerebral t at ion an d m an agem en t of gian t an terior com m u n icat ing ar ter y region
an eu r ysm s. J Neu rosu rg 1954;11:128–134 an eur ysm s. J Neurosurg 2000;92:267–277
31. Rosn er SS, Rh oton AL Jr, On o M, Barr y M. Microsurgical an atom y of th e 47. Halbach VV, Higash ida RT, Dow d CF, et al. Th e efficacy of en dosaccular
an terior p erforat ing ar teries. J Neu rosu rg 1984;61:468–485 an eur ysm occlu sion in alleviat ing n eurological deficit s produced by m ass
32. Yock DH Jr, Larson DA. Com puted tom ography of h em orrh age from an te- effect . J Neurosurg 1994;80:659–666
rior com m un icat ing ar ter y an eur ysm s, w ith angiograph ic correlat ion . 48. Gr u ber A, Killer M, Bavin zski G, Rich ling B. Clin ical an d angiograp h ic
Radiology 1980;134:399–407 resu lt s of en d osaccu lar coiling t reat m en t of gian t an d ver y large in t racra-
33. Joyn t RJ, Afifi A, Harrison J. Hypon at rem ia in subarach n oid h em orrhage. n ial aneu r ysm s: a 7-year, single-cen ter experien ce. Neurosurger y 1999;
Arch Neurol 1965;13:633–638 45:793–803, discussion 803–804
34. Iw an aga H, Wakai S, Och iai C, Narit a J, Inoh S, Nagai M. Rupt ured cerebral 49. Jah rom i BS, Mocco J, Bang JA, et al. Clin ical an d angiograph ic outcom e
an eu r ysm s m issed by in it ial angiograp h ic st u dy. Neu rosu rger y 1990; after en dovascular m an agem en t of gian t in t racranial an eur ysm s. Neuro-
27:45–51 surger y 2008;63:662–674, discussion 674–675
35. van Rooij W J, Peluso JP, Sluzew ski M, Beute GN. Addit ion al value of 3D 50. Pierot L. Flow diver ter stent s in th e t reat m en t of int racranial an eur ysm s:
rot at ion al angiograp hy in angiograp h ically n egat ive an eu r ysm al su b - W h ere are w e? J Neuroradiol 2011;38:40–46
arach n oid h em or rh age: How n egat ive is n egat ive? . AJNR Am J Neu rora- 51. Ringer AJ, Rodriguez-Mercado R, Vezn edaroglu E, et al. Defining the risk of
diol 2008;29:962–966 ret reat m ent for an eur ysm recurren ce or residual after in it ial t reat m en t
36. Bion di A, Jan ardh an V, Kat z JM, Salvaggio K, Riina HA, Gobin YP. Neuro- by en dovascular coiling: a m u lt icen ter st udy. Neurosurger y 2009;65:311–
form stent-assisted coil em bolization of w ide-neck intracranial aneurysm s: 315, discu ssion 315
st rategies in sten t d eploym en t an d m idterm follow -u p . Neu rosu rger y 52. Suzuki S, Kurat a A, Oh m om o T, et al. En dovascu lar surger y for ver y sm all
2007;61:460–468, discussion 468–469 rupt ured in t racran ial an eur ysm s. Techn ical n ote. J Neurosu rg 2006;105:
37. Lubicz B, Leclerc X, Levivier M, et al. Ret ract able self-expan dable sten t for 777–780
en dovascular t reat m en t of w ide-n ecked in t racran ial an eur ysm s: prelim i- 53. Slu zew ski M, Bosch JA, van Rooij W J, Nijssen PC, Wijn alda D. Rupt ure
n ar y experien ce. Neu rosurger y 2006;58:451–457, discu ssion 451–457 of in t racran ial an eu r ysm s d u ring t reat m en t w ith Guglielm i det ach able
38. Huang Q, Xu Y, Hong B, Zh ao R, Zh ao W, Liu J. Sten t-assisted em bolizat ion coils: in ciden ce, outcom e, an d risk factors. J Neurosu rg 2001;94:238–
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con secut ive cases. AJNR Am J Neu roradiol 2009;30:1502–1506 54. Tsu t sum i M, Aikaw a H, On izuka M, et al. En dovascular t reat m en t of t iny
39. Saatci I, Geyik S, Yavuz K, Cekirge S. X-con figured sten t-assisted coiling in r u pt u red an ter ior com m u n icat ing ar ter y an eu r ysm s. Neu roradiology
th e en dovascu lar t reat m en t of com p lex an terior com m u n icat ing ar ter y 2008;50:509–515
an eu r ysm s: a n ovel recon st r u ct ive tech n iqu e. AJNR Am J Neu rorad iol 55. Pierot L, Spelle L, Vit r y F; ATENA invest igators. Im m ediate an atom ic re-
2011;32:E113–E117 sult s after th e en dovascular t reat m en t of un r upt ured in t racran ial aneu-
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n ique” in th e t reat m en t of w ide n eck in t racran ial an eur ysm s. Angio- 140–144
grap h ic resu lt s an d clin ical follow -u p in 56 cases. In ter v Neu roradiol 56. Rin kel GJ, Prin s NE, Algra A. Outcom e of an eu r ysm al subarachn oid h em -
1997;3:21–35 orrhage in patients on anticoagulant treatm ent. Stroke 1997;28:6–9
41. Pierot L, Spelle L, Leclerc X, Cogn ard C, Bon afé A, Moret J. En dovascular 57. Taw k RG, Pan dey A, Levy E, et al. Coiling of r upt ured an eur ysm s follow ed
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of rem odeling tech n iqu e an d st an dard t reat m en t w ith coils. Radiology
2009;251:846–855

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52 Surgical Therapies for Distal Anterior
Cerebral Artery Aneurysms
Clem ens M. Schirm er and Carlos A. David

In t racran ial an eu r ysm s of t h e d ist al an ter ior cerebral ar ter ies gen u of th e corpu s callosum . Fu r th er com plicat ing th e m at ter,
(d ACAs) ar ise from t h e an ter ior cerebral ar ter y (ACA) an d it s th e an eu r ysm m ay be located at th e bifu rcat ion of an u np aired
bran ch es d ist al to t h e an terior com m u n icat in g ar ter y (ACoA). azygos A2. Clip p ing of a w ide- an d sclerot ic-n ecked an eu r ysm
First described by Sugar an d Tin sley 1 in 1948, th ey are relat ively m ay cause sten osis of th e pericallosal arter y. Mu lt iple an eur ysm s
rare, com p rising 5% of all in t racran ial an eu r ysm s, w ith a sligh t m ay requ ire addit ion al pterion al cran iotom y.
fem ale prepon deran ce. Most cit at ion s suggest an in ciden ce rang- Com pared w ith oth er an terior circu lat ion an eu r ysm s, dACA
ing from 2 to 9%2–9 an d th ey are frequ en tly associated w ith an eu - an eur ysm s are kn ow n to be associated w ith a relat ively h igh er
r ysm s in oth er locat ion s.3,5,9,10 Th ey m ost often arise from th e operat ive m orbidit y rate.2,12 Sign ifican t redu ct ion s in m or t alit y
branching point bet w een the callosom arginal artery and the m ain h ave been repor ted over t im e, st ar t ing w ith 32% in an early co-
ACA t ru n k. operat ive st u dy,13 10% in a sem in al series from Drake’s group,14
Due to th eir posit ion in th e in terh em isph eric fissure an d fre- an d 0.9% in a series from 2008.11 Moreover, becau se of th eir rare
qu en t adh eren ce to th e su rroun ding brain , p at ien t s w ith dACA occurren ce an d th e in creasing use of n on surgical en dovascular
an eu r ysm s often p re sen t w it h in t rap aren chym al h em atom as. opt ion s, n eu rosurgeon s h ave less experien ce w ith surgical t reat-
Th e relat ively n arrow corridor for access, obscu red an atom y, an d m en t of dACA an eu r ysm s.
sign ifican t sw elling in th e r u pt ured sit u at ion presen t sign ifican t Many of th e above issu es are exclu sively su rgical con sid er-
tech n ical t reat m en t ch allenges. Table 52.1 lists com m on pitfalls at ion s, an d t h e en d ovascu lar t reat m en t of p er icallosal ar ter y
an d m an agem en t suggest ion s.11 an eur ysm s is associated w ith un ique ch allenges.15 (Th e en dovas-
Many dACA an eu r ysm s ru pt u re w h en th ey are st ill ver y cular treatm ent of these aneurysm s are addressed in Chapter 53.)
sm all.5 Despite being often relat ively sm all, th ese an eu r ysm s can
produce sign ifican t m orbidit y. Th e in terh em isph eric fissu re an d
callosal cistern com prise a n arrow space su rrou n ded by th e cor-
pu s callosu m an d bilateral cingu late gyri w ith in ter ven ing falx ■ Relevant Anatomy
cerebri. Th e dom e of th e an eur ysm m ay be den sely fixed on th e
Arterial Anatomy
cingulate gyrus. Th e cingu late gyri can be den sely apposed w ith
in terdigit at ing convolu t ion s separated on ly by a ver y th in layer Th e ACA arises from th e bifu rcat ion of th e in tern al carot id ar ter y
of arachn oid. Th e approach can be lim ited by th e superior cere- (ICA) an d courses rost rom edially dorsal to th e opt ic n er ve as th e
bral vein s th at d rain in to th e su perior sagit tal sin us (SSS). An as- A1 segm en t . Th e ipsilateral an d con t ralateral A1 segm en ts run
sociated fron tal in t racerebral or in t raven t ricu lar h em atom a m ay togeth er an d con n ect via th e ACoA. Th e dACA com prises by defi-
h in der opt im al brain relaxat ion , an d in terh em isph eric blood can n it ion th e segm en t s of th e ACA distal to th e ACoA an d con t in ues
obscu re th e n or m al n eu roan atom y. Th e su rgeon m ay fin d it sup eriorly in to th e in terh em isph eric fissure, upw ard on th e m e-
ch allenging to obt ain p roxim al con t rol, as th e dist al p ericallosal dial su rface of th e h em isp h ere, an d th en con t in u es p osteriorly
ar ter y is usually en coun tered before iden t ificat ion of th e an eu - on th e superior su rface of th e corpus callosum , st aying m ostly
r ysm an d p roxim al A2 ACA segm en t , w h ich is h id d en by t h e below th e low er m argin of th e falx (Fig. 52.1).

Table 52.1 Common Pitfalls and Management Strategies

Pitfall Management Pearl

Positioning difficult y Use familiar orientation (nose is up); consider neuronavigation


Small craniotomy Use neuronavigation; allow for room to deal with bridging veins and for third/
fourth hand in case of rupture
Damage to bridging veins Make craniotomy large enough to allow for alternate approach route
Excessive retraction Consider lateral head position to utilize gravit y
Damage to cingulum akinetic mutism, m emory problems Minimize retraction
Intraoperative rupture Have clips ready before craniotomy
Stenosis of parent vessel Be cognizant of this potential pitfall; use micro-Doppler, indocyanine green
(ICG), or intraoperative angiogram to assess distal flow
Vasospasm Aggressive postoperative management; intraoperative use of calcium channel
blockers

605

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606 V Cerebral and Spinal Aneurysms

Th e dACA h as th e follow ing segm en t s, based on th e p referred par t of th e st riat u m . Th e n u m ber of p erforators is h igh ly vari-
nom en clature by Perlm ut ter and Rhoton,16,17 (Fig. 52.1): A2 below able. Perlm u t ter an d Rh oton 16 describe an average of five arising
th e gen u of th e corp u s callosu m , A3 arou n d th e gen u , an d A4 an d from th e A2 segm en t an d t h ree from each of th e A3 to A5 seg-
A5 as th e term in al por t ion s. Bran ch es of th e dACA can be divided m ents. The eight cortical branches of the dACA include the orbital
in to cen t ral an d cort ical grou ps. Cen t ral perforators arise m ostly bran ch es (orbitofron tal [OF] ar ter y); th e fron topolar ar ter y; an -
from th e A2 an d A3 segm en t s, w h ich en ter th e lam in a term in alis terior, m iddle, an d posterior in tern al fron tal ar teries; th e para-
an d an terior forebrain below th e corpus callosum to supply th e cen t ral ar ter y; an d t h e su p er ior an d in fer ior p ar iet al ar ter ies.
an terior hypoth alam us, sept um pellucidum , m edial por t ion of Th e callosom argin al ar ter y (CMA) as th e m ajor bran ch of th e A3
th e an terior com m issu re, p illars of th e forn ix, an d an teroin ferior segm en t h as th e m iddle an d posterior in tern al fron t al an d para-

Fig. 52.1 Schem atic representation of the relevant anatomy of the distal anterior cerebral artery and its surrounding structures. The m ost com m on sites
for traum atic aneurysm s are denoted (*). a., artery

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52 Surgical Therapies for Distal Anterior Cerebral Artery Aneurysm s 607

cen t ral ar teries as t ributaries, an d th e pericallosal ar ter y (A4 an d Th e oth er A2 segm en t is hyp op last ic an d gives rise to on ly som e
A5) give rise to th e lat ter t w o ar teries. proxim al bran ch es. An accessor y (t ype III) variat ion feat u res a
Th e term pericallosal artery h as been variably defin ed. Som e sm all m ed ian t h ird A2 segm en t t h at su p p lies som e p or t ion of
auth ors defin e th e A3–A5 segm en ts distal to th e bifu rcat ion of eit h er or bot h h em isp h eres. Regard less of t h e p roxim al bifu r-
th e CMA as t h e d ACA. Becau se t h e CMA is n ot alw ays p resen t , cat ion p at ter n , d ist al crossover vessels are relat ively com m on
Perlm u t ter an d Rh oton 16,17 recom m en d t h at t h e d ACA refer to (64%). Alth ough t ype I variat ion s are rare, th ey are associated
th e segm en t of th e ACA distal to th e ACoA. w ith dACA an eur ysm s in 7 to 10% of cases.4,5,9 An eur ysm s m ay
Th e recu rren t ar ter y of Heu bn er m ay arise from eith er th e A1 occur anyw h ere along th e course of th e dACA but are m ost com -
segm en t or th e p roxim al A2 segm en t . It su pp lies th e an terior m on at its m ajor bran ch ing poin ts, at th e gen u of th e corpu s cal-
m edial p ar t of th e h ead of th e cau date n ucleu s, adjacen t part s of losu m , an d at th e origin of th e CMA. Traum at ic an eu r ysm s are
th e in tern al capsu le an d pu t am en , an d p ar t s of th e sept al n u clei. m ost com m on ly associated w ith th e areas of the dACA bran ch es
Th e orbit al bran ch es su p ply th e orbit an d m edial su rfaces of th e th at overlap th e free edge of th e falx cerebri rath er th an bran ch -
fron t al lobe after arising from th e ascen ding p ar t of th e dACA ing poin t s. An eu r ysm s along th e ascen ding port ion of th e CMA
ven t ral to th e gen u of th e corpus callosu m . are frequ en t .
Th e CMA is a m ajor bran ch of th e dACA. It arises dist al to th e
fron top olar ar ter y an d t h e an terior in tern al fron t al ar ter y an d
cou rses after a sh or t ascen ding por t ion dorsally in th e calloso-
Venous Anatomy
m argin al sulcus. Bran ch es of th is arter y su pply th e paracen t ral Th e su perficial cerebral vein s arise from th e cor tex an d su bcor t i-
lobu le an d par ts of th e cingu late gyru s. Th e CMA varies inversely cal w h ite m at ter an d form larger vein s, w h ich em pt y in to t h e
in size w ith th at of th e distal p ericallosal ar ter y system an d m ay du ral sin u ses. Th ese larger vein s in clu d e th e su p erior (in clu ding
be a dist in ct vessel or con sist of a group of several ascen ding ves- vein of Trolard) an d in ferior cerebral (Labbé) vein s an d th e su-
sels th at arise from th e pericallosal ar ter y.11 perficial m id dle cerebral (sylvian ) vein . A variable n u m ber, u su -
Th e pericallosal ar ter y, regarded as th e term in al bran ch of th e ally 10 to 15, of superior cerebral vein s drain blood from th e cor-
dACA, cou rses t igh tly along th e corp u s callosu m , cau dally along tex an d m edial surfaces of th e h em isph ere an d drain in to th e
th e dorsal su rface of th e p ariet al lobe, in clu ding th e p recu n eu s. SSS. Th ese vein s en ter th e sin u s by cou rsing obliqu ely for w ard
Collaterals can be fou n d h ere bet w een th e dorsal callosal ar teries after freely bridging a 1- to 2-cm gap bet w een th e m ost dist al
arising from th e posterior cerebral ar teries th at supply th e sple- at tach m en t to th e pia-arach n oid an d th e en t r y in to th e sin u s
n ium of th e corpus callosum an d th e term in al bran ch es of th e across th e subdural space. Som e vein s join a m en ingeal sin u s in
pericallosal ar ter y. th e du ra m ater on th e w ay to th e SSS.20 Som e vein s on th e m edial
An om alies an d variat ion s of th e dACA are com m on (Fig. 52.2), su rface of th e h em isp h eres drain in to th e in ferior sagit tal sin u s.
accoun t ing for 25% of specim en s in a st u dy by Bapt ist a.18 Th e Vein s on th e m edial su rface of th e h em isph ere are divided by th e
usu al pat tern h as both A2 segm en t s arising from th e respect ive cingulate sulcus in to an ascen ding an d a descen ding group, th e
ipsilateral A1 segm en ts. A t ype I (azygos) variat ion 19 in cludes a form er drain ing tow ard th e SSS, th e lat ter com prising t ributaries
single A2 segm ent arising from th e junction of both A1 segm ents, th at d rain in to th e an terior cerebral vein .20 Occlu sion of th e large
w h ich t h en su bsequ en t ly d ivid es to su p p ly bot h h em isp h eres. su p erior cerebral vein s du ring th e in terh em isp h eric ap p roach
In th e t ype II (bih em isph eric) variat ion , on e A2 is dom in an t an d m ay cause ven ou s in farct ion , part icularly w h en th e sylvian vein
su p p lies sign ifican t p or t ion s of th e con t ralateral h em isp h ere. system or an astom osis is un derdeveloped.21

a b c

Fig . 52.2a–c (a) Illustrative case of a 63-year-old m an with extensive Computed tom ography angiography dem onstrated a dACA aneurysm as-
bifrontal flam e-shaped intracerebral hem atom a (ICH) due to a ruptured sociated with a Fisher grade III subarachnoid hem orrhage (SAH). She un-
distal anterior cerebral artery (dACA) aneurysm . (b,c) A 58-year-old wom en derwent clipping via an interhem ispheric approach. Tem porary clipping
presented with Hunt-Hess grade III after a sudden headache and collapse. (b) affords proxim al control prior to the definitive clippinc (c).

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608 V Cerebral and Spinal Aneurysms

cular th erapy an d surgical clipping. At ten t ion m ust be paid w h en


■ Pathophysiology and Natural History determ in ing th e lateralit y of th e an eu r ysm , in p ar t icu lar w h en
of Disease both dACAs are opacified from ipsilateral inject ion s due to a pat-
en t ACoA. Th e u se of com p u ted tom ograp hy angiography (CTA)
In several larger series, th e m ajorit y of pat ien t s presen ted w ith a
and m agnetic resonance angiography (MRA) sensitivit y for the de-
rupt ured an eur ysm , an d on ly 20%of an eur ysm s w ere foun d in ci-
tection of sm all aneurysm s is protocol- and m achine-dependent
den tally.2–6,9,22 Leh ecka et al23 repor ted a m ean diam eter of 7.4
an d sh ou ld n ot replace regu lar angiography. Rem em ber th at th e
m m an d 4.2 m m for a series of 67 rupt ured an d 41 u n rupt ured
field of view (FOV) of m ost CTA circle of Willis protocols is fo-
an eu r ysm s, resp ect ively. A broad base, w id er t h an t h e p aren t
cused aroun d a t issue slab from th e m id-pet rou s ICA to th e fron -
ar ter y, w as seen in 68% of pat ien ts, an d 94% of pat ien ts h ad a
tal ven t ricular h orn s, w h ich m ay n ot cover a dACA an eu r ysm . If
bran ch origin at th e base. Th e neck-to-dom e rat io w as 1:1 in 25%
a dACA an eur ysm locat ion is suspected or if a regular circle of
of pat ien ts. An om alies of th e ACA w ere seen in 23 pat ien t s (23%).
Willis CTA is n egat ive, con sider request ing a larger FOV CTA. Lau
Half of th e p at ien t s h ad m ore th an on e an eu r ysm , m ost often
et al33 poin ted ou t t h at if im aging is delayed by at least a w eek,
(38%) located in th e m iddle cerebral ar ter y dist ribu t ion .23 A sec-
callosal h em orrh ages m ay m im ic gliom as, an d calcified, in ciden -
on d dACA an eu r ysm w as presen t in 20% of cases.2–6,9,22
tal, supracallosal dACA an eur ysm s m ay be con fused w ith m en in -
In th e case of t raum at ic an eu r ysm s, pat ien ts usually presen t
giom as in th e sam e area.9
w ith subarach n oid h em orrh age (SAH) in th e days to w eeks fol-
Th e an atom y of th e cor t ical vein s drain ing in to th e SSS can be
low ing a usually sign ifican t h ead inju r y. In th ese cases, th e an eu -
assessed by st udying th e topm ost apical slices of a preoperat ive
r ysm s pu t at ively arise at th e locat ion w h ere th e dACA is in close
MRI or CTA.
apposit ion to th e free edge of th e falx. Th e proposed m ech an ism
post u lates th at su dden decelerat ion du ring th e t rau m a leads to
an inju r y of t h e ar ter ial w all. Trau m at ic an eu r ysm s are m ore
com m on in p ed iat r ic p at ien t s.24–26 Th ey h ave been rep or ted in
cases w ith ou t seem ingly severe en ough t raum a.27,28 ■ Discussion of Various
Surgical Approaches
Th e locat ion of t h e an eu r ysm dict ates th e opt im al su rgical ap -
proach . We rou t in ely u se on e of th ree app roach es for an eu r ysm s
■ Clinical Presentation
of th e dACA. An eu r ysm s dist al to th e ACoA an d in fracallosal A2
Pat ien t s w ith ru pt u red dACA an eu r ysm s p resen t w ith sign s an d an eur ysm s can be approach ed via an orbitozygom at ic approach .
sym ptom s th at are t yp ical of SAH. Radiograp h ically, th e h em or- An eur ysm s located m ore th an 1 cm distal to th e ACoA or in fron t
rh ages ap pear m u ch m ore severe th an th ose seen in m ost oth er of th e gen u of th e CC can be accessed via a basal fron t al in ter-
an eur ysm s (Fig. 52.2). Som e pat ien t s exh ibit low er ext rem it y h em isph eric approach . An eur ysm s located above th e CC or m ore
m on oparesis, paraparesis, or h em iparesis in associat ion w ith a dist al are best ap p roach ed via a p arasagit tal in terh em isp h eric
large intra parenchym al hem atom a. Significant intracallosal hem - ap proach (Table 52.2).
orrh age can result in a h em isph eric discon n ect ion syn drom e.29 Th ere are n u m erou s op in ion s abou t t h e p osit ion in g of t h e
Hern esn iem i et al3 an d oth ers 14 h ave n oted a h igh er th an usual p at ien t ’s h ead . Th e su rgeon sh ou ld evalu ate t h e relat ive im p or-
in ciden ce of p oor clin ical grades, w ith 60 to 63% of pat ien t s p re- tan ce of an in t uit ive an d t rusted fram e of referen ce (n ose an d
sen t ing w ith Hu n t-Hess grades of III or h igh er.3,14 In t racerebral an terior is u p) versu s th e ease of m an ipulat ion an d dissect ion in
h em orrh age can be seen com m on ly in cases w ith r upt ured dACA a space w ith a t ran sverse orien tat ion an d th e effect of gravit y.34
an eur ysm . Earlier series repor t an in ciden ce of 50%,4,14 w h ereas Difficu lt ies to con sid er in clu d e t h e sm all an d n ar row cor r id or
Leh ecka et al30–32 repor t an in ciden ce of in t racerebral h em ato- of approach , m an aging th e parasagit t al vein s, th e relat ively sm all
m as (ICHs) bet w een 13% an d 29% depen ding on th e exact loca- interhem ispheric cistern, and the difficult y in achieving adequate
t ion of th e an eu r ysm . Likew ise an in ciden ce bet w een 14% an d brain relaxat ion an d ret ract ion w ith out com prom ising bridging
24% for ICH w ith in t raven t ricu lar h em orrh age (IVH) an d 10 to vein s an d causing ret ract ion injur y.
12% for IVH alon e h ave been rep or ted.

■ Surgical Technique
■ Perioperative Evaluation
Infracallosal Aneurysms
The standard tenets for the evaluation for cerebral aneurysm s are
applicable for dACA an eur ysm s. Com puted tom ography fin dings For dACA an eu r ysm s located less th an 1 cm distal to th e ACoA,
in cases w ith ru pt ured d ACA an eu r ysm s are sim ilar to fin dings a st an dard pterion al cran iotom y is used. Con siderat ion can be
for rupt ured ACoA an eur ysm s. In rupt ured cases, th e h em atom a given to perform ing an orbitozygom at ic approach to gain in -
is often foun d to displace th e corpu s callosu m (CC) dow nw ard creased w orking angle upw ard an d to avoid u n due brain ret rac-
rath er th an u pw ard as often seen in th e case of ACoA an eur ysm s. t ion . We recom m en d p osit ion in g w ith t h e h ead t u r n ed 15 to
Form al angiography rem ain s th e gold stan dard for evalu at ion of 30 degrees using th e m alar em in en ce as th e h igh est poin t . Using
th e an eu r ysm an d th e fin er poin t s of th e n eck geom et r y an d re- sh ar p m icrod issect ion , t h e A1 ACA segm en t is id en t ified an d
lat ion sh ip to th e p aren t vessel. An eu r ysm geom et r y is p ar t icu - follow ed to th e ACoA. Frequen tly a gyrus rect u s resect ion is n ec-
larly im port an t w h en con sid ering th e ch oice bet w een en dovas- essar y to un cover th e A2 segm en t an d th e an eu r ysm .

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52 Surgical Therapies for Distal Anterior Cerebral Artery Aneurysm s 609

Table 52.2 Key Concepts of the Surgical Approaches to Distal Anterior Cerebral Artery Aneurysms

Location

Infracallosal Genu Supracallosal/ Distal

Approach Orbitocranial Basal frontal Interhemispheric, usually from


interhemispheric nondominant (right) side
Craniotomy Pterional Orbitozygomatic Large parasagit tal Parasagit tal craniotomy
craniotomy (one-third depending on location of
of the way or midway in aneurysm (consider
the nasion to bregma neuronavigation)
distance) Generous craniotomy for
unexpected veins
Positioning Turn head 15–30 degrees Turn head 15–30 degrees Inferior to genu: extend Turn neutral, flex 15 degrees
Malar eminence highest Extend further 15–20 15 degrees
point degrees Level of genu: neutral
position
Dissection strategy Follow A1 to ACoA to A2 Preserve veins Dural flap hinged on SSS
Gyrus rectus resection Gentle dissection: avoid Divide arachnoidal adhesions
Identify both A2 and OF artery retraction or only on Careful venous dissection
Dissect aneurysm -proximal and distal control falx Identify both pericallosal arteries
Confirm CC (white and (deep to transverse arachnoidal
transverse fibers) fibers)
Follow pericallosal vessels Follow proxim ally to obtain
or CMA to A3 control (dissect posterior to
Avoid fundus with pericallosal)
contralateral dissection, Consider callosotomy for CSF
over top, or CC drainage
resection Identify aneurysm
Proximal control A2 or A1 exposed in dissection A2, subcallosal A2, anterior (deep) in relation to
the aneurysm, consider genu
resection for proxim al control
Clipping strategy At tempt to clip parallel to parent artery; may need Temporary clipping Parallel to parent artery, small
angled or fenestrated clip Curved or side-angled curved clips
clips
Abbreviations: ACoA, anterior com m unicating artery; SSS, superior sagit tal sinus; OF, orbitofrontal; CC, corpus callosum; CMA, callosom arginal artery; CSF, cerebrospinal
fluid.

Genu Aneurysms SSS. Care is t aken n ot to tear any of th e bridging vein s. A con sid-
erate an d con ser vat ive ch oice h as to be m ade abou t sacrificing
For an eu r ysm s arising ≥ 1 cm dist al to th e ACoA or at th e level of any vein s to en able ad equ ate ret ract ion . Frequ en t ly a t rou ble-
th e gen u , a basal fron t al in terh em isp h eric ap p roach is u sed. For som e vein can be d issected free of t h e arach n oid w it h ou t t h e
th is p rocedu re, th e pat ien t’s h ead is posit ion ed in p in s in a n eu - n eed for sacrifice.
t ral posit ion or a 5-degree rotat ion to th e left (to aid th e righ t- Im age guidan ce can st ream lin e th e approach to an d dissect-
han ded surgeon ). For aneur ysm s in ferior to the genu , a 15-degree ing of th e an eur ysm . Th e closer th e an eu r ysm is to th e ACoA, th e
exten sion can be h elpfu l, w h ereas a n eu t ral posit ion p rovides m ore im perat ive it is to begin proxim al an d in feriorly to obt ain
bet ter access to th e level of th e gen u . A bicoron al in cision is m ost proxim al con t rol. Ret ract ion on th e righ t h em isp h ere exposes
com m on ly u t ilized an d sh ou ld exten d fu r th er tow ard th e zygo- th e falx, w h ich is follow ed to th e crist a galli. Exp osu re of th e su -
m at ic p rocess on t h e r igh t t h an on th e left . Th is in cision also prach iasm at ic cistern reveals th e ACoA com plex an d th e A2 seg-
en ables th e su rgeon to h ar vest a large p ericran ial graft to oblit - m en t s, w h ich are th en follow ed to th e an eur ysm . It is crucial to
erate th e fron tal sin u s, if n ecessar y. A u n ilateral large p arasagit- resist th e tem pt at ion to just dissect directly tow ard th e an eu-
t al cran iotom y (on e-t h ird of th e w ay or m idw ay in th e n asion rysm . The CC, w ith its transverse fibers, can ser ve as a useful land-
to bregm a d ist an ce) th at crosses t h e m id lin e is created . We m ark. Especially in larger an eu r ysm s, th e fun dus itself sh ould be
recom m en d placing th e m edial bu r h oles ju st across th e SSS to avoided du ring dissect ion . Th e tech n ique of dissect ion over th e
en able exp edit iou s con t rol in case of bleeding, an d to aid in re- top of th e an eur ysm can be useful, as can par t ial resect ion of th e
t ract ion th at m ay be lim ited by a bony edge. A sm all fron tal sin u s CC. Tem porar y clipping, com bin ed w ith a cerebral protect an t ad-
can be avoided by p lacing th e cran iotom y above it , bu t sacrific- m in istered by an esth esia m ay sign ifican tly decrease th e t urgor
ing exp osu re is n ot a recom m en ded t rade-off. Th e sin us can eas- of th e an eur ysm an d facilit ate fin al dissect ion . Care h as to be
ily be repaired by st ripp ing th e m u cosa dow n , packing th e sin us taken aroun d ath erosclerot ic n ecks, as clip applicat ion can frac-
w ith fat , an d sw inging a pericran ial flap over it . A dural flap of t ure th e n eck of th e an eur ysm . In gen eral, it is desirable to apply
about th e sam e size as th e bon e flap is raised an d h inged on th e th e clip in lin e w ith th e paren t vessel to avoid cau sing sign ifican t

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610 V Cerebral and Spinal Aneurysms

sten osis. Th is u su ally requ ires carefu l con siderat ion for cu r ved, id en t ified bot h p roxim ally an d d ist ally to obt ain p roxim al con -
fen estrated, or side-angled clips. After clip application, care should t rol. In m ost cases, clip placem en t parallel to th e p aren t vessel
be taken to fin ish a com plete dissect ion an d in spect ion aroun d ach ieves an excellen t an atom ic result , w h ereas perpen dicular
th e an eur ysm to en su re p rop er clip placem en t w ith ou t bran ch placem en t is fraugh t w ith th e risk of com prom ising th e p aren t
com prom ise. vessel th rough kin king.
Fusiform an eu r ysm s can represen t a con siderable ch allenge,
but tech n iques such as an A3–A3 bypass an d an eur ysm t rapping
Distal Aneurysms can be con sidered.35
Dist al an eu r ysm s are easier to ap p roach as t h e d issect ion is
lim ited to th e in terh em isph eric space. Th e h ead is posit ion ed in
15-degree flexion w ith n o or m in im al t u rn ing tow ard th e left .
We prefer a direct in terh em isp h eric ap proach w ith a cran iotom y
th at is t ailored to th e locat ion of t h e an eu r ysm . Navigat ion m ay
■ Patient Outcomes
be h elp fu l in p lan n ing th e cran iotom y. W h en n avigat ion is n ot Th e syn drom e of in farct ion of th e dACA w ith con cu rren t p reser-
available, t h e cran iotom y can be p lan n ed by st u dying a p re- vat ion of th e recurren t ar ter y of Heubn er h as been reported by
operat ive cross-sect ion al st u dy th at displays th e an eur ysm in a Critch ley.36 Th is syn drom e con sist s of con t ralateral m on oparesis
sagit t al p lan e in relat ion to th e coron al su t u re, w h ich can be felt of t h e low er lim b or h em ip aresis, con t ralateral sen sor y loss,
in m ost p at ien t s an d used as a lan dm ark. p sych om otor sym ptom s an d m em or y im pairm en t , in con t in en ce,
Th e exten t of th e cran iotom y is plan n ed u sing in t raop erat ive visu al agn osia, an d apraxia.36 Bilateral sym ptom s are p ossible,
n avigat ion or by u sin g th e coron al su t u re as a referen ce p oin t but due to th e relat ively rich collateral, poten t ial occlusion of a
on th e preoperat ive im ages. A parasagit tal fron tal cran iotom y is m ajor bran ch does n ot alw ays lead to a deficit .3,14
perform ed, en abling an an terior in terh em isp h eric ap p roach . We Th e In tern at ion al Coop erat ive St u dy rep or ted a w orse p rog-
advocate cen tering th e m edial th ird of th e cran iotom y over th e n osis for dACA an eur ysm s th an an eu r ysm s at oth er locat ion s.37
SSS. In m ost cases, w e w ou ld advocate cen tering th e cran iotom y Factors su ch as th e sm all cistern s, p roxim it y of fron t al lobes, fre-
over th e righ t h em isph ere. Regardless of th e sidedn ess, th e goal qu en cy of ICH, an d prep on deran ce of p oor-grade pat ien t s w ere
is to expose th e sin us an d a sm all am ou n t of con t ralateral du ra likely causes of p oor outcom es. More recen t st u dies suggest a
com p letely to allow for th e p ossibilit y of ret ract ion on th e sin u s, m ore favorable outcom e for th ese an eur ysm s. Table 52.3 su m -
an d con t rol of th e sin us in th e even t of sign ifican t bleeding after m arizes th e ch aracterist ics of th e larger series p ublish ed.
th e cran iotom y. Her n esn iem i an d collaborators 3 p u blish ed t h eir exp erien ce
We caution against creat ing a m inim al cran iotom y, w hich m ay in a large ser ies t h at in clu d ed 84 pat ien t s w it h 92 an eu r ysm s;
not allow for adequate retraction an d m anagem ent of un expected 65 pat ien t s h ad a rupt ured dACA aneur ysm , w h ereas in 19 cases
vein s. Perform ing a righ t (n on dom in an t) parasagit tal fron tal cra- th e an eu r ysm w as in ciden t ally iden t ified. Overall, th e au th ors
n iotom y ben efits th e righ t-h an ded surgeon by en abling sligh tly h ad a 9.3% m or t alit y an d 22% m orbidit y rate, w ith an 18.5% in -
m ore ret ract ion an d freed om of in st r u m en t angu lat ion from th e t raoperat ive rupt u re rate.3
righ t side. Th e sen ior editor of th is book an d oth ers h ave th ere- Th e resu lt s of su rgical t reat m en t of a series of 43 p at ien t s
fore advocated a h orizon t al posit ion of th e h ead, w h ich m ay be w ith 50 an eur ysm s of th e dACA before th e adven t of en dovascu -
su p erior as it en ables both h an ds to be u sed side by side rath er lar th erapy w ere described by Prou st et al.6 Th e in terh em isph eric
th an over th e top .34 Alth ough w e p refer th is ap proach an d be- approach w as used in 83%of cases. In 35 rupt ured cases, 63%h ad
lieve th at it h as sign ifican t m erit for th e surgeon w h o is com fort- a good recover y (Glasgow Outcom e Scale [GOS] score of 1). Un -
able w ith it , th e ch oice m ust be coun terbalan ced by th e u n fam il- sat isfactor y ou tcom es w ere m ain ly related to th e in it ial h em or-
iarit y of th is approach in ever yday pract ice. Locat ion , direct ion rh age, in adver ten t occlusion of th e paren t ar ter y, prolonged
of th e an eur ysm dom e project ion , an d size of th e an eur ysm also tem porar y occlu sion t im es, an d rebleeding due to in com plete
determ in e th e side of th e cran iotom y. An eu r ysm s th at arise in an clipping (2.8%).
area th at overlies th e falx can n ot be approach ed from th e con t ra- De Sou sa an d cow orkers 2 repor ted on a large series of 72 pa-
lateral side w ith ou t open ing th e falx, w h ich m ay n ot be desirable t ien ts w ith 65 r u pt u red an d seven u n r u pt u red dACA an eu r ysm s.
or sim p ly avoidable by com ing from th e ipsilateral side. Th ir t y-t w o pat ien t s h ad m u lt iple an eu r ysm s at oth er sites. Th eir
Th e du ral flap is h inged on th e SSS. We fin d it h elp fu l to re- m orbidit y an d m or t alit y rates w ere 8.3% an d 6.9%, resp ect ively.
t ract on th e m iddle of th e du ral flap u sing a st itch to em p loy All death s occu rred in p at ien t s w ith m u lt ip le an eu r ysm s, an d
som e am ou n t of t ract ion on th e SSS an d gain ext ra exposu re. We m ost poor results occurred in pat ien ts w ith a poor clin ical grade
prefer to preser ve larger vein s w h erever possible. In som e cases, u pon presen tat ion .
den se arach n oid adh esion s h ave to be divided to allow place- Nguyen et al15 reported a series of 25 en dovascularly m an -
m en t of a ret ractor. In som e cases th e falx is discon t igu ous, an d aged dACA an eu r ysm s, an d con clu ded th at th e p erip rocedu ral
ad h esion s to t h e con t ralateral h em isp h ere h ave to be divid ed . com p licat ion s w ere h igh er com p ared w it h ot h er an eu r ysm lo -
In m ost cases th e ver t ical depth of th e falx does n ot reach th e cat ion s, bu t th e long-term du rabilit y did n ot sign ifican tly differ.
cingulate gyri, w h ich are alm ost un iform ly den sely adh eren t . Pandey and coworkers 38 reported on 41 patients undergoing treat-
Th e last layer of t ran sverse arach n oid fibers obscu res th e p arallel m en t; in th e coiling grou p th at in clu ded 28 p at ien t s (22 fem ale),
run n ing pericallosal ar teries. If on ly on e ar ter y can be iden t ified, 90% h ad su ccessful em bolizat ion , 64% ach ieved fun ct ion al in de-
th e iden t it y of a p ericallosal ar ter y sh ou ld be qu est ion ed an d pen den ce (m odified GOS [m GOS] I–II), w ith an 18% recu rren ce
w id er exp osu re sh ou ld be sough t . Th e p aren t vessel m u st be rate at 16.5 m on th s, 0%recurren t SAH, an d on e p at ien t un dergo-

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52 Surgical Therapies for Distal Anterior Cerebral Artery Aneurysm s 611

Table 52.3 Clinical and Outcome Characteristics Reported in the Literature for Patients w ith dACA Aneurysms

% % % Age % %
First Author Year N Ruptured Cases Female (Median) Mortality Morbidity

Otani40 2009 20 100 N/A 55 64 10 0


Lehecka 39 2008 501 55 12 60 50 1 12
Lee 11 2008 126 70 3.5 73 54 0.9 5.1
Pandey38 2007 41 82 1.5 29 53 2.4 7.3
de Sousa 2 1999 72 90 5.3 51 44 6.9 8.3
Inci4 1998 14 86 2.8 8 44 7.1 0
Proust 6 1997 43 81 5.7 27 49 14 16.3
Hernesniemi3 1992 84 77 7.3 41 49 7.5 17.9
Ohno 5 1990 42 71 9.2 24 54 5.9 5.9
Sindou 22 1988 19 95 N/A 12 49 0 6.3
Yaşargil7 1984 100 2.3 15 42 0 13
Wisoff9 1987 20 60 N/A 13 51 15 10

ing ret reat m en t . In th e clipp ed grou p of 13 pat ien ts, 100% h ad r ysm s. W h en r u pt u red , t h ey cau se ICH in m ore t h an h alf of t h e
su ccessfu l clip ligat ion , 64% ach ieved fu n ct ion al in depen den ce cases. Advan ced age, p oor grad e, rebleed in g before t reat m en t ,
(m GOS I–II), w ith n o recurren ce. Pat ien ts in th e clipped group ICH, IVH, an d severe preop erat ive hydroceph alu s p redict u n fa-
did sligh tly bet ter, but the differen ce did not reach stat istical sig- vorable outcom es.
nifican ce and m ay be attributable to selection bias because sicker Microsurgical clipping is a safe an d effect ive treatm en t m ethod
an d older pat ien ts w ere preferen t ially placed in th e coiled grou p. for th ese an eu r ysm s w it h t h e sam e com p licat ion rates as for
In th e largest series to date, Leh ecka et al39 rep or ted th eir ex- an eur ysm s at oth er locat ion s. At raum at ic open ing of th e in ter-
perien ce w ith 501 dACA an eu r ysm an d focu sed on th e m icrosu r- h em isph eric fissu re, preser vat ion of m ajor drain ing vein s, accu-
gical era bet w een 1980 an d 2005, en com passing 427 pat ien ts; rate localizat ion of th e an eu r ysm , an d gain ing proxim al con t rol
17 pat ien t s w ere t reated by en dovascular m ean s. Leh ecka et al’s are n ecessar y for a safe operat ion . Th e in ten t ion al use of a tem -
overall outcom e is rem arkable, w ith on ly 1% m ort alit y an d 12% porar y clip, th e select ion of an ap p rop riate an eu r ysm clip, an d
m orbidit y. th e u se of m icrovascu lar flow Dopp ler son ography or in docya-
n in e green angiography aid in th e preser vat ion of th e dACA an d
its bran ch es. Th ere are lim ited dat a com p aring surgical clipp ing
w ith en dovascular th erapy, an d alth ough each m odalit y h as its
ow n un ique ch allenges, both seem appropriate for th e t reat m ent
■ Conclusion of dACA aneur ysm s after careful patient selection. Occlusive t reat-
Dist al ACA an eu r ysm s are u su ally sm all, regard less of t h e r u p - m en t of un rupt ured DACA an eur ysm s sm aller th an 7 m m is jus-
t u re st at u s, an d are frequ en t ly associated w it h m u lt ip le an eu - t ifiable in pat ien ts w ith an oth er w ise good progn osis.

References
1. Sugar O, Tin sley M. Aneur ysm of term in al por t ion of anterior cerebral ar- 8. Sh ucar t WA. Dist al an terior cerebral ar ter y aneu r ysm s. In : Apu zzo MLJ,
ter y. Arch Neurol Psych iat r y 1948;60:81–85 ed. Brain Su rger y: Com plicat ion Avoidan ce an d Man agem en t . New York:
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ar ter y an eu r ysm s. Su rg Neu rol 1999;52:128–135, d iscu ssion 135–136 9. W isoff JH, Flam m ES. An eu r ysm s of t h e d ist al an ter ior cerebral ar ter y
3. Hernesn iem i J, Tapan in ah o A, Vapalah t i M, Niskan en M, Kari A, Luu k- an d associated vascu lar an om alies. Neu rosu rger y 1987;20:735–741
konen M. Saccular aneur ysm s of th e dist al an terior cerebral arter y an d it s 10. Yosh im oto T, Uch ida K, Suzuki J. Surgical t reat m en t of dist al an terior ce-
bran ch es. Neurosurger y 1992;31:994–998, discu ssion 998–999 rebral arter y an eur ysm s. J Neurosurg 1979;50:40–44
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ter y: report of 14 cases and a review of th e literat ure. Surg Neurol 1998; an eur ysm s. Surg Neurol 2008;70:153–159, discu ssion 159
50:130–139, discussion 139–140 12. Man n KS, Yue CP, Wong G. An eur ysm s of the pericallosal-callosom argin al
5. Oh n o K, Mon m a S, Suzuki R, Masaoka H, Mat sush im a Y, Hirakaw a K. Sac- jun ct ion . Surg Neurol 1984;21:261–266
cu lar an eur ysm s of th e dist al an terior cerebral ar ter y. Neu rosurger y 13. Nish ioka H. Repor t on th e cooperat ive st u dy of in t racran ial an eur ysm s
1990;27:907–912, discussion 912–913 and subarach noid h em orrh age. Sect ion VII. I. Evaluat ion of the con ser va-
6. Proust F, Tou ssain t P, Han n equin D, Raben en oïn a C, Le Gars D, Fréger P. t ive m an agem en t of ru pt ured in t racran ial an eur ysm s. J Neurosurg 1966;
Ou tcom e in 43 pat ien t s w ith dist al an terior cerebral ar ter y an eu r ysm s. 25:574–592
St roke 1997;28:2405–2409 14. Snyckers FD, Drake CG. An eur ysm s of th e dist al an terior cerebral arter y. A
7. Yaşargil MG. Dist al anterior cerebral arter y an eur ysm s. In : Yaşargil MG, report on 24 verified cases. S Afr Med J 1973;47:1787–1791
ed. Microneurosurgery, vol 2. New York: Thiem e Medical Publishers; 1984: 15. Nguyen TN, Raym on d J, Roy D, et al. En dovascular t reat m ent of perical-
224–231 losal an eur ysm s. J Neurosurg 2007;107:973–976

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16. Perlm ut ter D, Rh oton AL Jr. Microsu rgical anatom y of the dist al an terior 30. Leh ecka M, Dash t i R, Hern esn iem i J, et al. Micron eurosurgical m anage-
cerebral ar ter y. J Neurosu rg 1978;49:204–228 m en t of aneur ysm s at A3 segm ent of an terior cerebral ar ter y. Surg Neurol
17. Perlm u t ter D, Rh oton AL Jr. Microsu rgical an atom y of t h e an ter ior 2008;70:135–151, d iscussion 152
cerebral- an terior com m un icat ing-recurren t ar ter y com plex. J Neurosurg 31. Leh ecka M, Dash t i R, Hern esn iem i J, et al. Micron eurosurgical m anage-
1976;45:259–272 m en t of an eur ysm s at th e A2 segm en t of anterior cerebral ar ter y (proxi-
18. Bapt ist a AG. St udies on th e Ar teries of th e Brain . II. Th e An terior Cerebral m al pericallosal ar ter y) an d it s fron tobasal bran ch es. Surg Neurol 2008;
Arter y: Som e An atom ic Feat ures an d Th eir Clin ical Im plicat ion s. Neu rol- 70:232–246, discussion 246
ogy 1963;13:825–835 32. Leh ecka M, Dash t i R, Hern esn iem i J, et al. Micron eurosurgical m anage-
19. Royand F, Carter P, Guthkelch N. Distal anterior cerebral artery aneur ysm s. m en t of an eur ysm s at A4 an d A5 segm en t s an d dist al cort ical bran ch es
In : Car ter LP, Spet zler RF, Ham ilton MG, eds. Neurovascular Surger y. New of an terior cerebral ar ter y. Surg Neurol 2008;70:352–367, discu ssion 367
York: McGraw -Hill, Health Profession s Division s; 1995:717–728 33. Lau LS, Ban n an E, Tress B. Pseudot um our of th e corpu s callosum due to
20. Rh oton AL Jr. Th e cerebral vein s. Neurosurger y 2002;51(4, Suppl):S159– subarach n oid h aem orrh age from pericallosal an eur ysm . Neuroradiology
S205 1984;26:67–69
21. Park J, Ham m IS. An terior in terh em isph eric approach for dist al an terior 34. Horiu ch i T, Nit t a J, Nakagaw a F, Hongo K. Horizon t al con t ralateral ap -
cerebral ar ter y an eu r ysm su rger y: p reop erat ive an alysis of t h e ven ou s proach for th e dist al an terior cerebral arter y an eur ysm : tech n ical n ote.
an atom y can h elp to avoid ven ou s in farct ion . Act a Neu roch ir (W ien ) Surg Neurol 2009;72:65–68
2004;146:973–977, discussion 977 35. Al-Kh ayat H, Kopit n ik TA. Prim ar y en d-to-en d an astom osis of an terior
22. Sin dou M, Pelissou - Guyot at I, Mer ten s P, Keravel Y, Ath ayde AA. Peri- cerebral ar ter y dissect ing an eu r ysm : techn ical case repor t an d review of
callosal an eur ysm s. Su rg Neurol 1988;30:434–440 literat ure. Neurosurger y 2004;55:435
23. Leh ecka M, Porras M, Dash t i R, Niem elä M, Hern esn iem i JA. An atom ic fea- 36. Critchley M. The an terior cerebral ar ter y, and it s syn drom e. Brain 1930;
t ures of dist al anterior cerebral ar ter y an eur ysm s: a det ailed angiograph ic 53:120–165
an alysis of 101 p at ien t s. Neu rosu rger y 2008;63:219–228, discu ssion 37. Kassell NF, Torn er JC, Jan e JA, Haley EC Jr, Adam s HP. The In tern at ion al
228–229 Cooperat ive St udy on th e Tim ing of An eu r ysm Su rger y. Par t 2: Surgical
24. Asari S, Nakam ura S, Yam ada O, Beck H, Sugat ani H. Traum at ic an eur ysm result s. J Neurosurg 1990;73:37–47
of periph eral cerebral ar teries. Repor t of t w o cases. J Neurosurg 1977; 38. Pan dey A, Rosenw asser RH, Vezn edaroglu E. Man agem en t of dist al an te-
46:795–803 rior cerebral ar ter y an eu r ysm s: a single in st it ut ion ret rospect ive an alysis
25. Fleischer AS, Pat ton JM, Tin dall GT. Cerebral aneu r ysm s of t raum at ic ori- (1997–2005). Neurosurgery 2007;61:909–916, discussion 916–917
gin . Surg Neurol 1975;4:233–239 39. Leh ecka M, Leh to H, Niem elä M, et al. Dist al an terior cerebral ar ter y an eu-
26. Nakst ad P, Norn es H, Hauge HN. Trau m at ic an eur ysm s of the pericallosal r ysm s: t reat m en t an d outcom e an alysis of 501 pat ien t s. Neurosurger y
arteries. Neuroradiology 1986;28:335–338 2008;62:590–601, d iscussion 590–601
27. Lam CH, Mon tes J, Farm er JP, O’Gorm an AM, Meagh er-Villem ure K. Trau- 40. Ot an i N, Takasato Y, Masaoka H, et al. Clin ical feat u res an d su rgical ou t-
m at ic aneur ysm from sh aken baby syn drom e: case repor t . Neurosurger y com es of ru pt ured dist al an terior cerebral ar ter y an eur ysm s in 20 con -
1996;39:1252–1255 secut ively m an aged pat ien t s. J Clin Neurosci 2009;16:802–806
28. Sen egor M. Traum at ic pericallosal an eur ysm in a pat ient w ith n o m ajor
t raum a. Case repor t . J Neu rosurg 1991;75:475–477
29. Levin HS, Goldstein FC, Gh ost in e SY, Wein er RL, Crofford MJ, Eisen berg
HM. Hem isph eric discon nect ion syn drom e persist ing after an terior cere-
bral arter y an eur ysm ru pt u re. Neurosurger y 1987;21:831–838

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53 Comprehensive Management of Distal
Anterior Cerebral Artery Aneurysms
Daniel W. Zum ofen, Donato R. Pacione, Peter Kim Nelson, and How ard A. Riina

Dist al an terior cerebral ar ter y (dACA) an eu r ysm s are defin ed as terior to th e gen u in 60% of cases, in ferior to th e gen u in 30% of
aneurysm s arising from the anterior cerebral arter y (ACA) distal to cases, an d su p erior to th e gen u in 5% of cases.5 Dist al to its pri-
the an terior com m unicating arter y (ACoA) com plex. They accoun t m ar y bifu rcat ion , t h e pericallosal ar ter y t yp ically ru n s in th e
for 6% of all in t racran ial an eu r ysm s.1 Ru pt ured dACA an eu r ysm s pericallosal cistern in close p roxim it y to th e body of th e corpu s
represen ted 4.4% of th e In tern at ion al Su barach n oid An eur ysm callosu m . Th e p ericallosal ar ter y h as a variable set of cor t ical
Trial (ISAT) coh or t .2,3 W h ereas t h e m ajorit y of u n ru pt u red dACA bran ch es in cluding th e ar ter y of th e m argin al sulcus, an d a vari-
an eu r ysm s are fou n d in cid en t ally, r u pt u red d ACA an eu r ysm s able n u m ber of in ter n al p ar iet al bran ch es. At th e level of t h e
com e to clin ical at ten t ion prim arily w ith classic m an ifest at ion s splen iu m , th e pericallosal ar ter y becom es th e anastom ot ic an te-
of acute su barach n oid h em orrh age (SAH), in cluding th un derclap rior sp len ial ar ter y. Th e callosom argin al ar ter y ru n s in th e peri-
h eadach e, an d acu te loss of con sciou sn ess. More specific clin ical callosal cistern, at a variable distan ce from the body of the corpus
fin dings m ay in clu de acu te on set of u n i- or bilateral p arasagit tal callosu m , bu t m ost com m on ly at th e level of th e cingu late su l-
cor t ical syn drom e, sup p lem en tar y m otor area syn drom e, cingu- cus. From th e callosom argin al arter y origin ates a variable set of
late syn drom e, an d a variet y of fron t al lobe syn drom es resu lt ing cor t ical bran ch es, in clu ding an an terior, m iddle, an d p osterior
eith er from m ass effect or st roke. Typ ical ACA an eu r ysm s arise in tern al fron t al bran ch . Th e paracen t ral ar ter y arises eith er from
eith er from a given set of ar terial bran ch ing p oin t s (bifu rcat ion the pericallosal or th e callosom arginal artery, depen ding on their
t ype), or along th e tor t uou s ACA segm en t s p rim arily aroun d th e respect ive predom in an ce (Fig. 53.1). In term s of territorial vas-
gen u of th e corpus callosu m (sidew all t ype). Com m on feat ures cu lar sup ply, bran ch es of th e dACA su pp ly th e an terior par t of
relevan t for t h erapy in clu d e sm all size, u n favorable d om e-to - th e corp u s callosu m , cingu late gyr u s, an d th e m edial asp ect of
n eck rat io, an d t h e p resen ce of an eloqu en t bran ch ar ising from th e fron t al an d p ariet al lobe. Cor t ical bran ch es of th e dACA u su -
a broad an eu r ysm base. At yp ical an eu r ysm s in clu d e saccu lar ally supply th e m ost cran ial por t ion of th e fron tal (superior fron -
an d fu sifor m an eu r ysm s of t rau m at ic, m ycot ic, an d ar ter iove- tal, prefron tal, precen t ral gyri), an d pariet al lobe (postcen t ral
n ou s m alform at ion -associated et iology. an d su perior parietal gyri).

■ Anatomic Considerations ■ Aneurysm Characteristics


Th e ACA is classically su bd ivided in to five segm en t s.4 In th e A1 Dist al ACA an eur ysm s arise in 70 to 80% of cases from th e peri-
segm en t , th e proxim al ACA cu r ves arou n d th e opt ic app arat u s, callosal-callosom argin al bifu rcat ion .6 Th is con figu rat ion is called
bet w een th e in tern al carot id ar ter y (ICA) bifurcat ion an d th e “loco classico.”6 Th ere is con siderable variat ion regarding th e p o-
ACoA com plex. Th e A2 segm en t exten ds bet w een th e ACoA com - sit ion of the pericallosal-callosom arginal bifurcation in relation to
plex an d th e rost r u m of th e corp u s callosu m w h ere th e ACA ru n s the corpus callosum . Consequen tly, pericallosal-callosom arginal
an ter iorly along t h e lam in a ter m in alis. Th e A3 segm en t goes bifurcat ion an eur ysm s are sit uated an terior to th e gen u in 70%of
arou n d th e gen u of th e corp u s callosum an d can be fu rth er clas- cases, in ferior to th e gen u in 18%, above th e body in 6%, an d su -
sified as p roxim al (in ferior to th e gen u ), m iddle (an terior to th e perior to the genu in 1%.5,7 “Non loco classico” saccular aneur ysm s
gen u ), an d distal (su perior to th e gen u). Th e A4 segm ent is in th e arise from th e orbitofron tal bifu rcat ion in 5%of cases, from dist al
an terior pericallosal cistern w h ere th e pericallosal and calloso- A4/A5 bran ch ing poin t s in 4%, an d from th e fron topolar bifurca-
m argin al bran ch es r u n along an d above th e body of th e corpu s t ion in 2%.5,7 Saccu lar an eu r ysm s of th e dACA are discovered at a
callosum . Th e A5 segm en t is th e m ost distal; it is posterior to an com p arat ively sm all average size of 4.2 m m .5 In th e con text of
im agin ar y ver t ical lin e draw n at th e level of th e coron al sut u re. SAH, th eir average diam eter is 7.4 m m ,5 bu t rough ly t w o-th irds
Altern at ively, th e ACA can be divided in to a p roxim al ACA th at are fou n d to be sm aller t h an 5 m m at th e t im e of r u pt u re.8,9
in clu des th e A1 segm en t an d ACoA com p lex, an d a distal ACA Oth er frequ en tly en coun tered ch aracterist ics of ru pt ured dACA
t h at com p r ises t h e segm en t s A2 to A5. Th e bran ch ing p at ter n an eur ysm s in clude an eloquen t bran ch (e.g., pericallosal ar ter y)
of th e dACA is h igh ly variable. A proxim al orbitofron tal bran ch arising from th e an eur ysm base in u p to 94%, an irregu lar dom e
an d a m ore distal fron topolar bran ch t ypically arise from th e sh ap e in 83%, an d a large base (n eck-to-dom e rat io > 1:2) in 80%
A2 t r u n k. Th e d ACA t h en d ivid es, at t h e level of it s p r im ar y bi- in large series.5 Gian t dACA an eur ysm s h ave been described,9 bu t
fu rcat ion , in to a p er icallosal an d a callosom argin al ar ter y. Th is rem ain exceedingly rare in daily pract ice. Dist al ACA an eur ysm s
p er icallosal-callosom argin al bifu rcat ion is, in t h e m ajor it y of are associated w ith at ypical A2 variat ion s in 23% of all cases, in -
cases, in th e A3 segm en t . More p recisely, th e bifu rcat ion lies an - clu ding a bih em isp h eric ACA in 15%, a t r u e azygou s disp osit ion

613

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614 V Cerebral and Spinal Aneurysms

a b

Fig. 53.1a,b (a) Digital angiography in lateral view of an internal carotid arises from the callosom arginal trunk. The pericallosal-callosom arginal
artery (ICA) injection in an early arterial phase. In this pericallosal-dominance bifurcation is situated above the genu of corpus callosum . The relation of
disposition the paracentral artery arises from the dom inant pericallosal the coronal suture to the parasagit tal bridging veins and the pericalloso-
trunk. The pericallosal-callosom arginal bifurcation is situated above the callosom arginal bifurcation is shown in the bone window. (a, courtesy of
genu of the corpus callosum and anterior to the coronal suture. (b) Sagit tal Maksim Shapiro, MD, section of Neurointerventional Radiology, Depart-
m axim um intensit y projection reconstruction computed tom ography angi- m ent of Radiology, New York Universit y Langone Medical Center, New
ography. In this callosomarginal dominant disposition the paracentral artery York, NY.)

in 4%, an d a t riplicate ACA in 4%.5 Th ere is n o sign ifican t associa- An eur ysm Trial (BRAT) 12 fou n d a sign ifican t ly low er rate of p oor
t ion bet w een th e side of th e d om in an t A1 an d th e lateralit y of outcom e an d a t ren d for a h igh er rate of recurren ce, but n o sta-
th e d ACA an eu r ysm . Most ru pt u red dACA an eu r ysm s are m id- t ist ically sign ifican t differen ce in th e rebleeding rate, for en do-
lin e an eu r ysm s, h aving th eir dom e p oin t ing u pw ard an d dor- vascular versus open surger y in pat ien t s w ith a ru pt ured an te-
sally. On ly 25% are fou n d to h ave a laterally p oin t ing dom e. Th is r ior circu lat ion an eu r ysm . Ret rosp ect ive m u lt ivar iate an alysis
disp osit ion p ar t icu larly p redisp oses th e an eu r ysm dom e to be of r upt ured pericallosal an eur ysm s in dicates th at en dovascu lar
st u ck again st , or bu ried in to, th e fron t al lobe paren chym a in case th erapy m ay ach ieve low er m orbidit y an d low er periprocedu ral
of ru pt u re. Fin ally, th ere is a st rong associat ion w ith m u lt iple an - m ortality.13 More precisely, intraprocedural m ortality w ith m icro-
eu r ysm s in on e-th ird 8 to n early h alf10 of all cases. In th e presen ce su rgical clipp ing is 0.4% an d m orbid it y is 15% in exp er t h an ds.1
of m ultiple an eur ysm s, con com itan t an eu r ysm s are foun d on th e In com p arison , en dovascu lar m an agem en t h arbors a ver y low
m iddle cerebral arter y bifurcation in 60%of cases, intracranial ICA periprocedu ral m or talit y, an d a m orbidit y of rough ly 9% in a
in 15%, ACoA com p lex in 10%, an d p osterior circulat ion in 6%.5 m et a-an alysis of large series. Th is rate is 11% if on ly rupt ured
dACA an eu r ysm s are taken in to accou n t .9 Despite th ese fin dings,
m icrosurgical clipping rem ain s th e gold stan dard, en abling com -
plete aneurysm obliteration in 90%of cases and subtotal occlusion
■ Indications and Modality of Therapy in 5% of cases.1 Follow ing th e in t roduct ion of m odern coiling
tech n iqu es for dACA an eu r ysm s,14 occlu sion rates of en d ovas-
Indications to Treat Ruptured dACA cu lar th erapy h ave im proved from as low as 25%15 to com p lete
Aneurysms obliterat ion in 50% of cases, an d n ear com plete occlu sion , de-
W it h t h e except ion of grad e 5 SAH, t h ere is lit t le d ebate on fin ed as > 90% occlu sion , in 45% of cases.9 If n ear-tot al occlu sion
w h eth er or n ot to t reat r upt ured dACA an eu r ysm s to preven t po- is con sidered a sat isfactor y result , en dovascular th erapy is n ow
ten t ially fat al recurren t h em orrh age. With regard to th e t im ing w ith in th e range of open surger y in term s of its abilit y to exclude
of th e procedu re, w e cu rren tly favor, in lin e w ith m ost academ ic dACA an eur ysm s from th e arterial circu lation .
cen ters, a “n ext day, first p osit ion ” st rategy, assum ing th at th e A key issu e for en dovascular th erapy is th e du rabilit y of an eu-
pat ien t h as been stabilized an d n ot deteriorat ing. r ysm occlusion , an d h en ce it s abilit y to protect from SAH over
t im e. Th e an eu r ysm recu rren ce rate after com plete clipp ing for
an terior circulat ion an eur ysm s is 2% over 10 years.16,17 With re-
Open Surgical Versus Endovascular Therapy for Ruptured
gard to en dovascular therapy, recurrence requiring ret reatm ent in
dACA Aneurysms
reported series occurs in 15 to 20% of cases at 6 to 15 m onths,2,18
Rupt u red dACA an eu r ysm s h ave t radit ion ally been secu red sur- w h ich is w ith in th e range repor ted for coiled an eur ysm s located
gically.11 In recen t years, th e ISAT3 an d t h e Bar row Ru pt u red on oth er in t racran ial sites.9 Regarding recu rren t SAH after en do-

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53 Comprehensive Management of Distal Anterior Cerebral Artery Aneurysms 615

vascu lar th erapy for dACA an eur ysm s, sm all ret rospect ive series st u dies con t ain s a su bgrou p an alysis ad dressing sp ecifically th e
suggest a ver y low rer u pt u re rate at 12 m on th s,9 bu t th is follow - n at ural h istor y of dACA an eur ysm s. In curren t pract ice, a th resh -
up period is too sh or t to d raw st rong con clusion s. In ou r opin ion , old for t reat m en t for asym ptom at ic dACA an eu r ysm s m ay be set
ISAT,3 even th ough n ot sp ecific for dACA an eu r ysm s, rem ain s t h e at arou n d 4 to 5 m m . We base th is recom m en dat ion on th e as-
m ost reliable eviden ce in th is regard, sh ow ing a rebleed ing rate su m pt ion th at th e con clu sion s draw n from th e ISUIA an d UCAS
after endovascular therapy of 0.2%per patient per year, and hence t rials app ly to dACA an eu r ysm s, bu t keep in m in d th at m ore th an
n o sign ifican t differen ce in th e frequen cy of rebleeding com - h alf of all r upt ured dACA an eur ysm s are foun d to be sm aller th an
pared w ith th at after op en su rger y. Taken all togeth er, th ere is n o 5 m m in ret rospect ive series.8,9 In lin e w ith UCAS an d oth er re-
evidence th at en dovascular th erapy h arbors an excess long-term por t s,5 w e recom m en d low ering th e th resh old for prophylact ic
m or t alit y, d esp ite a recan alizat ion r isk, or a ret reat m en t rate an eur ysm t reat m en t in th e presen ce of an irregular dom e sh ape,
p oten t ially h igh er th an th at of open su rger y.19 Given it s proven a m u lt ilobulated geom et r y, or an eu r ysm grow th on serial im ag-
low er m orbidit y, it is reason able in ou r opin ion to favor en dovas- ing. Finally, a n u m ber of an eu r ysm -in depen den t factors n eed to
cular th erapy for th ose dACA an eur ysm s w h ere both m odalit ies be t aken in to con siderat ion , su ch as pat ien t age, gen eral h ealth
seem equ ally su ited from a tech n ical poin t of view. con dit ion , p reviou s an eu r ysm al SAH, sp ecific system ic diseases
Th ere are a few sit u at ion s w h ere th e su rgical ap p roach m ay (e.g., au tosom al dom in an t p olycyst ic kid n ey d isease, Eh lers-
be con sidered m ore favorable. Classically, th e presen ce of an ex- Danlos, Marfan syndrom e), the presence of significant aneurysm -
p an d ing h em atom a h as been con sid ered as a st rong argu m en t related an xiet y, an d m ost im por tan tly th e in form ed preferen ce
in favor of surger y. Even th ough w e are n ot aw are of con clu sive of th e pat ien t.
eviden ce th at h em atom a evacuat ion en ables a bet ter n eurologic
outcom e, w e recogn ize th at rem oval of th e h em atom a m ay de-
Open Surgical Versus Endovascular Therapy for
crease th e in t racran ial p ressu re an d sp eed recover y. From a su r-
Unruptured dACA Aneurysms
gical p oin t of view , h em atom a rem oval m ay also in crease t h e
available w orkin g sp ace d u r in g an in terh em isp h er ic ap p roach , Th e qu est ion of op en su rgical versu s en dovascu lar th erapy for
an d h en ce m ay con sid erably facilit ate su bsequ en t an eu r ysm unruptured saccular anterior circulation aneurysm s has been ex-
clip ping. Bifu rcat ion t yp e dACA an eu r ysm s ten d to be of sm all ten sively debated, leading, over recen t years, to th e progressive
size, h ave u n favorable dom e-to-n eck rat ios, an d h arbor eloqu en t accept an ce of th e en d ovascu lar ap p roach as a valid alter n at ive
bran ch es arising from th eir broad an eur ysm base. Even th ough to op en su rger y,27,29,30 W it h regard to t h e ou tcom e after d ACA
th ere are variou s descript ion s of com plex en dovascu lar opt ion s an eur ysm th erapy, eviden ce is sparse but suggests th at both
for th ese an eur ysm s,2,20–24 w e curren tly th in k th at th ere m ay be tech n iques provide ver y sat isfying results for “loco classico” an -
a h igh er rate of durable com plete obliterat ion w ith open surgical eur ysm s if com pared w ith th eir n at ural h istor y. Un der appropri-
clip ping in th ese cases. ate circu m stan ces, th ere m ay be a lesser rate of p oor ou tcom e
Th ere are a few sit u at ion s w h ere th e en d ovascu lar ap proach (m odified Ran kin scale [m RS] score of 3 to 6) for en dovascular
m ay be con sidered m ore favorable. In curren t pract ice, w e prefer t h erapy, bu t p robably at th e cost of a h igh er ch an ce for recu r-
an en dovascular st rategy in cases of diffu se but exten sive SAH ren ce over t im e, an d t h u s t h e n eed for m ore regu lar follow -u p
(e.g., h igh -grade SAH) w h ere th e brain is sw ollen an d subarach - im aging, an d p robably a h igh er likelih ood of requ ir ing rep eat
n oid dissect ion h en ce is tech n ically m ore ch allenging. Th is is t reat m en t .13 In curren t pract ice, a few issues m ay be con sidered
par t icu larly valid for an eu r ysm s located p roxim al to th e rost r u m w h en debat ing w h eth er to clip or to coil.
of th e corpus callosu m , as proxim al con t rol is ach ieved, in th ese With regard to th e an atom ic locat ion , en dovascu lar th erapy
cases, on ly relat ively late in th e dissect ion , often after h aving ex- becom es progressively m ore tech n ically ch allenging th e m ore
posed th e an eu r ysm it self.25,26 Fin ally, w e cu rren tly favor an en - dist al th e an eu r ysm is located on th e ar terial t ree an d th e m ore
dovascular approach for cases of m ultiple aneur ysm s, un less both tor t uou s th e ar terial access. In con t rast to su rger y, th e evaluat ion
an eur ysm s can be easily reach ed by th e sam e surgical approach . of en dovascular access n eeds to t ake in to accoun t th e con st it u-
We can con clu de th at both en dovascu lar an d m icrosu rgical t ion of th e ext racran ial vascu lat u re, in p ar t icu lar th e aor t ic arch
t reat m en t of r u pt u red dACA an eu r ysm s are h igh ly effect ive an d th e su pra-aor t ic ar terial t ree. Su rger y, on th e oth er h an d, is
t reat m en t st rategies. Based on th e available body of eviden ce, w e lim ited by the available an atom ic corridors, an d h en ce t urn s out
curren tly recom m en d offering en dovascular em bolizat ion as a to be m ore involved for an eur ysm s of th e proxim al A3 segm en t ,
prim ar y t reat m en t opt ion for ru pt u red dACA an eu r ysm s involv- part icu larly for th ose lesion s h aving th eir n eck ju st below th e
ing a favorable angioarch itect ure. gen u of th e corpus callosum . Fin ally, th e presen ce of associated
ACA an om alies is, in our opin ion , a st rong argum en t in favor of
Indications to Treat Unruptured dACA an open surgical app roach , as dam age to th e paren t arter y, or its
bran ch es, m ay poten t ially result in irreversible bilateral isch em ic
Aneurysms com p licat ion s.
The natural histor y of intracranial aneur ysm s has been addressed With regard to an eur ysm con figurat ion , th e rate of coil com -
by th e In tern at ion al St u dy of Un r upt ured In t racran ial An eu - pact ion an d reperfu sion is part icu larly h igh in cases w h ere an
r ysm s (ISUIA) t rial,27 an d m ore recen tly th e Un r u pt u red Cerebral eloquen t branch (e.g., callosom arginal arter y) arises from a broad
An eur ysm St u dy (UCAS) of Japan .28 W h ereas th e ISUIA fou n d a an eu r ysm base.31 En d ovascu lar adju n ct s su it able to ad d ress
vir t u ally absen t r u pt u re risk for asym ptom at ic an terior circula- large-n eck con figu rat ion s (e.g., balloon an d sten t rem od elin g
t ion an eu r ysm s sm aller th an 7 m m , th e UCAS fou n d an an n u al tech n iques) or en dolum in al recon st ru ct ive devices are, at pres-
rupt ure risk of rough ly 1% for an eur ysm s larger th an 4 m m . Un - en t , of lim ited u se in t h e dACA, du e to th e sm all paren t ar ter y
for t u n ately, n eith er of th ese t w o large p rospect ive m ult icen ter caliber, an d in su fficien t su pp or t of th e deliver y con st ru ct . Th e

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616 V Cerebral and Spinal Aneurysms

ch oice, th erefore, of th e m ost advan t ageou s app roach for u n r u p - for proxim al con t rol. A bicoron al skin in cision in com bin at ion
tured dACA aneur ysm s depends on a w ide range of anatom ic and w ith a larger fron tal cran iotom y can be con sidered in th e con text
tech n ical con siderat ion s. In our opin ion , th e in dicat ion s for com - of SAH. Taking advan tage of a hybrid operat ing room , w e posi-
plex en dovascu lar tech n iqu es rem ain to be defin ed in th e dACA, t ion , in selected cases, a balloon cath eter p roxim al to th e ru pt u re
an d open surger y sh ould, at presen t , be favored for com plex- site, en abling safer m icrosu rgical n eck dissect ion in th e absen ce
sh ap e, w ide-n eck bifu rcat ion t yp e dACA an eu r ysm s, p ar t icu larly of direct surgical proxim al con t rol. Th e pat ien t is placed in th e
in th e p resen ce of an eloqu en t bran ch . su p in e posit ion , th e n eck exten ded 15 degrees, an d th e h ead is
fixed in a Mayfield h ead clam p. We perform a t ran sverse skin
in cision eith er in a skin crease in th e low er foreh ead or along th e
eyebrow, depen ding on th e pat ien t’s physiogn om y (Fig. 53.2a).
■ Surgical Approaches for dACA In terh em isp h er ic access is est ablish ed via a 2.5-cm keyh ole
cran iotom y just above th e glabella (Fig. 53.2b). Altern at ively, a
Aneurysms bicoron al skin in cision , h idden beh in d th e h airlin e, en ables re-
Ch allenges of open surger y for dACA an eur ysm s in clu de a rela- flect ing th e soft t issue flap in th e subgaleal plan e. A larger size
t ively n arrow op erat ive field, an d an an eu r ysm dom e th at ten ds fron t al cran iotom y is th en p erform ed over th e m idlin e. We gen -
to adh ere to th e surroun ding st ru ct ures (e.g., cingulate gyrus).14 erally prefer n ot to open t h e fron t al p aran asal sin u ses. If op en ing
Clipping p rocedu res h en ce h arbor a su bst an t ial risk of prem a- can n ot be avoid ed, m arsu p ializat ion of th e sin u s cavit y an d care-
t u re an eu r ysm al r u pt u re d u r in g in adver ten t ret ract ion .32 We fu l obliterat ion of th e fron tobasal du ct to avoid a postop erat ive
advocate tailoring th e cran iotom y for an angle of approach th at m ucocele can be perform ed. Th e dura is gen erally reflected su-
en ables early p roxim al con t rol, an d to reach th e an eu r ysm n eck p er iorly tow ard t h e su p er ior sagit t al sin u s, an d th e an eu r ysm
prior to exp osing th e an eu r ysm dom e. To fu r th er m in im ize th e is reach ed via an in terh em isp h eric su barach n oid dissect ion at a
risk of p rem at u re ru pt u re, an d to avoid isch em ic sequ elae from variable depth from th e dura, depen ding on its precise locat ion
su rger y, local subp ial resect ion of th e cingu late gyrus an d th e on th e ar terial t ree.
m ost an terior t ip of th e corpu s callosu m sh ou ld be con sidered
over forcefu l ret ract ion of t h e fron t al lobe. Resh ap in g of t h e
Parasagittal Interhemispheric Approach
an eu r ysm n eck w ith th e bipolar 5 an d using sm all cur ved t it a-
n iu m clip s m ay lim it in adver ten t sid e-bran ch en t rap m en t in We favor a parasagit tal in terh em isp h eric app roach p ar t icu larly
t h e clip blades. Real-t im e flow assessm en t w ith m icro-Dopp ler, for rupt ured an d un r upt ured dACA an eur ysm s th at h ave th eir
fluorescence-based angiography, and intraoperative transfem oral n eck above th e an terior t ip of th e corpu s callosum (Fig. 53.3).
angiography are addit ion al u sefu l tools to m in im ize th e risk of We ch oose, w ith few except ion s, a righ t-sided ap proach to ac-
ar terial com p rom ise an d to con firm an eu r ysm obliterat ion . com m odate righ t-h an ded su rgeon s, an d to avoid u n n ecessar y
ret ract ion of th e dom in an t left fron t al lobe. Except ion ally, a left-
sided ap p roach m ay be m ore favorable in t h e absen ce of any
Pterional Subfrontal Approach su it able cor r id or bet w een br idging vein s on t h e r igh t side, in
t h e case of a righ t laterally p oin t ing an eu r ysm dom e, or in th e
We favor t h is ap p roach for p roxim al A2 an eu r ysm s in clu d ing
presen ce of a sp ace-occu pying left in t racerebral h em atom a. CSF
th ose arising from th e orbitofron t al bifu rcat ion . Adm in ist rat ion
release from th e pericallosal cistern is n ot ver y efficien t in m any
of in t raven ou s m an n itol du ring th e cran iotom y, an d early cere-
cases. Preop erat ive in ser t ion of a lu m bar drain , p erip rocedu ral
brospin al fluid (CSF) drain age from th e basal cistern s, follow ed
in sert ion of an extern al ven t ricu lar drain age, or in t raoperat ive
p oten t ially by op en ing of th e lam in a ter m in alis, w ill rela x t h e
t ran scallosal ven t ricu lar pu n ct u re is u sefu l in relaxing th e brain
brain su fficien t ly to allow for ad equ ate su barach n oid w orking
sufficien tly to en able adequate in terh em isph eric w orking space,
space. Subpial resect ion of th e an terior gyr us rect u s m ay fur th er
especially in th e con text of SAH.
facilitate visu alizat ion of th e relevan t vascular st ruct ures w h ile
Th e pat ien t is posit ion ed su pin e w ith th e u p p er body elevated
lim it in g t h e requ ired ret ract ion of t h e fron t al lobe. In com p ar i-
30 degrees an d th e h ead flexed an d in n eut ral posit ion to en able
son to t h e classic ap p roach for ACoA com p lex an eu r ysm s, t h e
an ergon om ic w orking angle bet w een t h e cran iotom y an d t h e
su bp ial resect ion of t h e gyr u s rect u s is exten d ed m ore an ter i-
an eur ysm . Som e surgeon s m ay p refer a park ben ch posit ion , th e
orly, allow ing for ad equ ate w orking sp ace arou n d t h e an eu r ysm
h ead align ed parallel to th e floor. Alth ough th is posit ion en tails
n eck.
u sing gravit y for ret ract ion , w e cu rren tly prefer a n eu t ral posi-
t ion , as it en ables, in ou r opin ion , a m ore n at u ral u n derstan ding
of t h e relevan t an atom y. In ou r exp er ien ce, t h e in ter p ret at ion
Anterior Interhemispheric Approach of th e angiograph ic ven ous ph ase an d it s correlat ion w ith pre-
We favor th e an terior in terh em isph eric ap proach for an eur ysm s subtract ion im ages reveals th e relat ionship bet w een the external
m ore th an 1 cm distal to th e ACoA com plex, bu t proxim al to th e lan dm arks of th e sku ll an d th e p at tern of th e bridging vein s, an d
genu of the corpus callosum . Aneur ysm s having their dom e point- h en ce en ables select ing an advan t ageous cran iotom y site.
ing st raigh t u p are part icu larly su it able for th is approach .33,34 Th e sagit t al su t u re is u sefu l to d efin e th e m id lin e an d th u s th e
Th e eyebrow in cision in com bin at ion w ith a m edial sup raorbit al expected course of th e superior sagit tal sinus. The coronal sut ure
keyh ole cran iotom y is an excellen t ch oice for n on ru pt u red dist al is a key lan d m ark for defin ing th e an terop osterior exten t of th e
A2 an eu r ysm s, given t h at th e an eu r ysm n eck is in ferior to th e cran iotom y. Over th e last d ecade, n eu ron avigat ion h as becom e a
gen u of th e corpu s callosum . A poten t ial dow n side of th is m eth od ver y useful add-on tool n ot on ly to con firm th e exten t of th e cra-
is th e lim ited w orking sp ace an d th erefore th e lim ited possibilit y n iotom y in relat ion to th e corridor bet w een bridging vein s, but

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53 Comprehensive Management of Distal Anterior Cerebral Artery Aneurysms 617

a b

Fig. 53.2a,b (a) Skin incision for supraorbital eyebrow approach. (b) Sm all supraorbital keyhole craniotomy. (a, courtesy of David A. Staffenberg, MD,
Departm ent of Plastic Surgery, New York Universit y Langone Medical Center, New York, NY.)

also to adjust th e angle of approach during th e in terh em isph eric t ive field to be en larged m edially by gen tle ret ract ion of th e su -
m icrodissect ion . perior sagit tal sin us an d th e falx cerebri. The posterior lim it of the
We gen erally perform a cran iotom y, crossing ~ 1 cm over th e cran iotom y sh ou ld be at a safe dist an ce from th e prim ar y m otor
m idlin e, an d exten ding 1 to 2 cm beh in d th e coron al sut ure. We area. If bleeding occurs from th e sin us, im m ediate irrigat ion is
exten d th e cran iotom y across th e m idlin e to en able th e opera- u sed to avoid air em boli. Th e dura is alw ays reflected tow ard t h e

a b

Fig . 53.3a,b Parasagit tal interhem ispheric approach for an unruptured (a) Digital subtraction angiography (DSA) three-dimensional (3D) rendering
pericallosal aneurysm . A 55-year-old wom an was incident ally found to of the right internal carotid artery (ICA) injection demonstrates a small peri-
have a pericallosal artery aneurysm . Due to the broad-based neck of the callosal aneurysm with a wide-based neck. The aneurysm is located distal to
aneurysm , the decision was m ade to treat this aneurysm with open surgical the genu of the corpus callosum . (b) Intraoperative DSA lateral projection
clipping through a right-sided parasagit t al interhem ispheric approach. demonstrating complete obliteration of the aneurysm after surgical clipping.

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618 V Cerebral and Spinal Aneurysms

sin u s, an d p ar t icu lar at ten t ion is p aid n ot to h arm any bridging At th at t im e, en d ovascu lar tech n iqu es w ere t h ough t to be an
vein s th at m ay be st uck to th e in n er side of th e parasagit tal du ra. adjun ct to surger y at best .23 Over th e past d ecade, h ow ever, th e
During in terh em isph eric dissect ion , th e ipsilateral brain is introduction of very sm all hydrophilic m icrocatheters and shape-
protected by a large p iece of n on adh eren t cot ton oid . In cu rren t able m icrow ires has significantly enhanced the trackabilit y, push-
pract ice, w e ten d to perform su rger y w ith ou t th e u se of fixed abilit y, an d torqu e respon siven ess of devices, th us en abling th e
ret ractors w h en ever p ossible. If ret ract ion is to be u sed , p ar- cath eterizat ion of an eu r ysm s as dist ally located as t h e term in al
t icu lar care m u st be t aken if t h e an eu r ysm d om e is bu r ied in ACA (Fig. 53.4).14 Desp ite th ese tech n ical refin em en t s, dACA an -
t h e fron t al h em isp h ere to avoid p rem at u re r u pt u re. Sp ecial at - eur ysm s, and pericallosal-callosom arginal bifurcation aneur ysm s
ten t ion m ust also be paid during ret ractor posit ion ing to avoid in part icular, st ill rem ain ch allenging from an en dovascular poin t
t rapp ing of sm all p refron tal ar terial bran ch es u n der th e ret ractor of view, in p ar t icu lar d u e to t h eir above-average r isk (rough ly
blade, as th is poten t ially result s in th e t ran sitor y supplem en t ar y 6%) of in t raprocedural an eu r ysm p erforat ion .9,18
m otor area syn drom e from local isch em ia. A key ch allenge in en dovascular th erapy of dACA an eur ysm s
Th e p osit ion of t h e ret ractor blad es sh ou ld be regu larly is establish ing adequ ate su ppor t ,18 th u s en abling a lesser degree
ch an ged , as p rolon ged ret ract ion of t h e cin gu late gyr u s m ay of cath eter deflect ion w h en en coun tering resist an ce. Th e in t ro-
easily result in t ran sien t akin et ic m ut ism . As an altern at ive to du ct ion of dedicated gu iding cath eters led to th e u se of t ri-axial
relying on fixed ret ractors, in t rodu cing cot ton oids at th e an terior arrangem ents, consisting typically of a 90-cm guide sheath in com -
an d p oster ior en d of t h e exp osu re m ay be u sefu l to keep t h e bin at ion w ith a guiding cath eter placed in th e subm an dibular
exposed site op en . in tern al carot id ar ter y, an d h en ce providing sign ifican t st abilit y
Regarding th e m icrosu rgical dissect ion , w e gen erally follow to th e h igh ly m an euverable m icrocath eter coil deliver y system .
th e falx to its in ferior border to iden t ify th e cingulate su lcus an d Over t h e p ast few years, in ter m ed iate gu id in g cat h eters w ere
both callosom argin al ar teries. Th ereafter, w e iden t ify th e body in t rodu ced. Th ese cath eters w ere design ed to be placed in t racra-
of th e corpu s callosu m by it s brigh t w h ite color. We th en dissect n ially, eith er in th e pet rous in tern al carot id ar ter y or even as dis-
both pericallosal ar teries in th e callosal cistern . In som e cases, tally as h aving th eir t ip poin t ing in to A1. Alth ough th eir use m ay
part icu larly in th e presen ce of an azygou s ACA from w h ich A2 p rovid e an ad d it ion al d egree of su p p or t , su bsequ en t flow re-
th e an eur ysm arises, it m ay be ver y difficu lt to decide on p reop - d u ct ion in th e ACA th eoret ically could result in hypoperfu sion
erat ive im aging. Th u s, w e iden t ify an adequ ate locat ion for tem - inju r y. As a last resor t , d irect carot id access h as been u sed to
porar y clip app licat ion on both ACAs proxim al to th e su spected sh or ten t h e access rou te, an d to in crease t h e st abilit y of th e
an eur ysm locat ion . An terior callosotom y via th e resect ion of a d eliver y system .31
sm all am ou n t of th e an terior callosu m m ay be con sidered to gain Microcatheter navigation in dACA segm ents m ay be technically
proxim al con t rol in an eu r ysm s h aving th eir n eck h idden beh in d ch allenging. Presh aping t h e t ip of th e gu idew ire in to a J-sh ape
th e an terior lim it of th e gen u of th e corp u s callosu m . Resect ion facilitates n avigat ion from th e term in al in tern al carot id arter y,
of th e genu in th e in fracallosal region m u st be st rictly avoided, as aroun d th e cur vat ure of th e proxim al ACA, an d fin ally in to th e
th is m ay p oten t ially resu lt in devast at ing postop erat ive n eu ro- selected dACA bran ch . If th e m icrocath eter can n ot be advan ced
psych ological deficits.35 sim u lt an eou sly w it h t h e gu id ew ire du e to excessive ten sion
For r u pt u red an eu r ysm s above th e an terior t ip of th e corpu s buildup, w e fin d it h elpfu l to n avigate th e guidew ire to a stable
callosu m , w e ten d to w ork arou n d th e u n secu red an eu r ysm via posit ion dist al to th e an eu r ysm , en abling it to be an ch ored, an d
a lim ited su bpial resect ion of th e ipsilateral cingu late gyrus, al- th en to d elicately periscope th e m icrocath eter over th e n ow st a-
low ing for p roxim al con t rol prior to th e m icrodissect ion of th e bilized w ire. Cath eterizat ion of a dACA an eur ysm is par t icularly
an eur ysm per se. On ce proxim al con t rol is est ablish ed, m icrodis- delicate w h en th e t ip of th e cath eter is p osit ion ed again st th e
sect ion is perform ed along th e p aren t ar ter y to th e an eu r ysm fragile an eu r ysm w all d u ring in it ial fram ing coil dep loym en t .
n eck. In u n rupt ured an eu r ysm s, it is reason ably safe to follow Due to th e lim ited respon siven ess of th e deliver y system in tor-
the cortical ACA branches proxim ally tow ard the aneur ysm w ith - t uou s segm en t s, w e recom m en d th e u se of a “seesaw ” st rategy.
out h aving previously est ablish ed proxim al con t rol. Th e an eu - On ce th e m icrocath eter h as passed th e an eu r ysm , w e gen tly pu ll
r ysm is u sually located on th e bran ch ing poin t of th e pericallosal back t h e gu id ew ire, an d t h en gen t ly let t h e m icrocat h eter slip
and callosom arginal arteries. The clip is usually applied parallel to back to t h e vicin it y of t h e an eu r ysm , w h ile th e cath eter t ip re-
th e pericallosal ar ter y. Sh ap ing of th e n eck w ith th e bip olar an d m ain s or ien ted tow ard t h e an eu r ysm n eck. As t h e m icrocat h e-
using a cu r ved clip m ay be u sefu l tech n iqu es to preven t bran ch ter ten ds to w edge th e A2, road m apping m ay n eed to be don e
en t rap m en t an d red u ce kin kin g of t h e p aren t ar ter y. Flow as- th rough th e m icrocath eter. Un for t un ately, con t rol run s p rior to
sessm en t by Dop p ler or in t raop erat ive angiograp hy is, in ou r coil det ach m en t are often n ot possible w ith th is tech n iqu e.14
opin ion , crucial, as m in im al kin king of th e sm all caliber A3/A4 Finally, the introduction of sm all three-dim ensional (3D) fram -
vessels easily lead s to im m ediate vessel com prom ise. Fin ally, w e ing coils an d soft t w o-dim en sional (2D) filling coils h as in creased
do n ot h esitate to rep osit ion th e clip , if n eed be, by u sing tem p o- th e tech n ical su ccess rate,31 en abling a redu ced rate of recu r-
rar y clips w h en n ecessar y. ren ce an d com pact ion . At presen t , w e feel caut ious about th e use
of com plex en dovascu lar tech n iques for dACA an eur ysm s. Th e
average size of a pericallosal arter y is rough ly 2.5 m m an d as
sm all as 0.8 m m m ore dist ally.36,37 Th e cu rren t gen erat ion of in -
■ Endovascular Considerations t racran ial sten t s op en s to 2.5 m m , an d , accord in g to t h e m an u -
At th e begin n ing of th e en dovascu lar era for an eur ysm th erapy, fact u rer, can n ot safely be u sed in vessels sm aller t h an 2 m m .
th e p erip h eral locat ion of dACA an eu r ysm s an d t h eir relat ively Moreover, th e sm all ar terial size usu ally p reclu des th e requ ired
sm all size u su ally preclu ded su ccessfu l en dovascular th erapy.2,15 d ou ble-m icrocat h eter access for com p lex en d ovascu lar tech -

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53 Comprehensive Management of Distal Anterior Cerebral Artery Aneurysms 619
Fig. 53.4a–c Coiling of ruptured pericallosal aneurysm . A 63-year-old
wom an presented with a Hunt-Hess grade V subarachnoid hem orrhage.
Angiographic im aging revealed a 4 m m × 3 m m aneurysm , with a wide-
based neck, at the bifurcation of the right callosom arginal artery. Given the
patient’s poor grade and age, we decided to treat this aneurysm with endo-
vascular coiling. The m orphology and distal location did not allow for com -
plete obliteration of the aneurysm with a sm all rem nant located at the
neck. (a) A 3D angiogram of right internal carotid artery (ICA) injection
dem onstrating a 4 m m × 3 m m aneurysm at the bifurcation of the right
callosomarginal artery with a wide neck. (b) Lateral view digital subtraction
angiography (DSA) of a right ICA injection dem onstrating the aneurysm .
(c) Postem bolization with near obliteration of the aneurysm and a sm all
rem nant at the aneurysm neck.

b c

n iques (e.g., jailing, balloon rem odeling). Given th e su rgical al- fract u re. Trau m at ic an eu r ysm s are classified in to t w o grou p s:
tern at ives, com plex en dovascular tech n iques, even if tech n ically t ru e an eu r ysm s, form ed by in com p lete inju r y to th e vessel w all,
feasible,24,38 rem ain , in our op in ion , too h azardous to use in th e an d pseudoan eur ysm s, form ed by a pseudow all th at developed
dACA at presen t . from th e blood clot after com p lete disru pt ion of th e vessel w all.
In curren t pract ice, it m ay be difficult to dist inguish bet w een
t h ese t w o en t it ies w it h t h e available im agin g tech n iqu es. Lit t le
is kn ow n abou t th e n at u ral h istor y of th is con dit ion ,43 but spon -
tan eous resolut ion seem s rath er except ion al, an d th ese fragile
■ Traumatic dACA Aneurysms an eur ysm s ten d to en large, presen t ing w ith delayed ru pt ure in
Trau m at ic an eu r ysm s are rare, represen t ing less th an 1% of all u p to 60% of cases.44 Given th e est im ated m or t alit y of u p to 54%
in t racran ial an eur ysm s,39,40 w ith th e pediat ric p opu lat ion h av- in case of rupt u re, prophylact ic exclu sion of th e an eur ysm al seg-
ing th e h igh est risk.41 With regard to th e dACA, th e pericallosal m en t is gen erally preferred over expectan t serial im aging.45,46
ar ter y is p ar t icu larly p ron e to t rau m at ic an eu r ysm for m at ion Su rgical an d en d ovascu lar p aren t ar ter y occlu sion h ave both
during closed h ead inju r y, du e to its close relat ion sh ip to th e free been est ablish ed as reliable th erapeut ic opt ion s.44 We cu rren tly
edge of th e falx cerebri. Altern at ively, t rau m at ic an eur ysm s m ay favor en dovascular proxim al paren t ar ter y occlu sion , as surgical
resu lt from direct p en et rat ing t rau m a (e.g., gun sh ot s, sh arp ob - m ort alit y h as been rep or ted to be as h igh as 22%,47 due to th e
jects),42 or cor t ical ACA bran ch en t rapm en t in an overlying sku ll fragilit y of th e lesion , an d h en ce th e h igh risk of p rem at u re ru p -

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620 V Cerebral and Spinal Aneurysms

t ure during m icrosurgical dissect ion (Fig. 53.5). We do n ot rou - tolerated due to sufficien t cor t ical back-flow distal to th e t rapped
t in ely recom m en d d irect coil em bolizat ion , even th ough good segm en t as w ell as collateral circu lat ion . Th e risk of sym ptom at ic
resu lt s h ave be e n d escr ibe d for t h ose t rau m at ic an e u r ysm s isch em ic sequ elae is rep or ted ly < 5%,48 an d h en ce w e rely on
h aving a favorable dom e-to-n eck rat io, an d being accessible for angiograp h ic collateral assessm en t to decid e w h eth er or n ot
m icrocath eterizat ion .43 Paren t ar ter y occlusion is gen erally w ell com plem en t ar y revascu larizat ion is required.

a b

c d

Fig. 53.5a–d Em bolization of traum atic aneurysm secondary to direct rifice the pericallosal artery just distal to its origin. Coils were placed distal
penetrating traum a. A 39-year-old m an presented after being stabbed to the site of the pseudoaneurysm to prevent glue cast from em bolizing
through the left eye. A noncontrast head computed tomography (CT) dem - the distal vessels, after which the injured segment of the pericallosal artery
onstrated a left front al intraparenchym al hem atom a as well as an was occluded using N-but yl cyanoacrylate. Postembolization angiography
interhem ispheric hem atom a. A CT angiogram dem onstrated a distal left dem onstrated m oderate collateralization from the left callosom arginal and
pericallosal artery pseudoaneurysm . An angiogram was perform ed and did posterior pericallosal artery. (a) CT angiogram , which dem onstrates a left
not dem onstrate the previously visualized pseudoaneurysm but instead pericallosal artery pseudoaneurysm . (b) Lateral digital subtraction angiog-
only a sm all area of stenosis. On further visualization it was noted that there raphy (DSA) left internal carotid artery (ICA) injection, which dem onstrates
was alternating systolic opacification with the cardiac cycle in the region of a sm all area of focal stenosis (arrow) in the region of the pseudoaneurysm .
the pseudoaneurysm suggestive of slow persistent bleeding. Vertebral ar- (c) Lateral fluoroscopy of the glue cast and coils. (d) Lateral DSA left ICA
tery injection dem onstrated the presence of a posterior pericallosal artery injection after em bolization dem onstrates no flow in the distal pericallosal
capable of possibly providing collateral flow. The decision was m ade to sac- artery with som e collateralization from the callosom arginal artery.

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53 Comprehensive Management of Distal Anterior Cerebral Artery Aneurysms 621

ciplin ar y team s to provide th e pat ien t w ith th e best t reat m en t


■ Conclusion option. Despite the relative equipoise of endovascular and m icro-
An eu r ysm s of t h e d ACA are rare an d ch allenging lesion s. We su rgical tech n iqu es, each ap p roach h as advan t ages for a select
advocate a case-by-case evaluat ion of th ese lesion s by m ult idis- grou p of dACA an eu r ysm s.

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14–15 an eu r ysm s. Neu rosu rger y 1992;31:979–980
15. Pierot L, Bou lin A, Cast aings L, Rey A, Moret J. En dovascular t reat m en t of 36. Tü re U, Yaşargil MG, Krish t AF. Th e ar teries of th e corpus callosum : a m i-
pericallosal arter y an eur ysm s. Neurol Res 1996;18:49–53 crosurgical anatom ic st udy. Neurosurger y 1996;39:1075–1084, discus-
16. David CA, Vish teh AG, Spet zler RF, Lem ole M, Law ton MT, Partovi S. Late sion 1084–1085
angiograph ic follow -up review of surgically t reated an eur ysm s. J Neuro- 37. Stefan i MA, Sch n eider FL, Marron e AC, Severin o AG, Jackow ski AP, Wallace
surg 1999;91:396–401 MC. An atom ic variat ion s of an terior cerebral arter y cor t ical bran ch es. Clin
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in 280 pat ien t s w ith ru pt u red dist al an terior cerebral ar ter y an eur ysm s. t u res an d n at u ral h istor y. J Neu rol Neu rosu rg Psych iat r y 1973;36:127–
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40. Parkin son D, West M. Traum at ic in t racran ial an eur ysm s. J Neurosurg 45. Asari S, Nakam ura S, Yam ada O, Beck H, Sugat an i H. Traum at ic an eur ysm
1980;52:11–20 of periph eral cerebral ar teries. Repor t of t w o cases. J Neurosurg 1977;46:
41. Sim SY, Sh in YS, Yoon SH. En dovascu lar in tern al t rapping of t raum at ic 795–803
pericallosal p seu doan eu r ysm w ith hydrogel-coated self-exp an dable coil 46. Buckingh am MJ, Cron e KR, Ball WS, Tom sick TA, Berger TS, Tew JM Jr.
in a ch ild: a case report . Surg Neurol 2008;69:418–422, discussion 422 Trau m at ic in t racran ial an eu r ysm s in ch ildh ood : t w o cases an d a review of
42. Kieck CF, de Villiers JC. Vascu lar lesion s due to t ranscranial st ab w oun ds. th e literat u re. Neu rosu rger y 1988;22:398–408
J Neu rosu rg 1984;60:42–46 47. Larson PS, Reisn er A, Morassu t t i DJ, Abdulh adi B, Harpring JE. Traum at ic
43. Coh en JE, Rajz G, It sh ayek E, Sh osh an Y, Um an sky F, Gom ori JM. Endovas- in t racran ial an eur ysm s. Neu rosurg Focus 2000;8:e4
cular m anagem en t of t raum at ic an d iat rogen ic aneu r ysm s of th e perical- 48. Lem per t TE, Halbach VV, Higashida RT, et al. En dovascular t reat m ent of
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44. Ven t ureyra EC, Higgin s MJ. Traum at ic in t racran ial an eur ysm s in ch ild- roradiol 1998;19:907–911
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Ner v Syst 1994;10:361–379

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54 Surgical Therapies for Basilar
Artery Aneurysms
Ali F. Krisht

of basilar an eur ysm s sh ould be t reated to avoid th e risk of th eir


■ History rupt ure.
Th e first m icrosu rgical clip ping of a saccu lar basilar ar ter y an eu -
r ysm w as perform ed by Olivecron a in 1954.1 He u sed th e su b -
tem poral approach to clip an an teriorly project ing an eur ysm of
th e basilar ar ter y. Th e pat ien t recovered w ell en ough to w ork ■ Surgical Approaches
part-t im e. In th e early 1960s, Ch arles Drake 2 rep or ted on h is ex-
Drake u sed th e su btem poral approach in h is first case an d in th e
perien ce w ith fou r cases of ru pt u red basilar arter y an eu r ysm s.
m ajorit y of h is cases. In h is vertebrobasilar an eur ysm book, h e
Even th ough th e ou tcom e of th ese p at ien t s w as n ot en cou raging,
st ates, “It h ad been an t icip ated th at th e fron totem poral exp osu re
his subsequent publication, titled “Surgical Treatm ent of Ruptured
w ou ld p rovide th e best view of th e u p p er basilar, as seen after
An eu r ysm s of t h e Basilar Ar ter y: Exp er ien ce w it h 14 Cases,”3
rem oval of a sup rasellar t u m or, but in th e n orm al brain it seem ed
follow ed by h is 1968 publicat ion , “Fur th er Experien ce w ith Sur-
too n ar row beside t h e carot id even w h en t h e sylvian fissu re
gical Treat m en t of An eu r ysm of th e Basilar Ar ter y,”4 in dicates h is
w as split .”1 He fu r th er st ates, “In th e p ost m ortem room th e su b -
in -depth u n d erst an ding of th e reason s for failu res in th e in it ial
tem poral route seem ed m ost direct an d th e ten torium cou ld be
cases. Th ese rep or t s also h igh ligh t h is belief th at by fu r th er u n -
divided if n ecessar y.” Th is seem s to t race back to th e m om en t
derstan ding both th e n orm al an d th e p ath ological an atom y of
w h en Drake star ted favoring th e su btem poral approach . In h is
th is disease en t it y, bet ter ou tcom es cou ld be ach ieved. In terest-
later pu blicat ion s, recogn izing th at som e an eu r ysm s of th e basi-
ingly, Drake’s first basilar ar ter y an eu r ysm w as a basilar t r u n k
lar apex region were very high in location and that trying to reach
an eur ysm . During th e sam e period of t im e, K.G. Jam ieson 5 from
th ose an eu r ysm s u sing th e su btem p oral ap proach w as inju riou s
Au st ralia rep or ted h is exp erien ce w ith 19 cases of ver tebrobasi-
to th e tem poral lobe, h e con cluded th at som e an eur ysm s are
lar an eu r ysm s in 1964, follow ed by rep ort ing on seven oth er an -
best ser ved w ith th e pterion al approach .1
eu r ysm s in 1967 in th e Journal of Neurosurgery. Alth ough bot h
Th e in t rodu ct ion of th e m icroscop e by Yaşargil revolu t ion ized
su rgeon s are credited for th eir p ion eering at tem pts at t reat ing
n eu rosurger y. Ut ilizing th e w ide t ran ssylvian approach , coupled
t h ose ch allen gin g cases, Drake an d Yaşargil are cred ited w it h
w ith th e m icroscope, gave th e pterion al approach an advan t age
m aking basilar an eu r ysm s a t reat able surgical en t it y w ith good
th at m ade it m ore popu lar for an eur ysm surger y.9–11 Yaşargil’s
outcom es in th e m ajorit y of cases.1–4,6–11
m icrosu rgical tech n iqu es, w h ich w ere based on a th orough u n -
derstan ding of th e m icroan atom y of th e basal cistern s an d th e
Pathophysiology and Natural History of m icrovascular anatom y of the region of the interpeduncular fossa,
led to excellen t ou tcom es in th e m ajorit y of an eu r ysm s an d in
the Disease basilar ar ter y an eur ysm s in par t icular. St ill, both Drake an d Yaş
Factors p redisp osing to form at ion of basilar an eu r ysm s are n o argil recogn ized th e lim it at ion s of th eir favored approach es in a
differen t from th ose related to oth er an eu r ysm s in gen eral. Basi- good n u m ber of an eur ysm s. Th is led to m ore pion eering w ork
lar an eu r ysm s are m ore com m on in w om en . Pat ien t s w ith th ese u sing approach es th at u t ilized th e sku ll base rou te for bet ter ex-
aneurysm s m ost com m only present in the fifth and sixth decades posu re, both on th e su rface an d at th e d epth of th e su rgical field.
of life. Th ey can presen t w ith subarach n oid h em orrh age or a h is- Dolen c15 an d h is pion eering w ork on th e cavern ous sin us open ed
tor y of h eadach es, or th e an eu r ysm can be fou n d in ciden tally. a n ew road to th e basilar apex region . Several pion eers, in cluding
Occasion ally, in cases of ver y large or gian t an eu r ysm s, pat ien t s Spet zler, d e Oliveira, Al-Meft y, an d oth ers,16–40 fu rth er described
presen t w ith sym ptom s of m ass effect , in clu ding gait an d bal- the advantages gain ed by ut ilizing skull base approach es to bet ter
an ce problem s an d possible w eakn ess due to com pression of th e exp ose th e region of th e in terp edu n cu lar fossa, an d im p rove on
cerebral p ed un cles. Th ey rarely presen t w ith a th ird n er ve p alsy. the safet y of dealing w ith different disease ent ities in th is region.
Several n at u ral h istor y st u d ies in d icate t h at basilar ap ex an - Based on the evolution of these different approaches, and w ith
eu r ysm s are m ore p ron e to bleed t h an an eu r ysm s located in th e in creasing u n derst an ding of th e path ological an atom y of dif-
oth er sites. Th e rupt ure rate in creases w ith th e in crease in th eir feren t t ypes of an eu r ysm s involving th e basilar apex region , th is
size. Th e In tern at ion al St u dy of Un r u pt u red In t racran ial An eu - ch apter describes m y experien ce w ith basilar apex an eu r ysm s,
r ysm s (ISUIA) reported th e ru pt ure rate of basilar an eur ysm s to an d focuses on h ow to safely and successfully treat the m ore com -
be up to 13.8% per year (p < 0.001).12 Oth er st u dies suggest sim i- plex an eur ysm s th at are n ot su ited for, an d are likely to fail, en do-
lar h igh an n u al bleeding rates.13,14 For th is reason , th e m ajorit y vascu lar th erapy.22–25

623

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624 V Cerebral and Spinal Aneurysms

to th e posterior clin oid process. In h alf of th e pat ien ts th e basilar


■ Anatomy of the Basilar Apex bifurcat ion is at th e level of th e dorsu m sellae an d th e posterior
Th e safet y of m icrosu rgical t reat m en t of basilar ap ex an eu r ysm s clin oid p rocess. In an oth er th ird of p at ien t s it is h igh er th an th e
dep en ds on an u n derst an ding of th e m icrosu rgical an atom y of posterior clin oid processes, an d in th e rest it is below th e d orsu m
n ot on ly th e n orm al vasculat u re in th e in terpedun cu lar fossa, sellae. Th e locat ion of th e bifu rcat ion in flu en ces th e cou rse of
but also th e w ay th e an atom y is ch anged in th e state of disease. th e posterior cerebral ar ter y. Th is is due to th e con stan t locat ion
It is ver y im por t an t for th e n eu rosurgeon t reat ing basilar apex of th e ocu lom otor n er ve above w h ich th e P1 segm en t n eeds to
an eur ysm s to un derstan d th e relat ion sh ip bet w een th e differen t pass, before it contin ues in to the perim esencephalic cistern. These
n eu rovascular st ruct ures an d th eir n orm al variat ion s. Th e region variat ion s m ay in fluen ce th e course of th e perforator bran ch es
of th e in terpedu n cular fossa is crow ded w ith several perforator arising from th e P1 segm en t , an d h ow th ey relate to th e dom e of
system s th at t raverse th e sp ace in fron t of an d beh in d th e basilar th e an eu r ysm . For exam p le, in p at ien t s w ith a h igh bifu rcat ion
apex region . Th ese in clude th e th alam operforators from th e pos- (above th e posterior clin oid), th e P1 perforators course dow n -
terior com m un icat ing ar ter y, bran ch es of th e an terior ch oroidal w ard aw ay from th e superiorly project ing an eur ysm dom e. On
ar ter y, th e P1 p erforators, in addit ion to th e p erforators arising th e oth er h an d, in an eu r ysm s arising from a low -lying bifu rca-
from t h e su p er ior cerebellar ar ter y. Th ese p er forators are con - t ion , th e p erforators ten d to h ave m ore p roxim it y to th e an eu -
sidered en d ar teries, th e injur y of w h ich w ill lead to brain stem r ysm dom e because of th e V-sh ap ed bifu rcat ion resu lt ing from
an d th alam ic st rokes. For th is reason ever y effor t sh ould be m ade th e u pw ard cou rse of th e p oster ior cerebral ar ter y. Poster iorly
to save each an d ever y on e of th e basilar apex perforators, an d p roject in g an eu r ysm s are even m ore ch allen ging becau se t h e
u n der n o circu m st an ces sh ould th e t reat ing n eu rosu rgeon feel dom e an d th e n eck region of th e an eu r ysm s are bu ried in th e
th at a cer tain perforator is sm all an d n ot im p or tan t . It sh ould be in terpedu n cu lar fossa, beh in d th e t akeoff poin t s of t h e perfora-
st ressed th at it is in excu sable to be perm issive abou t sacrificing tors. In such cases, th e perforators of th e superior cerebellar ar-
any of th e perforators. ter y are draped over th e posterior aspect of th e n eck an d dom e
Th e basilar ap ex bifu rcat ion varies in it s locat ion as it relates region of th e an eu r ysm , as described below.

a b c

Fig. 54.1a–d (a) Sagit tal computed tom ography angiography (CTA) im age of an anteriorly project-
ing basilar apex aneurysm . (b) An illustration of a surgical view of an anterior projecting basilar apex
aneurysm at the normal level of a bifurcation as it relates to the anterior clinoid process. (c) An ante-
rior projecting aneurysm arising from a high bifurcation. (d) An anterior projecting aneurysm arising
d
from a low bifurcation.

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54 Surgical Therapies for Basilar Artery Aneurysms 625

Pathological Anatomy and Aneurysm Projection of t h e basilar t r u n k becom es m ore ch allenging. In t h ese cases,
u t ilizing th e t ran scavern ous app roach , as w ill be discu ssed later,
Th ere are several variat ion s of basilar ap ex an eu r ysm s in flu - in creases th e safet y of th e clip ping p rocess.
en ced by t h e locat ion of th e an eu r ysm , th e size of th e an eu r ysm ,
an d th e project ion of th e an eur ysm dom e. For th e purpose of
Superior Projecting Aneurysms
clarit y, w e w ill focu s on th e variat ion s of th e an atom y based on
th e an terior, su p erior, an d p osterior project ion s of th e an eu r ysm Su perior project ing an d sm all an eu r ysm s are th e m ost favorable
dom e. an eur ysm s, especially if th e bifurcat ion is n ot at too h igh a loca-
t ion (Fig. 54.2). In ver y h igh superiorly project ing basilar bifur-
cat ion an eu r ysm s, th e an eu r ysm cou ld be bu ried in to th e floor
Anterior Projecting Aneurysms
of th e th ird ven t ricle, n arrow ing th e space available for applying
An terior project ing an eur ysm s are relat ively less com plex to clip th e clip s at th e n eck region . In su ch cases, th e app licat ion of tem -
if th ey are sm all in size an d u n ru pt ured (Fig. 54.1). W h en th ey porar y clips in creases th e safet y of th e procedu re in th e even t of
are m ediu m -sized or large, an d th ey h ave r upt ured, th ey becom e a rupt ure. Th e perforators are n ot located in proxim it y to th e
m ore com plex because any m an ipulat ion of th e region of th e n eck, alth ough th ey m ay loop up tow ard th e posterior aspect of
dom e, w h ich is u su ally project ing tow ard th e p osterior clin oid th e n eck, an d t h u s care sh ou ld be t aken to avoid in clu ding th em
p rocess, can resu lt in a p rem at u re re-r u pt u re. In th ose cases, it in th e clips. Also in su ch circum st an ces, th e visualizat ion of th e
is of th e ut m ost im por tan ce to ach ieve proxim al con t rol by good opposite P1 segm en t perforators m ay be h in dered by th e ver y
visu alizat ion of th e basilar t r u n k before at tem pt ing to clip th e high location of the bifurcation. Before concluding the procedure,
an eu r ysm . In such cases, an d if th e level of th e bifurcat ion is sig- ever y effor t sh ou ld be m ade to visualize all th e perforators in a
n ifican t ly below t h e p oster ior clin oid p rocess, t h e visu alizat ion 360-degree fash ion arou n d th e an eur ysm base.

a b c

Fig . 54.2a–d (a) A sagit tal com puted tom ography angiography (CTA) im age of a superiorly pro -
jecting aneurysm . (b) An illustration of a surgical view of a superior projecting aneurysm at a regu-
lar location. (c) A superior projecting aneurysm arising from a high bifurcation as it relates to the
anterior clinoid process. (d) A superior projecting aneurysm arising from the bifurcation, which is
low in relationship to the anterior clinoid process. d

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626 V Cerebral and Spinal Aneurysms

a b

Fig. 54.3a,b (a) A sagit tal computed tomography angiography (CTA) im age of a posterior projecting aneurysm . (b) Illustration of a surgical view of a
posterior projecting aneurysm .

Posterior Projecting Aneurysms w ith out leaving a residual u n derbelly on th e posterior aspect .
Posterior project ing an eur ysm s becom e m ore com plex if th e bi-
Posterior project ing an eu r ysm s are th e m ost com plex cases (Fig.
furcat ion is h igh an d th e sac is large.
54.3). Th e P1 segm en t perforators are usually draped over th e
an ter ior asp ect of t h e base, w h ich m ay h in d er t h e clip ap p li-
cat ion process sign ifican tly. In ou r experien ce such an eu r ysm s
h ave a h igh er ch an ce of adh esion s bet w een th e perforators an d ■ Surgical Technique
th e an eu r ysm dom e. In addit ion , th e p erforators arising from th e
su p erior cerebellar ar teries m ay drap e over th e p osterior aspect
Craniotomy
of th e dom e an d m ay also be in cluded in th e posterior blade of Th e cran iotom y u sed is a fron totem p oral on e, w h ich is m ore like
th e clip s. Th ere are several t ricks th at w e u se at ou r cen ter to be a m odified pterion al approach w ith m ore tem poral exten sion
able to safely clip t h e an eu r ysm an d p reser ve t h e p er forators (Fig. 54.4). To gain access to th e pretem poral region , th e zygo-

a b

Fig. 54.4a,b (a) The extent of the exposure of the craniotomy. The exposure of the temporal side of the frontotemporal flap is enhanced by trimm ing
of the zygom atic notch, which enables a m ore inferior reflection of the temporalis m uscle. (b) The bur hole location and the craniotomy line.

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54 Surgical Therapies for Basilar Artery Aneurysms 627

Fig. 54.5 The extradural exposure after rem oval of the posterior third of
the orbital roof. Note the significant pretemporal exposure with m inim al
retraction. The dashed black lines illustrate the dural opening when the
transcavernous approach is needed. The solid black line delineates the syl-
vian fissure.

m at ic n otch is drilled to en able a m ore in ferior reflect ion of th e


tem poralis m uscle. After th e bon e flap is raised, epidu ral h em o-
st asis is est ablish ed w ith t ack-u p st itch es. Using th e m icroscope,
th e sp h en oid w ing is drilled flat w ith t h e roof of th e orbit . Th e
posterior th ird of th e roof an d lateral w all of th e orbit al con e is
rem oved eith er w ith a h igh -speed diam on d drill or bony ron -
geu rs (Fig. 54.5). Th e rem oval of th e bon e is exten ded m edially
to th e level of an terior clin oid p rocess.

Removal of the Anterior Clinoid Process and b


Exposure for the Transcavernous Route Fig. 54.6a,b (a) The surgical view of the epidural dissection of the lateral
cavernous sinus. (b) The extradural pretemporal exposure illustrating the
To facilitate th e rem oval of th e an terior clin oid process, an d to
different components of the lateral wall of the cavernous sinus, including
bet ter expose it , th e pretem poral dural dissect ion is m ade at th is the orbit (O); optic nerve (ON); ocular motor nerve (III); trochlear nerve
st age. Th is is started at th e level of th e m en ingo-orbital ar ter y, (IV); the V1, V2, and V3 branches of the trigem inal nerve; internal carotid
w h ich is coagulated an d cut (Fig. 54.5). Next , th e du ra propria of artery (ICA); Meckel’s cave (MC); gasserian ganglion (GG); frontal dura (FD);
th e tem p oral lobe is separated from th e lateral w all of th e cav- temporal dura (TD); and the superior orbital fissure (SOF). The black arrow
points to the site of injection of fibrin glue for hem ostasis of the cavernous
ern ou s sin u s. Th is is st ar ted at th e level of th e su perior orbit al
sinus.
fissure an d exten ds laterally an d posteriorly over th e differen t
bran ch es of th e t rigem in al n er ve.
W h en th e t ran scavern ou s app roach is th e p lan n ed exp osu re, sph en oid w ing, sh ould h ave already been rem oved. Th e rem ain -
th e dissect ion is con t in u ed p osteriorly to th e level of th e gasse- ing t w o at t ach m en t s, on e of w h ich is to th e roof of th e opt ic
rian ganglion an d Meckel’s cave. To m ake th is dissect ion easier, can al an d th e oth er is to th e floor of th e opt ic can al along its ex-
th e m iddle m en ingeal ar ter y is coagu lated an d cu t from it s root ten sion as th e opt ic st ru t , rem ain in p lace. Both at t ach m en ts are
at th e level of th e foram en sp in osu m . Hem ostasis w ith in th e cav- drilled w ith a h igh -sp eed diam on d drill w ith frequ en t in term it-
ern ou s sin u s is est ablish ed at th is st age. Th is is don e by inject ing ten t stops an d copious irrigat ion . Th is is to preven t gen erat ing
1 cc of fibrin glue (Tisseel, Baxter, West Lake Village, CA) in th e any excessive h eat th at m ay affect or injure th e opt ic n er ve. On ce
direct ion of th e cavern ou s sin u s p rop er bet w een th e V1 an d V2 th ese at t ach m en t s are drilled, th e t ip of th e an terior clin oid pro-
bran ch es of th e t rigem in al n er ve (Fig. 54.6). After th is st age of cess becom es m obile an d easy to rem ove from its dural bed. Care
th e ep idu ral dissect ion , th e an terior clin oid p rocess is rem oved. is t aken to d issect gen t ly arou n d t h e clin oidal segm en t of t h e
Th e an terior clin oid p rocess h as th ree m ain at t ach m en t s from carot id ar ter y. It is im por tan t to be cogn izan t of th e exten sion of
th e su rgical poin t of view (Fig. 54.7). Th e first at t ach m en t , w h ich th e clin oid at t ach m en t to th e opt ic st ru t an d th e sph en oid sin u s
is th e con t in u at ion of th e clin oid w ith th e orbit al roof an d th e at th e level of th e opt icocarot id angle. Occasion ally, th e clin oid

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628 V Cerebral and Spinal Aneurysms

Fig. 54.7 The three surgical at tachm ents of the anterior clinoid process,
including the sphenoid wing (gray shade), optic roof (orange shade), and the a
optic strut (yellow shade).

process it self is p n eu m at ized, an d rem oving th e clin oid t ip leads


to th e sph en oid sin us. In th ese cases, it is essen t ial to obliterate
th is w in dow in to th e sph en oid sin u s du ring th e closu re. We u su -
ally apply a sm all piece of th e tem poralis m uscle in to th e open -
ing of th e sph en oid sin us before com plet ion of d ural closu re.

The Dural Opening


Th e du ra is open ed in a cu r ved H-sh ap ed fash ion (Fig. 54.5). Th e
h orizon t al arm of th e H exten ds along th e in den tat ion of th e
sph en oid ridge bet w een th e fron t al an d tem poral lobes. Th is is
exten d ed all th e w ay to t h e level of th e ocu lom otor t rigon . Op en -
ing th e basal cistern s an d releasing spin al flu id en ables brain re-
la xat ion an d visu alizat ion of th e in t rad u ral cou rse of th e ocu lo-
m otor n er ve (Fig. 54.8a). Th e p reviou s d issect ion of th e lateral
w all of th e cavern ou s sin u s h as already exp osed th e ext radu ral
com p on en t of th e ocu lom otor n er ve. At th is st age, an d u n d er th e
m icroscope, both th e in t ra- an d ext radural port ion s of th e oculo-
m otor n er ve are visu alized . Usin g a sh ar p m icrokn ife, t h e d u ra b
is th en cut to fur th er open th e oculom otor can al from it s in t ra- Fig. 54.8a,b (a) The dissection and m obilization of the intracavernous
d u ral exten sion all t h e w ay to th e level of t h e su p er ior orbit al portion of the oculom otor nerve. (b) The extent of the exposure achieved
fissu re. A t r ian gu lar p iece of d u ra t h at exten d s from t h e opt ic before dissecting the interpeduncular fossa structures.
can al to th e level of th e ocu lom otor n er ve is th en rem oved an d
sh aved from its at tach m en t to th e carot id du ral ring.
along th e in ferior surface of th e tem poral lobe an d along its lat-
Intradural Dissection and Exposure of eral exten sion . Th is en ables leaving th e tem poral du ra w ith th e
at tach ed tem p orop olar vein s on th e su rface of th e tem poral lobe
the Aneurysm
an d un der th e applied spat ula. Gen tle lift ing an d ret ract ion of
On ce epidural h em ost asis is establish ed an d th e dura is open ed, th e tem p oral lobe in a p osterior an d lateral direct ion p rovides
t h e sylvian fissu re is w id ely op en ed from in sid e to ou t sid e, as st raigh t access from th e p retem p oral sp ace to t h e in terpedu n cu -
described by Yaşargil.11 Follow ing th is step , a self-ret ain ing brain lar fossa (Fig. 54.8b). Th e arach n oid along th e skull base, in clud-
spat ula is gen tly applied over th e con tour of th e tem poral lobe. ing Liliequ ist’s m em bran e, is dissected an d cu t . Th is leads to th e
We usually preser ve the attachm ent of the tem poropolar veins to exp osu re of th e root of th e ocu lom otor n er ve to t h e level of it s
th e tem p oral du ra. Fu r th er cu t t ing of th e tem poral du ra is d on e at tach m en t at th e brain stem . At th is stage th e level of th e basilar

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54 Surgical Therapies for Basilar Artery Aneurysms 629

bifurcat ion relat ive to th e posterior clin oid process is assessed. If perforator-free zon e below th e takeoff of th e su p erior cerebellar
th e bifu rcat ion is low, th e posterior clin oid process is rem oved to ar ter y, to w h ich th e tem porar y clips are app lied. Th e goal is to
provide bet ter exposu re of th e bifu rcat ion as w ell as th e basilar ach ieve proxim al con t rol but to con t in ue to allow a sm all am oun t
t run k for th e early applicat ion of th e tem p orar y clips. of collateral flow th rough th e superior cerebellar ar ter y system .
To rem ove th e posterior clin oid process, th e pet roclival dura Th is w ill d ecrease t h e am ou n t of flow w it h in t h e an eu r ysm ,
h as to be cut . Th is leads to th e posterom edial com par t m en t of soften t h e an eu r ysm , an d m akes it m ore com p ressible d u r ing
th e cavern ou s sin u s. In m ost cases, th e previou s inject ion of fi- t h e in it ial app licat ion of a perm an en t clip to th e n eck region (Fig.
brin glue fills th is com par t m en t w ith glue an d provides adequate 54.10). At th e sam e t im e, it m ain tain s a sm all am oun t of blood
h em ostasis. Occasion ally, m ore glue n eeds to be injected before flow in th e perforators, w h ich w ill im prove th e safet y of th e tem -
rem oval of th e dura an d exposu re of th e p osterior clin oid bon e porar y occlusion sh ould it be m ore p rolonged th an expected.
(Fig. 54.9a). Before rem oving th e clin oid process, it is im por t an t
to dissect th e oculom otor n er ve from all its at tach m en t s along
th e ocu lom otor can al. Th is facilit ates m obilizat ion of th e ocu lo-
Cutting of the Posterior Communicating Artery
m otor n er ve back an d forth from a m edial to a lateral posit ion , Th e adequ ate exposu re of th e posterior aspect of th e an eu r ysm ,
preven t s it from su stain ing a p erm an en t injur y, an d provides ad- to visu alize th e perforators arising from th e P1 segm en t of th e
equ ate exp osu re of th e differen t corn ers of th e posterior clin oid posterior cerebral ar ter y, m ay be en h an ced by resect ion of th e
process. We u sed to drill th e an terior clin oid p rocess w ith a 1- or posterior com m un icat ing ar ter y, w h ich can be don e if it is coag-
2-m m h igh -speed diam on d drill. Th is is don e w ith frequen t in - u lated an d cu t at th e perforator-free zon e (Fig. 54.11). Th is is
term it ten t stops an d copious irrigat ion . More recen tly w e h ave u su ally located at th e jun ct ion of th e posterior com m un icat ing
been u sing an ult rason ic aspirator (Om n i, St r yker Corp., Kalam a- ar ter y w ith th e posterior cerebral ar ter y. Th is step is im por tan t
zoo, MI), w h ich avoids th e n eed for th e drilling (Fig. 54.9b). On ce in posteriorly project ing an eu r ysm s an d to en large th e surgical
t h e p oster ior clin oid p rocess is rem oved , t h e level an d p osit ion field at it s d ept h in p at ien t s in w h om t h e p oster ior com m u n i-
of t h e basilar t r u n k are assessed (Fig. 54.9c). Th e p oster ior as- cat in g ar ter y is sh or t an d act s as a ten sion ban d by br in gin g
pect of th e t ru n k is carefu lly dissected to establish an adequ ate toget h er t h e p oster ior cerebral ar ter y an d t h e in ter n al carot id

Fig. 54.9a–c (a) The site of possible need of further injection of fibrin
glue into the posterior aspect of the cavernous sinus just anterior to the
petroclival dural fold. (b) The steps of the rem oval of the posterior clinoid
process (PCP). Note the significant space established by dissecting the third
nerve (III) along its intracavernous course. The bony rem oval of the poste-
rior clinoid is being perform ed using the Sonopet (Stryker, Kalamazoo, MI).
(c) The extent of exposure of the basilar trunk after rem oval of the poste-
rior clinoid process. Note the significant widening of the working space at
the depth of the surgical field.

b c

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630 V Cerebral and Spinal Aneurysms

Fig. 54.10 Illustration of the surgical view indicating the location of the
temporary clip at the perforator-free zone on the basilar trunk below the Fig. 54.11 Intraoperative view showing the step of cut ting the posterior
takeoff of the superior cerebellar arteries. Placing the clip at the perforator- com m unicating artery at the perforator free zone at the junction of the
free zone below the superior cerebellar arteries enables blood to perfuse posterior cerebral artery. Note the poor visualization of the interpeduncular
the perforators both above and below the temporary clip while the location fossa, which will become m ore enhanced as shown in Fig. 54.12.
of the temporary clip does not compromise the view of the region of the
aneurysm and the interpeduncular fossa.

ar ter y. Coagu lat ing an d resect ing th e posterior com m u n icat ing
ar ter y in su ch cases en larges th e field by det ach ing an d m obiliz-
ing th e intern al carot id ar ter y an teriorly. We h ave ut ilized th is
step in m ore t h an 35 p at ien t s w ith n o sign ifican t sequ elae. Th is
step is d on e w h en n ecessar y an d on ly if th e P1 segm en t is larger
in diam eter th an th e posterior com m u n icat ing arter y.

Clipping Process
On ce adequate exposure is ach ieved a tem porar y clip is applied
to th e basilar t r un k at a perforator-free zon e. Th e m icroscope is
th en m obilized to visu alize th e an eu r ysm n eck region . Th e an eu -
r ysm is n ow softer an d m ore com pressible. Th e con t ralateral P1
segm en t of t h e left p oster ior cerebral ar ter y is visu alized an d
assessed, as are any perforators arising from th is segm en t (Fig.
54.12). Th e an eur ysm is th en dissected on it s posterior aspect to
provide bet ter visu alize of th e perforators th at m ay be located
along t h e n eck region of t h e an eu r ysm or som et im es at t ach ed
to th e dom e of th e an eur ysm . Th is explorat ion is don e for a 1- to
2-m in ute period, after w h ich th e tem porar y clips are rem oved. It
can be repeated several t im es to gain as m u ch in form at ion abou t
th e locat ion of th e p erforators an d to bu ild a th ree-dim en sion al
im age in th e n eu rosu rgeon’s m in d of th e an atom y of th e an eu-
r ysm an d t h e su r rou n d in g p erforators. Th is exp lorat ion also Fig. 54.12 The wide surgical view achieved by cut ting the posterior com -
h eigh ten s th e level of con cen t rat ion of th e surgical team , in clud- m unicating artery at tachm ent to the posterior cerebral artery. Note the
presence of t wo temporary clips—one on the basilar trunk and another one
ing th e scrub n u rse an d th e an est h esiologist . On ce th e pict ure
on the contralateral P1 segment. Temporary clip placement led to soften-
becom es clear, th en th e tem porar y clips are applied to th e basi- ing of the aneurysm , enabling it to be m obilized for bet ter clipping. Note
lar t ru n k, after w h ich th e first p ilot clip is app lied to th e n eck of that there is still blood perfusing the perforators, as shown, usually from
th e an eu r ysm . Th e clip blades are im m ediately exp lored to verify collaterals com ing from the superior cerebellar artery.

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54 Surgical Therapies for Basilar Artery Aneurysms 631

th eir adequ ate locat ion before th e tem p orar y clip is rem oved.
Th is m ay en t ail an at tem pt at p u n ct u r in g an d sh r in kin g t h e an -
eu r ysm , or som et im es fu r t h er ap p licat ion of a clip to t h e con -
t ralateral P1 segm en t of t h e p oster ior cerebral ar ter y, on ce it
becom es bet ter visualized, an d to furth er deflate th e an eur ysm
and reposition the clip as needed. During this process, the som ato-
sensor y evoked potent ials, electroen cephalogram , and brain stem
evoked responses are con tin uously m onitored. Any changes found
on elect rophysiological m on itoring m ay dictate a ch ange in plan ,
especially if th e ch ange is associated w ith t h e p osit ion ing of th e
clips on th e vessel.
Th e tem porar y clip s are rem oved an d fu r t h er assessm en t is
don e to en su re th e adequ ate clip ping of th e n eck region w ith ou t
in clu sion of perforators in th e clip con st ru ct . Adjust m en ts are
m ad e accord in gly. In t h e m ajor it y of p at ien t s, w e favor coagu -
lat in g t h e an eu r ysm , w h ich h elp s sh r in k t h e an eu r ysm sac sig-
n ifican t ly an d at t h e sam e t im e seals any r u pt u re site. Th is step
h elp s conver t an acu te r u pt u re sit u at ion , p rovid in g a m ore re-
la xed at m osp h ere to bet ter visu alize t h e su r rou n d ing an atom y
of t h is region .
Th e m ain advan t age of t h e t ran scavern ou s ap proach is th at all
t h e above-m en t ion ed m an eu vers can be p er for m ed w it h fu ll
visu alizat ion of th e an atom y in th e in terp edu n cu lar fossa. Th e
tem porar y clip applied to th e basilar t run k is n ever in th e w ay Fig. 54.13 The final view after the clipping. Notice the significantly wid-
w h en w orking on th e basilar n eck region . If t w o sm all clips are ened exposure at the depth of the surgical field with the abilit y to fully
applied to th e posterior cerebral ar teries, th ey con t in ue to be ou t visualize the region of the neck of the aneurysm circum ferentially.
of th e w ay, too.
If th e an eur ysm rupt ures w ith th e tem porar y clips already
applied, th e use of th e suct ion can keep th e surgical field clear.
Occasion ally, in t raop erat ive r u pt u re m ay n eed im m ediate appli-
cat ion of an oth er clip to th e con t ralateral P1 segm en t . Th is is
w hy w e en sure, in th e m ajorit y of pat ien ts, adequate rem oval of
■ Discussion
th e p osterior clin oid process to gain access to th e con t ralateral Th e m icrosu rgical t reat m en t of basilar an eu r ysm s is cu rren tly
P1 segm en t before at t acking th e an eu r ysm . If con t in u ou s oozing lim ited to a few h igh -volu m e vascu lar cen ters. Th is t ren d con t in -
occurs before th e bleeding is con t rolled, it is im por tan t n ot to u es to be st ren gt h en ed in sp ite of evid en ce t h at en d ovascu lar
pan ic an d to con t in u e to visu alize all th e an atom y before any fu r- t h erapy is n ot d u rable in a good n u m ber of p at ien t s.41–52 Th e
th er step s are t aken . It is also good to keep in m in d th at if th e an eur ysm s th at are best su ited for en dovascu lar coiling are sm all
an eur ysm is bleeding it m ean s th e brain is adequately being per- in size an d h ave a sm all n eck. How ever, th ese are th e sam e aneu-
fused w ith blood, w h ich also m ean s th at th e p rolongat ion of th e r ysm s th at h ave a low m orbidit y an d good durabilit y if t reated
tem porar y occlusion process does n ot en tail a h igh risk of cau s- w ith m icrosurgical clipping. Large an eur ysm s w ith w ide necks
ing isch em ia to th e brain . Th e m ost com m on cau se of injur y is a h ave a h igh er rate of recan alizat ion an d th e n eed for furth er
h ast y clipping applicat ion as a react ion to th e bleeding, w ith ou t th erapy w h en t reated w ith th e en dovascu lar opt ion . Th e recan a-
proper visu alizat ion of w h ere th e clip s are going. lizat ion rate of an eu r ysm s t reated w ith en dovascu lar coiling, in
Alth ough m any su rgeon s advocate th e u se of cerebral protec- gen eral, is 20 to 30%. About 15 to 20%of all coiled an eur ysm s w ill
tion agen ts, w e depend on the neurophysiological m on itoring for n eed fu r th er fu t u re t reat m en t . Th is rate of recan alizat ion in -
guidan ce. We do n ot use cerebral protect ive agen ts because th ey creases to 40 to 60% in large an d gian t an eur ysm s.
provide a false sen se of secu rit y th at th e brain is protected. We Basilar aneurysm s especially are m ore pron e to recanalization
w ould rather depend on efficien t an d safe steps in the clip applica- an d regrow th after en dovascular coiling.52 Th is is th ough t to be
t ion p rocess. It is im p or tan t to bu ild ou r p lan on th e assum pt ion du e to th e locat ion of th ese an eu r ysm s at th e basilar bifu rcat ion
of ign oran ce abou t th e exten t of collateral flow, an d th us exer- an d in th e direct ion of th e blood flow. Th eir recan alizat ion usu-
cise m ore cau t ion , th an on th e false assu m pt ion of kn ow ledge. ally com es back in t h e for m of com p act ion . In ad d it ion , recen t
In th e overall m ajorit y of pat ien ts, on e tem porar y clip applied st u d ies in d icate t h at t h e an n u al rebleed ing rate in com p letely
to th e basilar t r un k is en ough to gain adequate h em odyn am ic coiled an eu r ysm s is 1.3% per year, an d in par t ially coiled an eu -
con t rol of th e blood flow ing to th e an eu r ysm . Occasion ally an d r ysm it is as h igh as 1.8%per year. Th ese facts lead to a sign ifican t
for a ver y sh or t period of t im e, t w o addit ion al clips are applied con cern regarding th e du rabilit y of coiling of su ch an eu r ysm s
to both P1 segm en ts to fur th er coagu late an d sh rin k th e an eu- an d th e am oun t of protect ion th ey provide from fut ure bleeding.
r ysm before th e fin al clip is applied (Fig. 54.13). Th is is don e for Kn ow ing th at th e an n u al bleeding rate of an u n ru pt u red an eu -
n o m ore th an 2 m in utes. In spite of th e th ree clips, th ere is st ill r ysm is bet w een 1 an d 2%, it m akes sen se to quest ion w h eth er
som e flow th at com es from th e su p erior cerebellar ar ter y col- coiling an u n ru pt u red an eu r ysm h as any valu e in term s of fu t u re
lateral system an d p erfu ses th e brain stem . protect ion from ru pt u re.

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632 V Cerebral and Spinal Aneurysms

Th e sh or tcom ings of en dovascu lar th erapy h ave led to th e u se of t h is ap p roach is t h e in creased m an eu verabilit y, w h ich d e-
of m ore com p licated en d ovascu lar p rocedu res, su ch as in ser t ion creases th e t im e n eed ed to ach ieve t h e step s of exp osu re an d
of a stent or dou ble sten ts, to ach ieve adequate obliterat ion of clip p in g. In creased m an eu verabilit y is ach ieved by (1) p lacin g
th e an eur ysm s.53 Th is sign ifican t in crease in th e com plexit y of tem porar y clips on th e perforator-free zon e below th e superior
th e en dovascu lar procedu res, th e ad dit ion of risks related to th e cerebellar arter y on the basilar trunk, thereby taking aw ay the clip
in ser t ion of sten t s, as w ell as com plicat ion s related to th e n eed of from th e an eu r ysm n eck region an d avoid ing any obst ru ct ion of
fu ll an t icoagu lat ion , lead to a sign ifican t in crease in m orbidit y of th e view in th at area; or (2) rem oving th e p osterior clin oid p ro-
su ch p rocedu res. With ou t a proven record of long-term du rabil- cess, w h en in dicated, w h ich provides im proved visualizat ion of
it y, th is scen ario raises th e qu est ion of th e w isdom of pursu ing th e con t ralateral P1 segm en t , alth ough it m ay be m ore difficu lt
su ch t reat m en t m odalit ies. In addit ion , cer t ain coiled an eu r ysm s in an teriorly project ing an eu r ysm s, w h ich can som et im es be at-
are in appropriate for fur th er coiling. Th e recurren ce of th ese an - tach ed to th e posterior aspect of th e clivus an d posterior clin oid
eu r ysm s p laces a sign ifican t em ot ion al bu rden on th e pat ien t s. process; in th ese cases, w e t r y to visu alize th e P1 segm en t from
Historically, en dovascu lar th erapy w as in t rod uced as a m ean s to a m ore posterior approach beh in d th e an eur ysm . Th e oth er ad-
overcom e th e sh or tcom ings of m icrosu rgical th erapy. At th is van t age of t h is ap p roach is in m ain t ain ing blood flow from t h e
st age, th e recen t advan ces in m icrosu rger y, esp ecially as th ey re- su p er ior cerebellar ar ter y collateral system to t h e p er forators.
late to th e im proved safet y of sku ll base ap p roach es, can be u t i- Th is im proves th e safet y of th e tem porar y occlu sion p rocess. Th e
lized as a m ean s to overcom e th e sh or tcom ings of en d ovascu lar w ide su rgical field at th e depth of th e in terpedun cular fossa en -
t h erapy, esp ecially w h en d ealin g w it h com p lex large an d gian t ables th e surgeon to m an euver th e an eur ysm , an d possibly re-
an eur ysm s. sect it , to recon st r u ct th e base of th e an eu r ysm . Th is is a m ajor
Th e classic su btem p oral an d pterion al ap p roach es w ere ver y advan t age over en dovascular coiling, w h ich leaves th e an eur ysm
u sefu l in t h e h an d s of t h e m asters w h o in t rod u ced t h ose ap - w ith a w ide n eck, resulting in a h igh er rate of recan alizat ion .
proach es for th e treat m en t of basilar an eu r ysm s. Drake an d Yaş
argil’s experien ce is clearly difficult to m atch . How ever, th ese
m asters in dicated th e lim itat ion s of th ese app roach es.
Th e su btem p oral app roach dem an ds a sign ifican t am ou n t of
ret ract ion on th e tem p oral lobe, w h ich can be h igh ly inju r iou s
■ Complications and Outcomes
in acu te su barach n oid h em or rh age cases. Also, w h en d ealin g Historically, th e com plicat ion rate of m icrosu rgical clipping of
w it h an eu r ysm s located below th e posterior clin oid process, th e basilar aneur ysm s has been higher than w ith other aneur ysm s lo-
su btem p oral ap p roach m akes it d ifficu lt to ap p ly p roxim al clip s cated in the an terior circulation. The best outcom es w ere ach ieved
from a su p erolateral to an in ferom ed ial p roject ion w it h ou t in h igh -volu m e cen ters w h ere surgeon s w ere accu stom ed to th e
com prom ising th e view of th e n eck of th e an eu r ysm . Th e ot h er in t ricacies of t reat m en t of posterior circulat ion an eu r ysm s.
disadvan t age of th e su btem poral ap proach is th e difficu lt y in vi- Over t im e, th e lack of experien ce in dealing w ith posterior
su alizing th e con tralateral P1 segm en t esp ecially w ith large an - circulat ion an eur ysm s h as led n eurosurgeon s to shy aw ay from
eu r ysm s. Drake exp ressed h opes th at in th e fu t u re an app roach t reat ing basilar an eu r ysm s w ith th e sam e in ten sit y as t reat ing
cou ld be design ed th at com bin ed th e advan t ages of both th e su b - anterior circulation aneur ysm s. Furtherm ore, the experience w ith
tem poral and th e pterion al approach to bet ter visualize the region advan ced tech n iqu es, su ch as bypass surger y, n ecessar y for th e
of the aneurysm and the interpeduncular fossa circum ferentially. t reat m en t of com p lex posterior circu lat ion an eu r ysm s, h as sig-
Th e pterion al ap p roach is at a disadvan t age in visu alizing th e nifican tly decreased.55 Th is tren d coincided w ith the int roduction
p oster ior asp ect of t h e an eu r ysm w h ere t h e p er forators are lo- of en dovascu lar th erapy, w h ich becam e a less involved an d rela-
cated . Also, t h e classic pter ion al ap p roach p rovid es a n ar row t ively safer altern at ive. How ever, en dovascu lar th erapy con t in -
w in dow to th e in terpedun cu lar fossa, w h ich lim its th e m an eu- u es to h ave th e problem of lack of durabilit y an d th e persisten ce
verabilit y for t h e clip app licat ion p rocess. Th e p osterior clin oid of th e risk of h em orrh age in a sign ifican t n um ber of pat ien ts.
p rocess can also be in t h e w ay, esp ecially in low -lying basilar Part ially t reated an eur ysm s an d th ose w ith a com pressive coil
bifu rcat ion s. Yaşargil, in h is w rit ings an d person al com m un ica- m ass p er t urbing th e brain stem presen t oth er un iqu e ch allenges.
t ion s, exp ressed th e n eed to en large th e su rgical w in d ow at it s In addit ion , th e com plex con figu rat ion of basilar an eu r ysm s an d
depth to bet ter ach ieve p roxim al con t rol of th e basilar t r u n k be- th eir w ide n eck an d large size n ecessit ates u sing a m ore com plex
fore at tacking th e an eu r ysm s. en d ovascu lar tech n ique, lead ing to a h igh er m orbidit y. Th ese
Th e t ran scavern ou s ap p roach part ially rem edies th e sh or t- problem s h ave led several experien ced n eu rosu rgeon s to revive
com ings of the previous approaches. This approach w as pioneered th e in terest in m icrosurgical t reat m en t of basilar an eu r ysm s. In
by Dolen c et al54 as a t ran scavern ous-t ran ssellar approach to th e our experien ce, an d th e experien ce of oth ers, w e w ere able to
basilar apex. Th ey repor ted on 11 rupt ured basilar an eur ysm s, ach ieve a m odified Ran kin scale (m RS) score of 0 to 2 at dis-
four of w h ich w ere large in size. Th ey cited th e n eed for m edial ch arge in m ore th an 85% of p at ien t s, w h ich in creases to m ore
ret ract ion of th e in tern al carot id ar ter y to expose th e region of t h an 90% at 6-m on t h follow -u p (Fig. 54.14).23 Th e n u m ber of
th e dorsu m sella, th e diap h ragm a sellae, an d th e p it u it ar y st alk. favorable outcom es is even h igh er for u n rupt ured an eu r ysm s.
In our experien ce, it is n ot n ecessar y to ret ract th e in tern al ca- Th e overall m ajorit y of sm all, m ediu m , an d large basilar ap ex
rot id ar ter y, w h ich m ean s th at Dolen c et al u sed a m ore an terior an eur ysm s can be safely m an aged by an experienced team using
rou te to app roach th e in terpedun cular fossa th an th e on e u sed at m icrosu rgical tech n iqu es. Com p licat ion s con t in u e to be p re-
our in st it u t ion . Sw inging th e m icroscop e to a m ore m edial poin t dom in an tly related to p erforator inju ries. In ou r experien ce, an
en ables u s to visualize th e con t ralateral P1 segm en t an d th e p os- u n derst an ding of both th e n orm al an atom y of the perforators as
terior aspect of th e an eur ysm . On e of th e addit ion al advan tages w ell as th e path ological an atom y of th e perforators, as it relates

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54 Surgical Therapies for Basilar Artery Aneurysms 633

in t racavern ou s port ion h as sign ifican tly im proved th e safet y of


th e su rgical procedure an d decreased th e rates of m orbidit y. In i-
t ially, several of our p at ien t s developed com plete ocu lom otor
palsies in th e im m ediate p ostop erat ive p eriod . A fu ll recover y
w as th e ru le rath er th an th e except ion . In looking back at a series
of m ore th an 100 cases, th e full recover y rate is up to 98%. A par-
t ial recover y n ecessitat ing p rism glasses occu rred in a m in orit y
of p at ien t s. More recen tly, w ith our in creased experien ce w ith
h an dling th e oculom otor n er ve an d it s dissect ion , w e h ave been
able to ach ieve on ly par t ial oculom otor palsies in th e postopera-
t ive period in th e overall m ajorit y of pat ien ts.

■ Conclusion
Fig. 54.14 The modified Rankin scale (m RS) scores at discharge, and after
6 m onths in patient s treated with m icrosurgical clipping of basilar apex Th e adven t an d w idesp read u se of en dovascu lar tech n iqu es h ave
aneurysm s. sign ifican tly decreased th e exp erien ce w ith m icrosu rgical t reat-
m en t of posterior circulat ion an eur ysm s. Basilar an eur ysm s are
challenging lesions for both m icrosurgery and endovascular treat-
to th e differen t t ypes an d project ion s of basilar an eur ysm s, h as m ent. The lack of durabilit y of current endovascular technologies
sign ifican tly decreased th e rates of postop erat ive m orbidit y. an d th e abilit y to ach ieve durable resu lt s w ith lit tle m orbidit y
Ocu lom otor n er ve palsy is a frequ en t occu rren ce after m icro- require a n ew gen erat ion of surgeon s to be t rain ed in th e ar t of
su rger y for basilar ap ex an eu r ysm . In ou r exp er ien ce, t h e u t ili- m icrosurger y for posterior circu lat ion an eur ysm s in gen eral, an d
zat ion of t h e step s of exp osin g t h e ocu lom otor n er ve alon g it s basilar an eu r ysm s in par t icular.

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r ysm ch aracter ist ics: an u p dated m et a-an alysis. St roke 2007;38:1404– 26. Kaw ase T, Toya S, Sh iobara R, Min e T. Tran spet rosal approach for an eu-
1410 r ysm s of th e low er basilar ar ter y. J Neurosurg 1985;63:857–861
15. Dolen c VV, Skrap M, Su stersic J, Skrbec M, Morin a A. A t ran scavern ous- 27. Lubicz B, Leclerc X, Gauvrit JY, Lejeun e JP, Pr uvo JP. Gian t ver tebrobasilar
t ran ssellar approach to the basilar t ip an eu r ysm s. Br J Neurosurg 1987; an eu r ysm s: en dovascu lar t reat m en t an d long-term follow -u p. Neu rosu r-
1:251–259 ger y 2004;55:316–323, discussion 323–326

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28. Morcos JJ, Heros RC. Dist al basilar ar ter y an eur ysm s: su rgical techn iques. 43. Friedm an JA, Nich ols DA, Meyer FB, et al. Guglielm i det ach able coil t reat-
In : Batjer HH, ed. Cerebrovascu lar Disorders. Ph iladelph ia: Lippin cot t- m en t of rupt ured saccu lar cerebral an eu r ysm s: ret rospect ive review of a
Raven ; 1997:1055–1078 10-year single-cen ter experien ce. AJNR Am J Neuroradiol 2003;24:526–
29. Neil-Dw yer G, Lang DA, Evan s BT, Neil–Dw eir G. Th e effect of orbitozygo- 533
m at ic access for r upt ured basilar an d related an eur ysm s on m an agem en t 44. Guglielm i G, Viñ uela F, Duckw iler G, et al. En dovascular t reat m en t of pos-
outcom e. Su rg Neurol 1997;47:354–358, discussion 358–359 terior circulat ion an eur ysm s by elect rothrom bosis u sing elect rically de-
30. Nukui H, Mit suka S, Hosaka T, et al. Techn ical poin t s to im prove surgical t ach able coils. J Neu rosurg 1992;77:515–524
resu lt s in cases w it h basilar t ip an eu r ysm s. Neu rol Med Ch ir (Tokyo) 45. McDougall CG, Halbach VV, Dow d CF, Higash ida RT, Larsen DW, Hiesh im a
1998;38(Suppl):74–78 GB. En dovascular t reat m ent of basilar t ip an eur ysm s u sing elect rolyt i-
31. Nu t ik SL. Pterion al cran iotom y via a t ran scavern ous approach for th e cally det ach able coils. J Neurosurg 1996;84:393–399
t reat m en t of low -lying dist al basilar ar ter y an eur ysm s. J Neurosu rg 1998; 46. Nich ols DA, Brow n RD Jr, Thielen KR, Meyer FB, Atkin son JLD, Piepgras DG.
89:921–926 En dovascular treatm ent of rupt ured posterior circulation an eurysm s using
32. Origit an o TC, An derson DE, Tarassoli Y, Reich m an OH, al-Meft y O. Skull elect rolyt ically det ach able coils. J Neurosurg 1997;87:374–380
base approaches to com plex cerebral an eur ysm s. Surg Neurol 1993;40: 47. Ogilvy CS, Hoh BL, Singer RJ, Put m an CM. Clin ical an d radiograph ic out-
339–346 com e in th e m an agem en t of posterior circulat ion aneu r ysm s by u se of
33. San o K. Tem poro-polar approach to aneu r ysm s of th e basilar ar ter y at an d direct surgical or endovascular techniques. Neurosurgery 2002;51:14–21,
aroun d th e dist al bifurcat ion : tech nical n ote. Neurol Res 1980;2:361– discu ssion 21–22
367 48. Pierot L, Boulin A, Cast aings L, Rey A, Moret J. Select ive occlusion of basilar
34. Seoan e E, Tedesch i H, de Oliveira E, Wen HT, Rh oton AL Jr. Th e pretem po- ar ter y an eur ysm s u sing con t rolled det ach able coils: repor t of 35 cases.
ral t ran scavern ous approach to th e in terpedu ncular an d prepon t in e cis- Neu rosurger y 1996;38:948–953, discussion 953–954
tern s: m icrosu rgical an atom y an d tech n iqu e ap p licat ion . Neu rosu rger y 49. Raym on d J, Roy D, Bojan ow ski M, Moum djian R, L’Espéran ce G. En dovas-
2000;46:891–898, discu ssion 898–899 cu lar t reat m ent of acutely ru pt ured an d un ru pt u red an eur ysm s of th e
35. Sh iokaw a Y, Saito I, Aoki N, Mizu t an i H. Zygom at ic tem p orop olar ap - basilar bifurcat ion . J Neurosurg 1997;86:211–219
p roach for basilar ar ter y an eu r ysm s. Neu rosu rger y 1989;25:793–796, 50. Tatesh im a S, Murayam a Y, Gobin YP, Duckw iler GR, Guglielm i G, Viñ uela F.
d iscu ssion 796–797 En dovascular t reat m en t of basilar t ip an eur ysm s using Guglielm i det ach -
36. Solom on RA, Stein BM. Surgical approach es to an eur ysm s of th e vertebral able coils: an atom ic an d clinical outcom es in 73 pat ien t s from a single
an d basilar arteries. Neu rosurger y 1988;23:203–208 in st it u t ion . Neurosu rger y 2000;47:1332–1339, discu ssion 1339–1342
37. Spet zler RF, Hadley MN, Rigam on t i D, et al. An eur ysm s of th e basilar ar- 51. Vallee JN, Aym ard A, Vicaut E, Reis M, Merlan d JJ. Endovascular t reat m en t
ter y t reated w ith circulator y arrest , hypoth erm ia, an d barbit urate cere- of basilar t ip an eur ysm s w ith Guglielm i det ach able coils: predictors of
bral protect ion . J Neurosurg 1988;68:868–879 im m ediate an d long-term result s w ith m ult ivariate analysis 6-year expe-
38. Sugit a K, Kobayash i S, Sh in t an i A, Mut suga N. Micron eurosu rger y for an - rien ce. Radiology 2003;226:867–879
eur ysm s of th e basilar ar ter y. J Neurosurg 1979;51:615–620 52. Hen kes H, Fisch er S, Mariush i W, et al. Angiograph ic an d clin ical result s in
39. Tan aka Y, Kobayash i S, Kyosh im a K, Gibo H. Factors in fluen cing surgical 316 coil-t reated basilar arter y bifurcat ion an eur ysm s. J Neurosurg 2005;
outcom e of th e basilar bifurcat ion an eur ysm s. Neurol Med Ch ir (Tokyo) 103:990–999
1998;38(Su ppl):79–82 53. Fargen KM, Mocco J, Neal D, et al. A m ult icen ter st udy of sten t-assisted
40. Wasch er TM, Spet zler RF. Saccular an eur ysm s of th e basilar bifurcat ion . coiling of cerebral an eu r ysm s w ith a Y con figu rat ion. Neurosurger y 2013;
In : Car ter LP, Spet zler RF, Ham ilton MG, eds. Neurovascular Surger y. New 73:466–472
York: McGraw -Hill; 1995:729–752 54. Dolen c VV, Skrap M, Sustersic J, Skrbec M, Morina A. A t ran scavern ous-
41. Bavin zski G, Killer M, Gru ber A, Reinprech t A, Gross CE, Rich ling B. Treat- t ran ssellar approach to th e basilar t ip an eur ysm s. Br J Neurosurg 1987;
m en t of basilar ar ter y bifurcat ion an eur ysm s by using Guglielm i det ach - 1:251–259
able coils: a 6-year experien ce. J Neurosurg 1999;90:843–852 55. Kalani MY, Zabram ski JM, Nakaji P, Spet zler RF. Bypass an d flow reduct ion
42. Eskridge JM, Song JK. En dovascular em bolizat ion of 150 basilar t ip aneu - for com p lex basilar an d ver tebrobasilar ju n ct ion an eu r ysm s. Neu rosu r-
r ysm s w ith Guglielm i det ach able coils: result s of th e Food an d Drug Ad- ger y 2013;72:763–775, discussion 775–776
m inistration m ulticenter clinical trial. J Neurosurg 1998;89:81–86

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55 Endovascular Therapies for Basilar
Artery Aneurysms
Robert W.J. Ryan, Abhineet Chow dhary, and Michael J. Alexander

ing th ese an atom ic relat ion sh ip s in m in d du ring angiograph ic


■ Relevant Anatomy procedu res can h elp orien t th e pract it ion er w ith resp ect to th e
Th e basilar ar ter y is form ed by th e ju n ct ion of th e t w o ver tebral size an d locat ion of a lesion an d expected clin ical sequelae.
ar teries at th e an terior surface of th e pon tom edullar y jun ct ion Th e large pon tine vessels are the second set of bran ches arising
an d t ravels an average distan ce of 30 m m to it s apex n ear th e from th e basilar ar ter y, an d sim ilarly to th e cerebellar bran ch es,
pontom esencephalic junction, opposite the interpeduncular fossa, th ree m ain vessel pairs are t yp ically fou n d. From cau dal to ros-
w h ere it term in ates in th e bifurcat ion of th e posterior cerebral t ral, th ey in clu de th e p on tom edu llar y ar teries, th e posterolateral
ar teries (PCA).1 Th e basilar ar ter y t apers sligh tly from it s origin , ar teries, an d th e long lateral pon t in e bran ch es.3
w h ere it averages a lit tle less th an 5 m m in diam eter, to it s apex, Th e p er forat in g vessels are t h e fin al set of basilar bran ch
w h ich averages 4 m m in diam eter, an d term in ates often w ith a ar ter ies, an d t h ey are t h e sm allest , m ost n u m erou s, an d m ost
cruciate appearan ce, w ith th e bifurcat ion of th e PCAs superiorly variable. Th e perforators can be divided in to th ree m ain groups:
an d th e su perior cerebellar ar teries (SCAs) in feriorly. Th e level of caudal, m iddle, an d rost ral. Th ey ten d to arise from th e basilar
th e bifu rcat ion determ in es th e in it ial cou rse of th ese con t in u ing ar ter y itself but m ay also arise from adjacen t cerebellar or pon -
ar teries, an d is a n orm al h eigh t (at th e level of pon tom esen ce- t in e vessels an d also th e PCA. Th ere are t ypically 10 to 18 p erfo-
ph alic ju n ct ion ) in 72 to 80% of sp ecim en s, h igh (an terior to th e rators th at sup ply th e brain stem an d th alam us an d also create
m esen cep h alon ) in 10 to 24%, an d low (an terior to th e p on s) in 4 n um erous an astom oses am ong th em selves, w ith a plexu s often
to 10%.1,2 Th e h eigh t of th e bifu rcat ion can h ave im por t an t im p li- observed in the interpeduncular fossa.1,3 One study found that the
cat ion s for th e op erat ive ap p roach to th e basilar arter y for op en dist al 1 cm of th e basilar ar ter y w as th e rich est sou rce of perfo-
su rgical cases. rat ing vessels, an d t h at 50% arose from t h e posterior su rface of
Th e basilar ar ter y gives rise to th ree set s of bran ch vessels: t h e ar ter y, 25% from each of t h e t w o sid es, an d n on e from t h e
th e cerebellar arteries, th e large pon t in e vessels, an d t h e perfo- an ter ior su r face.2 Th is h as im p or t an t im p licat ion s in t reat in g
rat ing ar teries. Th e cerebellar arteries in clu de th e posterior in fe- an eur ysm s arising from th e dist al basilar ar ter y an d apex, as an -
rior cerebellar arter y (PICA), the anterior inferior cerebellar arter y teriorly directed lesion s are m ore favorable for surgical clipping
(AICA), and th e SCA. Th e PICA m ay be defin ed as th e cerebellar because th e posteriorly arising p erforators can be spared.
ar ter y th at arises from th e ver tebral ar ter y, in w h ich case it origi- An aw aren ess of th e m u lt ip le bran ch es of th e basilar ar ter y is
n ates along th e ver tebral ar ter y w ith in 0 to 35 m m of th e jun c- im por t an t w h en assessing an eu r ysm s of th is region , as iden t ify-
t ion w ith th e basilar ar ter y, or it m ay be defin ed as th e ar ter y ing th e vessel m ost closely associated w ith th e an eur ysm n eck
su p plying th e p osteroin ferior por t ion of th e cerebellu m an d m ay can h elp predict th e n at u re of th e lesion an d gu ide th erap eu t ic
or igin ate from t h e basilar ar ter y in u p to 25% of cases.1,3 Th e decision m aking.
AICA m ay arise from th e basilar ar ter y anyw h ere along it s length ,
but in 90% of specim en s occurs in th e low er h alf, alth ough th ere
m ay be a sign ifican t discrepan cy bet w een th e t akeoffs on t h e
righ t an d left sides.3 Th e SCAs are th e m ost con sisten t in th eir
takeoff from th e distal basilar ar ter y, ju st p roxim al to th e bifur-
■ Pathophysiology and Natural History
cat ion of th e PCAs, an d th eir relat ion to t h e ten toriu m is deter- An eur ysm s occu rring along th e basilar ar ter y can be divided in to
m in ed by th e h eigh t of th e basilar apex; th e SCAs lie above th e saccu lar, fu siform , d issect in g, an d in fect iou s t yp es. Th e m ost
ten tor iu m w it h a h igh ap ex, adjacen t to t h e free edge w it h a com m on t yp e is saccu lar, an d t h e classic t h eor y of an eu r ysm
n or m al apex an d below th e ten torium w ith a low apex. Rh oton 1 for m at ion im plicates en dolum in al factors: an eu r ysm s are foun d
describes th e cerebellar ar teries w ith resp ect to th eir associated at bran ch poin ts of vessels, on th e convex side of a cu r ve w h ere
n eu rovascular st ruct ures. Th e SCA is par t of th e upper n eurovas- th e greatest h em odyn am ic an d sh ear st ress forces occu r, an d
cular com plex th at in cludes th e m idbrain ; superior cerebellar poin t in th e direct ion of blood flow.4 How ever, path ological evi-
peduncle; cerebellom esencephalic fissure; tentorial surface of the den ce also suggests th at ablu m in al, or vessel w all, factors play a
cerebellu m ; an d cran ial n er ves III, IV, an d V. Th e AICA is p ar t of role in an eu r ysm form at ion , in cluding disru pt ion of th e in tern al
t h e m id d le com p lex t h at in clu d es t h e p on s; m id d le cerebellar elast ic lam ina at th e en tran ce to the aneur ysm sac and in flam m a-
p ed u n cle; cerebellop on t in e fissu re; t h e p et rosal su r face of th e tor y ch anges in th e w all.5 Th is m ay h elp to explain th e fam ilial
cerebellum ; an d cran ial n er ves VI, VII, an d VIII. Th e PICA is par t (10%) an d con n ect ive t issu e disorders (5%), such as polycyst ic
of th e in ferior com plex th at in cludes th e m edu lla; in ferior cere- kidn ey disease an d Eh lers-Dan los syn drom e t ype 4, th at h ave
bellar peduncle; cerebellom edullar y fissure; the suboccipital sur- been obser ved to be related to aneur ysm form ation, likely through
face of th e cerebellum ; an d cran ial n er ves IX, X, XI, an d XII. Keep - alterat ion s in th e vessel w all.6 Fusiform an eur ysm s involve th e

635

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636 V Cerebral and Spinal Aneurysms

circu m feren t ial dilat ion of a segm en t of an in t racran ial ar ter y, General risk factors for the developm ent and rupt ure com m on
an d are ch aracterized path ologically by degen erat ion of th e in - to all in t racran ial an eur ysm s, in cluding th ose of th e basilar ar-
tern al elast ic lam in a, sm ooth m uscle at rophy in th e m edia layer, ter y, in clu de fem ale sex; in creasing age; fam ily h istor y; con n ec-
an d in t im al hyperplasia w ith out ath erom atou s deposit s.5 Un like t ive t issu e disease; previou s SAH; an d m odifiable factors su ch as
saccu lar an eu r ysm s, th e fu siform t ype is n ot u su ally associated sm oking, excessive alcoh ol in t ake, an d hyp er ten sion . An eu r ysm s
w it h a bran ch ing vessel, alth ough p erforators or sm all bran ch of th e vertebrobasilar system rep resen t 10 to 18% of all in t racra-
ar teries m ay arise from th e path ologically dilated segm en t an d n ial an eur ysm s, an d 50 to 65%of such lesion s occur at th e basilar
pose a risk if occlu ded du ring t reat m en t . Fu siform an eur ysm s bifurcat ion . Alth ough n ot as com m on as an eur ysm s of th e an te-
m ay range in size from sm all segm en tal dilat ion s to giant doli- rior circu lat ion , lesion s of th e posterior circu lat ion seem to be
choectatic lesions, often filled w ith throm bus. Patients w ith these associated w ith h igh er risks an d w orse progn osis. Th is h as been
aneurysm s, particularly the latter t ype, often present w ith sym p - born e ou t in several st udies, an d for both un ru pt ured an d rup -
tom s related to m ass effect in clu d in g brain stem com p ression , t ured an eu r ysm s. With regard to th e form er, th e In tern at ion al
cran ial n er ve deficit s, an d obst ruct ive hydroceph alu s, in addi- St udy of Un r u pt u red In t racran ial An eu r ysm s (ISUIA) fou n d th at
t ion to su barach n oid h em orrh age (SAH) from ru pt u re or em bolic across all sizes, posterior circu lat ion an eur ysm s h ad a h igh er rate
st rokes from p ar t ial th rom bosis.7,8 of rupt ure over a 5-year period com pared w ith sim ilar size of
In Drake’s 9 exp erien ce w ith gian t an eu r ysm s of th e p osterior cavernous and anterior circulation aneurysm s (Table 55.1).12 An-
circulat ion , 17% w ere fusiform , an d in con t rast to th e saccular oth er large m eta-an alysis exam in ing both pat ien t an d an eu rysm
t yp e, w h ich m ostly arose at th e basilar bifu rcat ion or SCA bran ch ch aracterist ics as risks for ru pt u re fou n d an in creased relat ive
poin t s, th e fu siform variet y w as m ore often fou n d along th e bas- risk of ru pt u re of 2.5 for an eu r ysm s in th e posterior circu lat ion ,
ilar t r u n k an d ver tebral arteries. Dissect ing an eur ysm s occu r as on e of th e st rongest predictors for rupt ure along w ith in creasing
a result of blood en tering th e ar ter y w all th rough a sudden dis- size an d sym ptom at ic lesion s.13 A Jap an ese sin gle in st it u t ion
rupt ion in th e en doth elium an d in tern al elast ic lam in a, creat ing series also foun d a h azard rat io of 2.9 for un rupt ured an eur ysm s
a false lum en bet w een th e t issue layers in a longit u din al direc- of th e posterior circulat ion , a sim ilar t ren d dem on st rat ing th e
t ion . Alth ough occasion ally repor ted follow ing t rau m a, m ost dis- in creased risk of rupt ure for th is locat ion .14
sect ion s occur sp on tan eou sly, an d th e false lu m en m ay occur Th e n at u ral h istor y of ru pt u red an eu r ysm s t reated con ser va-
bet w een th e in tern al elast ic lam in a an d m edia if th ere is m in i- t ively is poor, w ith rates of rebleeding of 4% th e first day, 12 to
m al disru pt ion of th e m u scu lar layer, or bet w een t h e m edia an d 20%w ith in th e first 2 w eeks, 37%at 4 w eeks, an d m or talit y from
adven t it ia w ith m ore advan ced m edia disr upt ion .10 Th e n at u re repeated h em orrh age app roach ing 50%.15–17 To preven t th e m or-
of, an d sym ptom s related to, a d issect ing an eu r ysm are d eter- bidit y an d m or talit y associated w ith rebleeding, early (w ith in 24
m in ed by t h e p at h of t h e p seu d olu m en , w h ich follow s on e of to 72 h ou rs of presen tat ion ) an d ult ra-early (w ith in 24 h ours)
th ree cou rses: en ding blin dly w ith in th e ar terial w all, reen tering t reat m en t of an eu r ysm al SAH h as been sh ow n to im p rove ou t-
th e t ru e lu m en , or ru pt u ring th rough th e adven t it ia. In fect iou s com e, as u p to 7% of p at ien t s in a large ter t iar y cen ter h ad re-
in t racran ial an eu r ysm s resu lt from d egradat ion of t h e ar ter y r u pt ure w ith in th e first 3 days, 20%of w h om h ad vertebrobasilar
w all, w ith dest ru ct ion of th e in tern al elast ic lam in a, in t im al pro- an eur ysm s.15,16 With regard to locat ion of rupt u red an eur ysm s,
liferat ion , an d in flam m at ion w ith p olym orp h on uclear cell in fil- a sur vey of pat ien ts from th e Mayo Clin ic foun d th at th ose h ar-
t rat ion of th e m edia an d adven t it ia from an in fect ious process.11 boring lesions of the posterior circulation had significantly w orse
Alth ough som et im es referred to as m ycot ic an eu r ysm s, fu ngal presen t ing grade, early m or talit y, an d poorer overall sur vival;
in fect ion s are a rare cau se of th is t yp e of an eu r ysm , w ith m ost 48-h our sur vival w as 77% for an terior circulat ion versus 32% for
resulting from bacterial sources, especially Staphylococcus aureus posterior circu lat ion , an d 30-day su r vival w as 57% an d 11% for
an d St reptococcus viridians, an d th u s in fect iou s an eu r ysm s is a th ose locat ion s, respect ively.17 Th ese fin dings suggest th at th e
bet ter m on iker for th ese lesion s. In fect ion of th e vessel w all m ay proxim it y to th e brain stem an d th e com m on occu rren ce of in t ra-
occur from h em atogen ous spread or direct exten sion of a n earby ven t ricular h em orrh age an d hydroceph alus w ith th e r upt ure of
sou rce; in th e case of th e form er, d ist al arterial bran ch ing sites posterior circu lat ion an eu r ysm s likely con t ribu te to th e p oor
are m ost often involved, w h ereas th e lat ter ten ds to affect m ore outcom es; th e early death s, often prior to arrival to th e h ospital
proxim al vessel segm en t s, an d both h ave been reported in th e or peripheral m edical centers, m ight lead to underrepresentation
posterior circu lat ion .11 of th ese lesion s in large series based at ter t iar y h ospitals.

Table 55.1 Percent Risk of Aneurysm Rupture Over 5 Years Based on Aneurysm Size and Location

< 7 mm, < 7 mm,


Aneurysm Location No Previous SAH Previous SAH 7–12 mm 13–24 mm ≥ 25 mm

Cavernous carotid 0 0 0 3 6.4


AC/MC/IC 0 1.5 2.6 14.5 40
Post/PCo 2.5 3.4 14.5 18.4 50
Abbreviations: AC, anterior com municating or anterior cerebral artery; MC, m iddle cerebral artery; IC, internal carotid artery; Post/PCo, vertebrobasilar,
posterior cerebral, or posterior com m unicating artery.
Source: Adapted from Wiebers DO, Whisnant JP, Huston J III, et al; International Study of Unruptured Intracranial Aneurysm s Investigators. Unruptured
intracranial aneurysm s: natural history, clinical outcom e, and risks of surgical and endovascular treatm ent. Lancet 2003;362:103–110
Note: For all size categories, aneurysm s of the posterior circulation have a higher rate of rupture.

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55 Endovascular Therapies for Basilar Artery Aneurysm s 637

Most natural histor y data for aneur ysm s of the vertebrobasilar From th e en dovascu lar series of posterior circu lat ion an eu -
system con cern saccu lar-t ype lesion s or h ave n ot been st rat ified r ysm s, th e rate of pat ien ts w ith u n ru pt ured an eu r ysm s presen t-
by an eur ysm t ype, alth ough som e in form at ion for oth er an eu- in g to clin ical at ten t ion is 22 to 45%, alt h ough on ly 14 to 31%
r ysm s exist s.8 Pat ien ts w ith dissect ing an eur ysm s w h o presen t are asym ptom at ic, w ith th e rem ain der dem on st rat ing on e or a
w ith SAH h ave a 24%rate of rebleeding, w ith h igh m ort alit y from com bin at ion of th e follow ing, in decreasing order of frequ en cy:
su bsequ en t even ts, favoring t reat m en t for lesion s in p at ien t s h eadach e, th ird n er ve palsy, con fusion , h em ip aresis, m en ingis-
w h o presen t w ith h em orrh age.18 Pat ien ts w ith fusiform an d dol- m us, drow sin ess, diplopia, an d n ausea an d vom it ing. Headach e
ich oectatic aneur ysm s have a variet y of presentations and behav- and nausea w ere som etim es associated w ith hydrocephalus from
iors, m aking their optim al treatm ent a source of debate. Som e th e aqu edu ct , th ird or fou r th ven t ricle com pression , an d dip lopia
auth ors believe th at th ese an eu r ysm s are n on aggressive lesion s, an d occulom otor paresis from direct com pression by en larging
an d th ey favor serial im aging.5 Bu t on e series of 159 p at ien t s fol- an eur ysm s on th e adjacen t cran ial n er ves III, IV, an d VI. Isch em ic
low ed over t im e fou n d th at 48% h ad an eu r ysm en largem en t , sym ptom s can occu r w ith p osterior circu lat ion an eu r ysm s ei-
w h ich w as associated w ith sign ifican t m orbidit y an d death , an d th er as a resu lt of propagat ion of th e em bolu s from a th rom bosed
an oth er series of 28 pat ien t s w ith gian t fusiform an eu r ysm s h ad or p ar t ially t h rom bosed lesion , or from occlu sion of p er forator
46% m or talit y over 4 years, arguing again st a ben ign n at ure.19,20 vessels, bot h of w h ich are m ore com m on w it h fu sifor m an eu -
Th e m ech an ism of en largem en t , an d w hy h alf of th ese lesion s r ysm s bu t can also occu r w it h t h e saccu lar or d issect ing t yp e.7
grow, is n ot en t irely clear, bu t in som e cases m ay be related to In addit ion , som e pat ien t s w ith fusiform an eur ysm s h ave been
intram ural hem orrhage and throm bus form ation; m any fusiform rep or ted to p resen t w it h com p ressive sym ptom s of t h e low er
an eur ysm s are n oted to be par t ially th rom bosed, an d alth ough cran ial n er ves, in clu d ing t rigem in al n eu ralgia an d h em ifacial
th e rate of SAH is 10 to 25%, m ore of th ese an eu r ysm s cau se sp asm , dysp h agia, an d sen sorin eural h earing loss.
sym ptom s an d m orbidit y from m ass effect , an d m any of th em An eur ysm rupt ure w ith SAH w as th e m ost com m on presen t-
are of gian t size (≥ 2.5 cm ).21 Th is h igh ligh t s an im por tan t feat ure ing sym ptom , from 55 to 78% of t h e t im e, in th e series of poste-
in assessm en t of p osterior circu lat ion an eu r ysm s, as th e pres- r ior circu lat ion an eu r ysm s t reated w ith en d ovascu lar coilin g.
en ce of th rom bu s m ay lim it th e ap p aren t size of th e lesion by Th ere w as a ran ge in t h e Hu n t -Hess grad e on ad m ission , w it h
intralum inal contrast im aging techniques such as digital substrac- 35 to 70% of pat ien ts presen t ing as grade I an d II, 12 to 25% as
t ion angiograp hy (DSA) an d com p u ted tom ograp hy angiography grade III, an d 15 to 29% as grade IV an d V, an d a w orse in it ial
(CTA), w hereas conventional cross-sectional im aging such as m ag- grade correlated w ith a w orse ou tcom e. Ru pt u re rates ten d to be
n et ic reson an ce im aging (MRI) m ay give a m ore accurate m ea- h igh er in saccular an eu r ysm s an d low er in fu siform an eur ysm s,
su rem en t . Iden t ifying th e t ru e size is im p or tan t , as th e n at u ral w h ich are m ore likely to presen t w ith com pressive or isch em ic
h istor y of all t ypes of gian t an eur ysm s rem ain s ver y poor, w ith sym ptom s.7–9
80% of u n t reated p at ien t s disabled or dead w ith in 5 years.22

■ Perioperative Evaluation
■ Clinical Presentation Th e in it ial w orku p of a p at ien t w ith a ver tebrobasilar an eu r ysm
An eur ysm s of th e posterior circulat ion m ay com e to clin ical at- sh ou ld st ar t w ith a detailed h istor y an d p hysical exam in at ion ,
ten t ion from on e of th ree m ajor sym ptom groups: r upt ure w ith w ith an em ph asis on determ in ing th e r upt ure stat us an d sym p -
SAH, m ass effect on adjacen t n eu ral st r u ct u res, or isch em ic tom s at t ributable to th e lesion. Historical feat ures such as per-
com p licat ion s. Altern ately, th ey m ay be discovered as asym p - son al or fam ily histor y of SAH, sm oking, hyperten sion, an d under-
tom at ic lesion s during th e invest igat ion of oth er an eur ysm s, or lying con nective t issu e disorders raise th e risk of h arboring an
in ciden tally du ring cran ial im aging for w orkup of oth er sym p - an eur ysm . Recen t in fect ion s or im m un osuppression , t raum a, or
tom s or screen ing tests. W h en assessed from th e largest series of isch em ic sym ptom s m ay suggest in fect iou s, dissect ing, or par-
posterior circu lat ion an eu r ysm s t reated by en dovascu lar m eth - t ially th rom bosed an eu r ysm s. On set an d du rat ion of sym ptom s
ods, th e average age of th ese pat ien ts is 50.5 to 53.9 years an d 59 are also im por tan t , as a classic th un derclap h eadach e usually
to 72% are fem ale, sim ilar to t h e age an d sex d ist r ibu t ion s seen h eralds acute rupt u re, w h ereas progressive m orn ing h eadach es
in large st udies of an eur ysm s of all in t racran ial locat ion s.23–30 w ith n ausea an d vom it ing m ay suggest an en larging lesion w ith
Th ese sam e st u d ies fou n d t h e locat ion of p oster ior circu lat ion hydroceph alu s. A list of m edicat ion s an d allergies sh ould be ob -
an eu r ysm s to be t h e basilar ap ex in 49 to 72% of cases, t h e SCA tain ed, an d th e abilit y to tolerate an t iplatelet th erapy sh ould be
in 7 to 9%, t h e basilar t r u n k in 2 to 8%, t h e ver tebrobasilar ju n c- determ in ed, as it is requ ired for m any en dovascu lar t reat m en ts.
t ion in 9 to 13%, an d th e ver tebral ar ter y or PICA in 11 to 16%. A gen eral physical exam in at ion sh ould be con ducted to deter-
Posterior circu lat ion an eu r ysm s w ere sm all (≤ 11 m m ) in 47 to m in e a pat ien t’s fit n ess for en dovascular t reat m en ts th at m ay
63%, large (12–24 m m ) in 25 to 40%, an d gian t (≥ 25 m m ) in 6.5 require sedation or general anesthesia. Focused exam ination should
to 9% of th ese lesion s t reated by en dovascular m eth ods, com - assess ext raocular m ot ilit y an d th e fu n ct ion of cran ial n er ves III,
pared w ith 78%, 20%, an d 2%, respect ively, for th e sam e size cat- IV, an d VI, an d th e presen ce of Parin aud’s syn drom e. Cerebellar
egories in th e coop erat ive st u dy.31 An oth er m orph ological fea- signs, such as coordination problem s, dysm etria, dysdiadokinesis,
t u re, th e w ide n eck, defin ed as > 4 m m across or a d om e-to-n eck an d ataxia, sh ou ld be elicited.
rat io of < 2, h ave been obser ved in 40 to 60% of p oster ior circu - Basic preoperative bloodwork, including a com plete blood count ,
lat ion an eu r ysm s, an d in crease t h e d ifficu lt y of en d ovascu lar coagu lat ion st at u s, an d kid n ey fu n ct ion , sh ou ld be m easu red
t reat m en t .32,33 before any en d ovascu lar p roced u re. For p at ien t s p reviou sly on

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638 V Cerebral and Spinal Aneurysms

an t iplatelet m edicat ion s, or loaded in an t icipat ion of using sten t even in th e set t ing of dissect ion s an d fusiform dilat ion s, an d can
assist an ce, m easuring form al platelet fun ct ion assays or poin t of reveal th e t rue lu m en . As w ith CTA, a lim it at ion of DSA can be
care test s su ch as P2Y12 in h ibit ion an d asp ir in react ivit y u n it s determ in ing t ru e an eu r ysm size in th e set t ing of th rom bosis, as
(ARUs) can h elp in form th erapy. on ly th e filling por t ion of th e an eur ysm w ill be visu alized. An -
If ru pt ure is suspected, th e first invest igat ion sh ould be n on - oth er im port an t role for DSA is assessing th e path w ays of collat-
en h an ced com pu ted tom ograp hy (CT) of th e brain , w h ich h as eral flow to th e posterior circulat ion an d poten t ial don or vessels
a sen sitivit y for detect ing SAH approach ing 100% in th e in it ial if byp ass is requ ired as p ar t of t h e t reat m en t p arad igm . As p ar t
h ours after ict u s, an d falling to arou n d 50% after 7 days, as blood of th is w orkup, balloon test occlu sion (BTO) of on e or both ver te-
clears from th e basal cistern s.34 If th e clin ical stor y raises st rong bral ar teries or th e basilar ar ter y m ay be perform ed w ith clin ical
su spicion for an eu r ysm ru pt u re bu t th e in it ial CT is n egat ive, th e assessm en t of th e pat ien t during balloon in flat ion ; toleran ce is
n ext test in m ost cen ters is lum bar pun ct ure (LP) perform ed at in dicated by n o sym ptom s du ring 15 to 30 m in u tes of in flat ion
least 12 h ours after t h e in it ial even t (bu t w ith in 14 days), w ith an d evid en ce of collateral su p p ly from t h e ot h er ar ter ies in -
cerebrospin al fluid (CSF) sen t to th e lab for cen t rifugat ion an d jected .40 Ch allenges, su ch as in d u ced hyp oten sion , m ay be u sed
spect roph otom et r y for bilir ubin; visu al in spect ion for xan th o- d u r ing balloon in flat ion in an at tem pt to elicit sym ptom s an d
ch rom ia m ay also be p erform ed bu t is less sen sit ive.35 In place of predict delayed failu re. Oth er adju n ct ive test s, su ch as cerebral
LP, som e facilit ies in stead obtain a CTA of th e brain in cases of blood flow an d perfusion assessed by single ph oton em ission
n egat ive CT w ith a stor y suggest ive for an eur ysm rupt ure, as th is com p u ted tom ography scan n ing before an d d u ring t h e test oc-
w ou ld u su ally be th e n ext test ordered if th e CT revealed SAH. clu sion are u sed at som e cen ters in th e h opes of im p roving th e
CTA h as a post test p robabilit y of 99% for ru ling out lesion al SAH, reliabilit y of th e BTO. Th ese m an euvers h ave n ot been u sed in
an d it avoids th e risks of LP.36 A CTA w ith th ree-dim en sion al (3D) th e p osterior circu lat ion to th e sam e degree as th e an terior cir-
recon st ru ct ion can reveal m any an atom ic feat u res of vertebro- culat ion .41 Th e u t ilit y of BTO in th e basilar ar ter y h as been de-
basilar an eur ysm s, in cluding n eck size, dom e size, dom e-to-n eck bated, as there is a repor t of a pat ien t w h o developed dysar th ria
rat io, aspect rat io (h eigh t-to-n eck rat io), an d relat ion sh ip to ad- du ring BTO bu t w en t on to tolerate su rgical clip ping of th e basi-
jacen t bony st r u ct u res, p ar t icu larly th e p osterior clin oid s. lar artery for treatm ent of an aneurysm , w ith the explanation that
A recen t st u dy com p ar ing 64-slice CTA w it h 3D rot at ion al th e balloon likely occlu d ed a longer segm en t of th e ar ter y w ith
DSA foun d th at CTA h ad a sen sit ivit y of 96% for an eur ysm s as brain stem perforators th an th e clip.42
sm all as 3 m m , an d an oth er grou p of invest igators determ in ed Perhaps th e strongest predictor of tolerance of proxim al vessel
that anatom ic in form at ion from CTA is sufficien t w ithout DSA for occlusion is the size of the posterior com m unicating arter y; w hen
m aking t reat m en t decision s in m ore th an t w o-th irds of cases.37,38 at least on e vessel is > 1 m m in diam eter, th ere is a h igh rate of
CTA can also provide in form at ion about collateral circulat ion toleran ce an d good long-term outcom e.22 Th e reason th at som e
su ch as th e presen ce an d size of posterior com m u n icat ing ar ter- pat ien ts w ith long, fu siform an eu r ysm s th at con tain m u ltip le
ies, bu t is un able to resolve th e involvem en t of p erforators w ith perforators are able to tolerate proxim al vessel occlu sion an d an -
basilar aneur ysm s, and given its dependence on intravenous con - eu r ysm th rom bosis is st ill n ot clear, bu t it m ay be a result of u n -
t rast , m ay u n derest im ate an eu r ysm size if th rom bu s is p resen t . appreciated collateral circulat ion at th e level of th e brain stem .8,9
MRI an d m agn et ic reson an ce angiography (MRA) can p rovide In any case, patients w ho clearly fail BTO based on clinical or per-
excellen t det ail of soft t issu es an d accu rate an eu r ysm sizing in fu sion criteria are at h igh er risk of isch em ic com p licat ion s w ith
th e case of par t ially th rom bosed lesion s, as blood can ap pear as vessel occlu sion , an d som e t ype of ext racran ial-to-in t racran ial
differen t in ten sit ies based on th e oxygen at ion state of h em oglo- (EC–IC) revascularization procedure is recom m en ded-to-prevent
bin , an d m easu rem en t s can be m ad e bet w een t h e visu alized st roke before th erapeu t ic occlu sion of a p aren t arter y.9
w alls of t h e an eu r ysm . Alt h ough n ot t yp ically u sed in r u pt u red
lesion s du e to longer acquisit ion t im es an d th e n eed to rapidly
secu re th e an eu r ysm , MRA is th e preferred test for screen ing an d
follow ing un rupt ured an eur ysm s, as it requires n o radiat ion ex-
posure. Som e con cern s in it ially existed abou t th e abilit y of MRA
■ Endovascular Approaches
to resolve sm all aneur ysm s; how ever, w ith m odern tim e-of-fligh t Th e en dovascu lar m an agem en t paradigm s for ver tebrobasilar
sequ en ces, in creased m agn et ic field st rengt h s of 3 tesla, an d an eur ysm s can be broadly divided in to decon st r uct ive st rategies
ju dicious use of con t rast-en h an ced MRA, th is n on invasive m o- (paren t arter y occlusion ) w ith or w ith out revascularizat ion , an d
dalit y is an im p or t an t p ar t of t h e assessm en t of p oster ior circu - con st r u ct ive st rategies (an eu r ysm occlu sion w ith p aren t ar ter y
lat ion an eu r ysm s.36 Th ere are also descript ion s of quan t itat ive preser vat ion ). Con st ru ct ive st rategies in clu de coil em bolizat ion
MRA being u sed to determ in e blood flow in th e p osterior circu - alon e or w ith balloon or sten t assistan ce, liquid polym er em boli-
lat ion ; th e direct ion an d volu m e of flow com p ared w ith n orm al zat ion , an d low -p orosit y flow -diver t ing sten t s.
exp ected valu es m ay h elp predict th e abilit y to tolerate vessel Adapt ing th e use of in t ravascular balloon s described by Ser-
sacrifice or n eed for bypass in th e t reat m en t of an eur ysm s.39 bin en ko 39 in 1974, Higash ida et al40 rep or ted on t h e en dovas-
Digit al subt ract ion angiography rem ain s th e gold stan dard for cu lar m an agem en t of p oster ior circu lat ion an eu r ysm s in 25
assessm en t of p osterior circu lat ion an eu r ysm s. Use of rotat ion al p at ien t s, n on e of w h om required paren t vessel occlusion due to
DSA provides h igh ly accurate 3D recon st ruct ion s of th e paren t an eu r ysm m or p h ology. After a p er iod of tem p orar y occlu sion
ar ter y an d an eur ysm , yielding th e m ost detailed m orph ological to con firm th e adequacy of collateral blood flow, balloon s w ere
in form at ion . Biplan ar DSA im ages acqu ired at h igh fram e rates filled w ith a h arden ing agen t an d detach ed. Th e advan tages of
give a dyn am ic view of blood flow an d an eu r ysm al h em ody- u sing detach able balloon s in clu de th e abilit y to in flate an d de-
n am ics, an d ch aracterize th e an eur ysm n eck an d in flow pat tern , flate to con firm opt im al posit ion ing, rapid occlu sion of th e ar-

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55 Endovascular Therapies for Basilar Artery Aneurysm s 639

ter y w ith a single device, an d h igh rates of an eur ysm th rom bosis Alth ough BTO m ay h elp determ in e w h ich pat ien ts w ill ben efit
w ith th is form of h u n terian ligat ion . Th e disadvan t ages in clude from a revascu larizat ion p rocedu re to redu ce th is risk, th e p eri-
th e risk of vessel ru pt u re w ith overin flat ion , balloon deflat ion operat ive m or talit y for posterior circu lat ion bypass procedu res
w ith ret u rn of flow to an eur ysm , an d prem at ure detach m en t in a recen t review w as 15%, m u ch h igh er th an for th e an terior
w ith distal em bolizat ion ; curren tly n o detach able balloon s are circulat ion , so oth er t reat m en t opt ion s sh ou ld be carefully con -
approved or available in th e Un ited States. Th e oth er en dovascu - sidered an d tried before em barking on th is therapy.43 Deconstruc-
lar tech n iqu e for paren t ar ter y occlu sion (an d th e on ly on e cu r- t ive st rategies n ow ten d to be reser ved for persisten tly en larging
ren t ly available in th e Un ited St ates) is deliver y of det ach able fu siform lesion s w it h m ass effect , in p at ien t s w it h su fficien t
coils in to th e lu m en (Fig. 55.1). An advan t age of th is m eth od is collaterals an d toleran ce on BTO, or in t h ose w h o are good can -
t h at coils m ay be p laced over a sh or ter segm en t of t h e vessel d idates for byp ass w it h or w it h ou t t rap p ing an d resect ion to
t h an a balloon , low er in g t h e r isk to p er forat in g ar ter ies, bu t a reduce an eu r ysm m ass effect .
draw back is th e in creased t im e for deliver y, an d usu ally m ore Early at tem pt s at en d ovascu lar recon st r u ct ive tech n iqu es
devices are n eeded com p ared w ith balloon s. Th e m ost im p or tan t u t ilizing balloon s to fill an eu r ysm s w h ile p reser ving blood flow
con siderat ion before paren t ar ter y occlu sion is th e st at u s of col- in t h e p aren t ar ter y h ad m od erate su ccess, bu t t h e safet y an d
lateral circu lat ion , as u p to 13% of pat ien ts are at risk of sym p - efficacy w as m arked ly im p roved w it h t h e d evelop m en t of d e-
tom at ic isch em ia w ith su dden occlu sion of th e basilar ar ter y.22 t ach able p lat in u m coils by Guglielm i et al44 in 1991. Sh or t ly

a b

Fig. 55.1a–c (a) Preoperative lateral vertebral artery (LVA) angiogram


showing a large fusiform basilar aneurysm in a 9-year-old boy with sub-
arachnoid hem orrhage. (b) Postoperative LVA angiogram dem onstrating
segm ental parent artery occlusion of the basilar trunk aneurysm with coils.
(c) Postoperative lateral carotid artery angiogram shows adequate collater-
als through the posterior com m unicating artery to supply the distal basilar
c artery and its branches.

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640 V Cerebral and Spinal Aneurysms

after, th ese au th ors repor ted on th eir experien ce coiling r up - as single piece, an d th e pores are fixed an d closed; in th e open -
t ured basilar t ip an eur ysm s; th ey h ad im pressive early results, cell d esign , abou t h alf of t h e t in es are n ot con n ected , allow in g
w ith h igh rates of com plete occlusion in an eur ysm s w ith n arrow som e of t h e p ores to be op en . Th e goal of sten t d eliver y is to
n ecks, and a low 4.8% m orbidit y an d 2.4% m or talit y. Th ey also cover t h e n eck of th e an eu r ysm , p roviding a st ru ct u ral su pp or t
h elped create a paradigm sh ift for coiling from an experim en tal to keep coils in side. Th e sten t m ay also provide a h em odyn am ic
p roced u re for p at ien t s u n able to tolerate su rger y to a viable ben efit , redirect ing flow in side th e n orm al vessel lum en , an d
t reat m en t altern at ive.25 Cu rren tly, prim ar y coiling of vertebro- also ser ve as a scaffold for en doth elializat ion .
basilar an eur ysm s is th e first ch oice of t reat m en t , par t icularly in Th ere are n u m erou s m eth ods by w h ich sten t -assisted coiling
lesion s w ith favorable m orp h ology, as th e p rocedure is t im e ef- can be perform ed; th e sten t m ay be delivered follow ed by reac-
ficien t , offers good protect ion from r upt ure, an d does n ot require cessing th e an eur ysm by passing th e m icrocath eter th rough th e
pre- or postop erat ive an t ip latelet th erapy. Lim itat ion s of coiling sten t t in es for coiling, requ iring th e u se of on ly a single m icro-
alon e are m ost n ot iceable w ith difficult lesion sh apes; early re- cath eter. Altern ately, t w o m icrocath eters m ay be used, w ith th e
su lt s fou n d t h at 85% of n ar row -n ecked an eu r ysm s cou ld be first p osit ion ed in sid e t h e an eu r ysm , an d t h e secon d u sed to
com p letely occlu ded as com p ared w ith on ly 15%of w ide-n ecked d eliver th e sten t , “jailing” th e first in a st able con figurat ion for
lesion s.33 With w ider n ecks, th e risk of coil h ern iat ion in to th e coiling an d obviat ing th e n eed for p assing th rough th e sten t . For
paren t arter y is h igh er, an d su rgeon s ten d to be less aggressive an eur ysm s arising from th e basilar t run k or a single bran ch ing
about achieving h igh packing den sit ies, leading to low er rates of ar ter y, a single sten t is u sed. For basilar bifurcat ion an eur ysm s, a
com plete occlu sion , in creased n eck rem n an t s, an d m ore recu r- Y-sten t tech n ique is often em ployed, w ith sten ts placed in both
ren ces over t im e. PCAs to fully protect th e paren t ar teries during coiling 50,51 (Fig.
Several adju n ct ive tech n iqu es h ave been develop ed to h elp 55.2). For Y-sten t ing, th e first device m u st be an open -cell design
address th e sh or tcom ings of coiling alon e. Th e first tech n ique so t h at t h e secon d device, w h ich m ay be op en - or closed-cell,
develop ed to assist in coil deliver y for w id e-n ecked an eu r ysm s can fit th rough w ith ou t becom ing n arrow ed . Th e first sten t is
w as balloon rem odeling w ith tem porarily in flatable, n on d et ach - d ep loyed in t h e PCA t h at is t h e m ost ch allenging to access; as
able balloon s.45,46 Using th is m eth od , a m icrocat h eter capable of t h e in terst ices of th e sten t can m ake su bsequen t select ion of th e
delivering coils is p osit ion ed in side th e an eur ysm , an d a balloon con t ralateral PCA m ore difficu lt , it is bet ter to access th e m ore
is th en in flated in th e paren t arter y across th e n eck of th e an eu - favorable vessel at th is poin t . With both PCAs protected, the an -
r ysm , stabilizing th e cath eter an d allow ing coil deliver y w ith out eu r ysm is t h en reaccessed t h rough t h e st r u t s of t h e sten t an d
h ern iat ion in to th e paren t ar ter y. Typically, th e balloon is th en coils are deployed.
deflated, an d th e coil rem ain s in place. Recen tly, som e au th ors An oth er m eth od th at h as been described for protect ing both
h ave advocated delivering an d detach ing several coils during on e PCAs w ith a single sten t relies on a sufficien tly large posterior
balloon in flat ion to in crease th e com plexit y an d st abilit y of th e com m u n icat ing ar ter y from th e an terior circu lat ion , w ith a m i-
coil m ass.47 Th e benefits of balloon -assisted coiling are the abilit y crocath eter directed from th e in tern al carot id via th e posterior
to t reat w ide-n eck lesion s an d ach ieve h igh er packing den sit ies com m u n icat ing ar ter y in to th e ip silateral P1 segm en t of t h e PCA,
w ith out th e n eed for im plan ted devices or an t iplatelet th erapy; across th e basilar bifurcat ion in to th e con t ralateral PCA.52 Th is
th is lat ter poin t is especially im p or t an t for redu cing h em orrh agic approach en ables th e surgeon to avoid overly tor t uous or hypo-
com plicat ion s w ith ru pt u red an eu r ysm s. Som e risks of u sing a plast ic ver tebral ar teries an d requ ires on ly on e sten t , bu t is n ot
balloon in clude ar terial injur y or ru pt ure during in flat ion , an d possible if th e posterior com m u n icat ing ar teries are sm all, an d
rupture of the aneurysm . Throm botic and em bolic com plications m ay ch ange th e sh ap e of th e basilar bifu rcat ion from a “Y” to a
are h igh er w ith balloon u se, bu t can be m it igated w ith judiciou s “T,” poten t ially pu t t ing perforat ing arteries on st retch an d at risk.
periprocedu ral an t icoagu lat ion . Balloon in flat ion cau ses tem po- Each basilar apex an eu r ysm m u st be assessed in dividu ally to de-
rar y cessat ion of blood flow an d risk of isch em ia if collateral cir- term in e th e opt im um t reat m en t paradigm . W h en possible, use
culation is lim ited; slow coil detachm ent system s can increase the of a single sten t to rem odel w ide-n ecked an eur ysm s is desirable,
t im e at risk, w h ereas m ore rapid d et ach m en ts facilitate sh or ter as th is is often sufficien t to create a safe geom et r y for coiling
inflation tim es. Finally, w ith balloon deflation, there is a sm all risk w h ile red u cing sten t -related com p licat ion s. Th e u se of t h e Y-
of prolapse or fran k h ern iat ion an d m igrat ion of th e coil m ass, tech n ique can be reser ved for ver y w ide n ecks w h ere both PCAs
especially if several coils h ave been det ach ed togeth er.48 are at risk.
An oth er adjun ct ive m eth od for coiling of basilar ar ter y an eu- Alt h ough sten t rem od eling can be a h igh ly effect ive tech -
r ysm s is t h e u se of an in t ravascu lar sten t . Th e first sten t u sed n ique, allow ing safe coiling of som e w ide-n ecked an d fusiform
in th e cran ial circu lat ion w as a st ain less steel, balloon -m ou n ted lesion s th at w ou ld n ot oth er w ise be t reat able, it also creates cer-
coron ar y sten t for th e t reat m en t of a r upt ured, fusiform , basilar tain risks an d ch allenges. First , to preven t th rom boem bolic com -
ar ter y an eur ysm th at w as deem ed un clippable; a m icrocath eter plicat ion s an d th rom bosis of th e sten t , pat ien ts are loaded w ith
w as advan ced th rough th e sten t t in es in to th e an eu r ysm , an d du al an t iplatelet m edicat ion s, in creasing th e risk of h em orrh agic
coils w ere successfully delivered.49 New er sten ts h ave been de- even ts. Alth ough th is risk is t ypically ver y low for un ru pt ured
sign ed specifically for u se in th e brain th at are m ore com p lian t cases, it r ises d ram at ically for r u pt u red an eu r ysm s, esp ecially
an d n avigable t h rough tor t u ou s an atom y an d m ad e of self- w it h resp ect to ot h er n eu rosu rgical p roced u res su ch as ven -
exp an ding n it in ol. Th e t w o m ost com m on sten t s u sed today for t r icu lostom y an d ven t riculoperiton eal sh u n t ing. A recen t review
su p por t ing an eu r ysm coiling are th e op en -cell Neu roform sten t fou n d rough ly dou ble t h e n u m ber of com p licat ion s in sten t -
(St r yker Neu rovascular, Frem on t , CA) an d th e closed-cell En ter- assisted coiling of r upt ured versus un r upt ured an eu r ysm s (13%
prise stent (Codm an an d Shurtleff, Rayn ham , MA). In the closed- vs 6–7%).53 An oth er poten t ial con cern w ith th e use of sten ts in
cell design , all of th e sten t t in es are con n ected, th e sten t m oves th e basilar ar ter y is occlu sion of perforators or sm all bran ch ar-

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55 Endovascular Therapies for Basilar Artery Aneurysm s 641

a b

Fig. 55.2a–c (a) Preoperative Townes view of a large wide-neck basilar


apex aneurysm . (b) Two stents placed in a Y-stent configuration are seen
extending into the bilateral posterior cerebral arteries and the aneurysm
sac is coiled. (c) Postoperative Townes view dem onstrating obliteration of
c the aneurysm and preservation of the posterior cerebral arteries.

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642 V Cerebral and Spinal Aneurysms

a b

Fig. 55.3a,b (a) Midbasilar trunk dissecting aneurysm with previous coil em bolization and clear evidence of interval aneurysm growth. (b) Postoperative
vertebral artery angiogram dem onstrates obliteration of the residual aneurysm with Onyx HD-500 liquid em bolic.

teries. Although the porosit y of th e com m only used stents is h igh an d leading to st agn at ion an d th rom bosis w ith in a covered an -
w ith a low ratio of m etal com pared w ith the size of the interstices, eu r ysm , bu t p erm it t ing ongoing dem an d-based flow in to cov-
it is st ill possible th at a st ru t m ay cover over th e ost ium of a per- ered bran ch es an d p erforat ing ar teries. Th e t w o devices w ith th e
forator and acutely occlu de it , or th at occlusion m ay occur gradu- m ost clin ical experien ce are th e Pipelin e em bolizat ion device
ally as the sten t h eals in to th e paren t vessel w all an d is covered (ev3- Covidien ), curren tly Food an d Drug Adm in ist rat ion (FDA)
by en doth eliu m . Fin ally, as n oted in coron ar y an d oth er vessels in approved for an terior circulat ion an eur ysm s larger th an 10 m m
th e body, in t racran ial sten ts are at risk of develop ing in -sten t ste- an d proxim al to th e su perior hypop hyseal ar ter y, an d th e Silk
n osis, w hich can be m ore problem at ic in sm all vessels an d w h ile stent (Balt Extrusion, Montm orency, France), available in Europe.
rarely sym ptom at ic, th eir u se w arran ts ju d iciou s follow -up . Early exp erien ce w ith flow diver ters for gian t an d fu siform basi-
To address con cern s of in com plete an eu r ysm filling often lar ar ter y an eu r ysm s w as ver y en cou raging, w ith rep or ts of large
seen w ith coils, liqu id p olym ers h ave been develop ed th at con - lesion s th at h ad been cau sing brain stem com p ression an d w ere
form to the in terior sh ape of an eur ysm s an d com pletely fill th em , felt to be oth er w ise un safe to t reat able to be excluded w ith par-
t h e m ost w id ely u sed agen t bein g Onyx (ev3- Covid ien , Ir vin e, en t vessel recon st ru ct ion , an eu r ysm th rom bosis, an d regression
CA). Onyx is an ethylen e-vinyl alcoh ol co-polym er, an d a h igh an d im provem en t in clin ical sym ptom s 55 (Fig. 55.4). En th usiasm
viscosit y form u lat ion , Onyx HD-500, is design ed specifically for h as been tem pered by repor ts of delayed an eur ysm ru pt u re, pos-
use w ith in t racran ial an eur ysm s (Fig. 55.3). Th e use of Onyx re- sibly as a resu lt of m u ral destabilizat ion an d breakdow n of th e
qu ires a balloon rem odeling tech n iqu e, w ith th e deliver y cath e- an eur ysm w all, an d oth er repor t s of gradual occlusion of covered
ter position ed in side th e an eur ysm an d th e balloon in flated perforat ing ar teries w ith brain stem isch em ia.56 In addit ion , th e
across the n eck to preven t reflu x of th e liquid em bolic agen t in to u se of flow diverters requ ires dual an t iplatelet m edicat ion s, an d
th e paren t ar ter y. Th e advan tages of th e use of Onyx in clu de th e the delayed nat ure of aneurysm th rom bosis w ith perm issive flow
abilit y to com pletely fill com plex or m ult ilobed an eur ysm s, such th rough th e sten t to areas of dem an d fu r th er lim it s th eir u t ilit y
as m ay be foun d at th e basilar apex or n ear bifurcat ion s, an d in th e set t ing of SAH. Given th e h igh rates of m orbidit y an d m or-
sm all but w ide-n ecked an eu r ysm s, as m ay be fou n d along th e talit y w ith both th e n at ural h istor y an d conven t ion al t reat m en ts
basilar t run k. In addit ion , Onyx m ay be useful for t reat ing recur- for gian t an d fu sifor m basilar an eu r ysm s, flow d iver ters m ay
ren t an eur ysm s or n eck rem n an t s after coiling, as th e liquid can prove to be th e best opt ion for cer tain pat ien ts, bu t th e risks an d
in sin u ate arou n d th e coils, an d it h as been fou n d to be a du rable ben efits of th eir u se m u st be assessed on a case-by-case basis.
t reat m en t .54 Draw backs w ith th e use of liquid polym ers are th e More lon g-ter m dat a an d exp er ien ce are n eed ed before t h eir
requ irem en t for an t ip latelet m ed icat ion s, t h e long t reat m en t rout in e use.
t im es an d isch em ic risk w ith balloon in flat ion , th e risk of reflu x
of th e agen t in to th e paren t arter y w ith n arrow ing or dist al em -
boli, an d th e relat ive paucit y of experien ce an d long-term data
regarding outcom e.
■ Endovascular Technique
Flow -d iver t in g sten t s d iffer from ot h er in t racran ial sten t s Th e en dovascu lar tech n iqu e em p loyed m u st be t ailored to th e
by h aving m uch low er p orosit y, favoring in t ralu m in al blood flow clin ical sit u at ion , in clu ding r u pt u re st at u s of th e an eu r ysm , th e

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55 Endovascular Therapies for Basilar Artery Aneurysm s 643

a b

Fig. 55.4a–c (a) Preoperative lateral angiogram dem onstrates a large fu-
siform basilar artery aneurysm in a patient who presented with symptom s
of m ass effect on the brainstem . (b) Following placem ent of a flow di-
verter, st agnation of contrast is seen in the aneurysm sac in the late venous
phase of the angiogram. (c) The follow-up DynaCT of the flow diverter in
the basilar artery at the skull base shows patency of the basilar artery and
c stent with m inim al residual filling of the aneurysm.

intended approach (constructive or deconstructive), and the local is in ser ted , an d system ic h ep ar in is ad m in istered , t yp ically a
equ ip m en t an d exper t ise available. Th e follow ing gen eral gu ide- 5,000-u n it IV bolu s in u n r u pt u red cases. For r u pt u red cases
lin es reflect ou r p referen ces in m ost cases, bu t can be easily w it h SAH, a low er dose of h eparin is used, an d u sually given on ce
adapted to fit a w ide variet y of clin ical n eeds. th e first coils are in side th e an eu r ysm . In t raop erat ive m on itoring
For any u n ru pt u red an eu r ysm s w h ere th e p ossibilit y of u sing of coagu lat ion st at u s is assessed 10 m in u tes later w it h p oin t -
a sten t is an t icipated by preoperat ive im aging, pat ien ts are pre- of-care test ing (VerifyNow, Accum et rics, San Diego, CA) for act i-
m edicated th e day before th e procedure w ith dual an t iplatelet vated clot t ing t im e (ACT), P2Y12 in h ibit ion for clopidogrel effi-
m ed icat ion s, u su ally 325 m g of asp ir in an d 600 m g of clop id o - cacy, an d ARUs for aspirin effect an d re-bolused as n eeded to
grel (su bst it u ted for allergies as n eed ed), an d m ain t ain ed on reach t h erap eu t ic levels (ACT > 250, P2Y12 in h ibit ion > 20%,
81 m g of aspirin an d 75 m g of clopidogrel th e m orn ing of th e ARU < 550). If a pat ien t is fully resist an t to aspirin or clopidogrel,
procedu re. Gen eral an esth esia w ith stan dard m on itoring in clu d- an oth er an t iplatelet is st ar ted. In pat ien ts w ith un com plicated
in g a radial ar ter ial lin e is u sed . A 6-Fren ch (F) fem oral sh eat h an atom y, a 6F gu id e cat h eter (su ch as MPD Envoy ® , Cord is,

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644 V Cerebral and Spinal Aneurysms

Miam i, FL) an d a 0.035-in ch w ire are t h en advan ced to th e ca-


rot id arteries, an d DSA im ages are obtain ed to assess collateral
■ Patient Outcomes
blood flow an d any oth er in t racran ial lesion s before select ing th e Th e goals of t reat m en t of basilar ar ter y an eur ysm s are com plete
larger ver tebral ar ter y, as iden t ified from p reoperat ive im aging, occlusion of th e lesion , preven t ion of rupt u re, an d ach ieving a
to obt ain biplan e an d 3D rotat ion al DSA im ages of th e lesion . In good clin ical an d n eurologic outcom e for th e pat ien t. Th ere are
pat ien ts w ith difficu lt aort ic arch es or tor t u ou s an atom y, an ap - m any factors th at in fluen ce th ese outcom es, in cluding an eur ysm
propriate 5F select ion cath eter (su ch as an angled Glide, H-1, or size, t yp e, n eck dim en sion s, an d ru pt u re st at u s. Com paring th e
Sim m on s 2) is u sed to obtain th e diagn ost ic im ages an d th en ex- m erits of differen t t reat m en t s can be difficu lt am ong h eteroge-
ch anged over a long w ire for a 6F gu ide in to th e larger ver tebral neous population s. Results from t w o large random ized controlled
ar ter y. t rials com p aring op en su rger y w ith en dovascu lar t reat m en t of
Im ages of th e an eu r ysm are t h en an alyzed on t h e w orkst a- rupt ured an eu r ysm s, th e In tern at ion al Subarach n oid An eur ysm
t ion for size, orien t at ion , an d n eck t ype, an d an opt im al w orking Trial (ISAT) an d th e Barrow Ru pt u red An eu r ysm Trial (BRAT),
angle is determ in ed. If a single sten t is to be placed, dist al an d both foun d th at 10%few er pat ien t s died or becam e depen den t in
proxim al lan ding zon es are iden t ified, n ecessar y length an d di- th e en d ovascu lar grou p , alth ough th ey did n ot st rat ify th e resu lt
am eter are m easured, an d a vir t ual sten t can be draw n to ap - by an eu r ysm locat ion , an d on ly 3% an d 15% of lesion s in th ese
proxim ate th e desired p osit ion ing. A m agn ified angiogram u sing t rials, resp ect ively, w ere in th e posterior circulat ion .57,58
t h e d esired w orkin g an gle is t h en sh ot an d referen ced , an d a As th ere are n o oth er ran dom ized con t rolled t rials or direct
roadm ap im age is acqu ired . For cases of p rim ar y coiling, a m icro- com parison s of op en versu s en dovascu lar t reat m en t of basilar
cath eter is n avigated by th e assist an ce of a 0.010- or 0.014-in ch an eur ysm s, th e rem ain ing eviden ce is based on com parison s of
m icrow ire in to th e an eur ysm , th e w ire is rem oved, an d coils of h istor ical resu lt s from single or m u lt icen ter ser ies. Th e largest
appropriate size, as determ in ed by th e previous m easurem en ts, su rgical series, rep or ted by Peerless an d colleagu es,59 fou n d an
are delivered to occlude th e an eur ysm . If vessel sacrifice is th e overall m orbidit y of 25%an d m ortalit y of 8%for all basilar an eu-
plan n ed t reat m en t , th e m icrocath eter is p osit ion ed in a sim ilar r ysm s t reated. Th is st udy cites in creasing rates of m orbidit y an d
fash ion but th e t ip rem ain s w ith in th e desired vessel. Ideally th e m ortalit y based on an eur ysm size, from 13%for sm all, to 25%for
sacr ifice locat ion w ill be d ist al to im p or t an t bran ch es, m ost large, to 42%for gian t lesion s. Th ese n u m bers are con sisten t w ith
com m on ly t h e or igin of t h e PICA, w it h coils d elivered carefu lly oth er h istorical surgical series, up to a 1999 report from Sam son
to avoid bran ch occlu sion . et al,60 w h o fou n d 17% m orbid it y an d 7% m or t alit y at t h e t im e
For cases of sten t-assisted coiling, a t riden t-t ype valve is u sed of h ospit al disch arge an d 10% m orbidit y an d 9% m or talit y at 6
w ith th e guide cath eter to allow t w o m icrocath eters to be in t ro- m on ths for pat ien ts w ith open operat ion s for basilar an eur ysm s.
du ced sim u ltan eou sly an d n avigated in to posit ion . Th e m icro- Th is group also fou n d in creased m orbidit y, up to 40%, w ith larger
cath eter th at w ill deliver th e coils m ay first be posit ion ed in side an eur ysm s, an d a 6% rate of residual an eur ysm or n eck rem n an t
th e an eur ysm , an d th en th e sten t dep loyed across it , jailing it in on follow -u p. In con t rast , t w o review s of en dovascular m an age-
place. Th is obviates th e n eed for crossing th e t in es of th e sten t m en t of basilar arter y an eur ysm s w ith coiling alon e foun d m or-
an d m ay provide a m ore st able posit ion , but requires dragging bidit y (3–9%) and m ortalit y (3–9%) rates that com pared favorably
th e m icrocath eter ou t again st th e vessel w all at th e en d of th e w ith open surgical t reat m en t . More recen t series th at in clude
coiling an d m ay be a difficu lt in it ial posit ion to ach ieve. Alter- sten t assist an ce h ave sim ilar com plicat ion rates.27,29,61 How ever,
n ately, the sten t m ay first be dep loyed an d th en th e coiling m i- t h e n u m ber of an eu r ysm s t h at are occlu d ed > 90% ran ge from
crocath eter n avigated th rough it in to th e an eur ysm ; th is n egates 78 to 90%, w ith part ial recan alizat ion seen in up to 25% of cases
th e n eed for sim u lt an eou s m icrocath eters, bu t crossing th e t in es an d 5 to 10% requiring ret reat m en t . Risks for subtotal occlusion
of th e sten t can som et im es be ch allenging. If Y-sten t ing is re- an d recan alizat ion in clude rupt ured lesion s, in creased size, w ide
quired to rem odel the neck, th e m ore difficult PCA is accessed and n ecks, an d com plex geom et r y in cluding fusiform sh ape. Th e rate
an open -cell sten t is delivered first , an d th en th e con t ralateral of recu r ren t SAH from coiled an eu r ysm s is low , bet w een 0.2%
PCA is accessed th rough th e t in es of th e first sten t an d a secon d an d 0.8%, bu t h igh er t h an t h at from p reviou sly clip ped an eu -
open - or closed-cell sten t is delivered. Th e m icrocath eter is th en r ysm s in th e long-term follow -u p from ISAT.27,62
reposit ion ed in sid e th e an eu r ysm an d coils are delivered. For th e More recen t series, an d th ose th at h ave an alyzed single-in st i-
balloon -rem odeling tech n ique, t w o m icrocath eters are required, t ution dat a over an exten ded t im e period, h ave foun d low er rates
w ith th e first jailed w ith in th e an eur ysm an d th e secon d used to of m orbidit y an d m or talit y an d in creased rates of com plete oc-
posit ion an d in flate th e balloon . Usu ally a con form able balloon clusion over t im e, likely reflect ing im p rovem en ts in tech n ology,
su ch as th e Hyp erForm (ev3- Covidien ) is u sed, as it is able to adju n ct ive devices, an d operator experien ce. A m ajor difficu lt y
adju st to th e an atom y an d accoun ts for irregular sh apes, in clud- in in terpret ing th e resu lt s of m any series is th e in clusion of both
ing bifu rcat ion s, allow ing deliver y of coils w ith out h ern iat ion rupt ured an d un r upt ured an eur ysm s togeth er, as th e goal of
in to th e paren t vessel du ring in flat ion . W h en a sat isfactor y coil- t reat m en t in th e form er is often ju st dom e p rotect ion for sh or t-
ing resu lt h as been ach ieved, fin al m agn ified (w orking view ) an d term preven t ion of rerupt u re. In th e set t ing of rupt u re, sten t as-
n on m agnified (stan dard biplan e view s) DSA r un s are recorded. sistan ce is relat ively con t rain dicated, so p acking den sities w ou ld
Th e cat h eter an d sh eath are rem oved an d th e groin site is closed, tend to be low er. Th is w ould lead to h igh er rates of recan aliza-
eith er w ith m an u al com p ression or a closu re device. We p refer a t ion an d ret reat m en t in th is grou p of pat ien ts, w h ich , if view ed
polyp ropylen e su t u re device as it allow s im m ediate reaccess to as st aged t h erapy an d p er for m ed w it h low com p licat ion s an d
th e sam e groin if an oth er angiogram or en dovascu lar p rocedu re low reh em orrh age rates, m ay be m ore desirable th an a h igh -risk
m u st be perform ed. t reat m en t w ith th e goal of com plete occlu sion u pfron t .

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55 Endovascular Therapies for Basilar Artery Aneurysm s 645

lin e t reat m en t in ligh t of it s favorable m orbidit y an d m or t alit y


■ Conclusion rates com bined w ith acceptable rates of aneurysm occlusion. How -
Basilar ar ter y an eu r ysm s, alth ough less com m on th an th ose of ever, given th e risk of an eur ysm recurren ce, judicious follow -up
th e an terior circu lat ion , p resen t u n iqu e ch allenges as a resu lt of is requ ired, an d ret reat m en t sh ou ld be perform ed for sign ifican t
th eir an atom y an d m orp h ology. Th e difficu lt y of surgical access residu al or regrow th . Ver y large, gian t , an d fusiform basilar ar-
to th is area an d th e risk of perforat ing ar ter y inju r y h elped in - ter y an eur ysm s m ay involve a separate path ophysiology from
spire th e developm en t of en dovascular t reat m en ts for th ese le- oth er lesion s in th is area, carr y a h igh er risk both in n at ural h is-
sions. Progress in adjun ctive techniques, in cluding self-expan ding tor y an d w it h t reat m en t , an d requ ire sp ecial con siderat ion for
sten t s, h as dram at ically in creased th e abilit y to t reat basilar an - opt im al m an agem en t .
eu r ysm s. In m any in st it u t ion s, en dovascu lar th erapy is th e first-

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surg 2001;94:712–717 coil em bolizat ion of posterior circu lat ion an eu r ysm s: a system at ic review
11. Ducruet AF, Hickm an ZL, Zacharia BE, et al. In t racran ial in fect ious an eu- of th e literat u re. St roke 2002;33:2509–2518
r ysm s: a com preh en sive review. Neu rosurg Rev 2010;33:37–46 28. Mordasin i P, Sch roth G, Gu zm an R, Bar th A, Seiler RW, Rem onda L. En do-
12. W iebers DO, W h isn an t JP, Hu ston J III, et al; In tern at ion al St u dy of Un - vascu lar t reat m en t of p osterior circu lat ion cerebral an eu r ysm s by u sing
r u pt ured In t racran ial An eur ysm s Invest igators. Un rupt ured in t racran ial Guglielm i det ach able coils: a 10-year single-cen ter experience w ith spe-
an eur ysm s: n at ural h istor y, clin ical outcom e, and risks of surgical and cial regard to tech n ical developm en t . AJNR Am J Neu roradiol 2005;26:
en dovascular t reat m en t . Lan cet 2003;362:103–110 1732–1738
13. Werm er MJ, van der Schaaf IC, Algra A, Rin kel GJ. Risk of rupt ure of un ru p - 29. Pan dey AS, Koebbe C, Rosenw asser RH, Vezn edaroglu E. En dovascular coil
t u red in t racran ial an eu r ysm s in relat ion to p at ien t an d an eu r ysm ch arac- em bolizat ion of rupt ured an d un rupt ured posterior circulat ion an eu-
terist ics: an updated m et a-an alysis. St roke 2007;38:1404–1410 r ysm s: review of a 10-year experien ce. Neu rosurger y 2007;60:626–636,
14. Ish ibash i T, Murayam a Y, Urash im a M, et al. Un rupt ured in t racran ial an - discu ssion 636–637
eur ysm s: in ciden ce of rupt ure and risk factors. St roke 2009;40:313–316 30. Peluso JP, van Rooij W J, Slu zew ski M, Beute GN. Coiling of basilar t ip an eu-
15. Naidech AM, Janjua N, Kreiter KT, et al. Predictors an d im pact of an eur ysm r ysm s: result s in 154 con secut ive pat ient s w ith em ph asis on recurren t
rebleeding after subarachnoid hem orrhage. Arch Neurol 2005;62:410–416 h aem orrh age an d re-t reat m en t during m id- an d long-term follow -up.
16. Ph illips TJ, Dow ling RJ, Yan B, Laidlaw JD, Mitch ell PJ. Does t reat m en t of J Neu rol Neu rosu rg Psych iat r y 2008;79:706–711
r u pt u red in t racran ial an eu r ysm s w ith in 24 h ou rs im p rove clin ical ou t- 31. Kassell NF, Torn er JC, Haley EC Jr, Jane JA, Adam s HP, Kongable GL. Th e In -
com e? St roke 2011;42:1936–1945 tern at ion al Cooperat ive St udy on th e Tim ing of An eur ysm Surger y. Par t 1:
17. Sch ievin k W I, Wijdicks EF, Piepgras DG, Ch u CP, O’Fallon W M, W h isn an t Overall m an agem en t result s. J Neurosurg 1990;73:18–36
JP. Th e p oor p rogn osis of r u pt u red in t racran ial an eu r ysm s of th e posterior 32. Debr un GM, Alet ich VA, Keh rli P, Misra M, Ausm an JI, Ch arbel F. Select ion
circulat ion . J Neurosurg 1995;82:791–795 of cerebral an eur ysm s for t reat m en t using Guglielm i det ach able coils: the
18. Yam au ra I, Tani E, Yokot a M, et al. En dovascular t reat m en t of rupt ured prelim in ar y Un iversit y of Illin ois at Ch icago exp erien ce. Neu rosu rger y
dissect ing an eu r ysm s aim ed at occlu sion of th e dissected site by u sing 1998;43:1281–1295, discussion 1296–1297
Guglielm i det ach able coils. J Neu rosurg 1999;90:853–856 33. Fer n an d ez Zu billaga A, Guglielm i G, Viñ u ela F, Du ckw iler GR. En d ovas-
19. Hanel RA, Boulos AS, Sauvageau EG, Levy EI, Guterm an LR, Hopkin s LN. cu lar occlusion of in t racran ial an eur ysm s w ith elect rically det ach able
Sten t placem en t for th e t reat m en t of n on saccular an eur ysm s of th e verte- coils: correlat ion of an eur ysm n eck size an d t reat m en t resu lt s. AJNR Am J
brobasilar system . Neurosurg Focus 2005;18:E8 Neuroradiol 1994;15:815–820
20. Mangrum W I, Huston J III, Lin k MJ, et al. En larging ver tebrobasilar n on - 34. Horst m an P, Lin n FH, Voorbij HA, Rin kel GJ. Chan ce of an eur ysm in pa-
saccular in t racran ial aneur ysm s: frequen cy, predictors, an d clin ical out- t ien t s suspected of SAH w h o have a “n egat ive” CT scan but a “posit ive”
com e of grow th . J Neu rosurg 2005;102:72–79 lum bar pun ct ure. J Neurol 2012;259:649–652

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35. Cr uicksh ank A, Auld P, Beeth am R, et al; UK NEQAS Specialist Advisor y 49. Higashida RT, Sm ith W, Gress D, et al. In t ravascular sten t an d en dovascu-
Grou p for Extern al Qu alit y Assuran ce of CSF Protein s an d Bioch em ist r y. lar coil placem en t for a r upt ured fusiform an eur ysm of th e basilar ar ter y.
Revised n at ion al gu idelin es for an alysis of cerebrosp in al flu id for biliru bin Case rep or t an d review of th e literat u re. J Neu rosu rg 1997;87:944–949
in suspected subarachnoid haem orrhage. Ann Clin Biochem 2008;45(Pt 3): 50. Ch ow MM, Woo HH, Masar yk TJ, Rasm ussen PA. A novel endovascular
238–244 t reat m en t of a w ide-n ecked basilar apex an eur ysm by using a Y-con figu-
36. Kapsalaki EZ, Roun t as CD, Foun t as KN. Th e role of 3 tesla MRA in th e de- rat ion , dou ble-sten t techn ique. AJNR Am J Neuroradiol 2004;25:509–512
tect ion of in t racran ial an eur ysm s. In t J Vasc Med 2012;2012:792834 51. Fargen KM, Mocco J, Neal D, et al. A m u lt icen ter st udy of sten t-assisted
37. Miley JT, Taylor RA, Jan ardh an V, Tum m ala R, Lan zin o G, Quresh i AI. Th e coiling of cerebral an eu r ysm s w ith a Y con figu rat ion. Neurosurger y 2013;
valu e of com p u ted tom ography angiograp hy in determ in ing t reat m en t al- 73:466–472
locat ion for an eur ysm al su barach n oid h em orrh age. Neu rocrit Care 2008; 52. Wan ke I, Gizew ski E, Forst ing M. Horizon t al sten t placem en t plus coiling
9:300–306 in a broad-based basilar-t ip an eur ysm : an altern at ive to th e Y-sten t tech -
38. Xing W, Ch en W, Sheng J, et al. Sixt y-four-row m ult islice com puted tom o- n ique. Neuroradiology 2006;48:817–820
graph ic angiography in the diagn osis an d ch aracterizat ion of in t racran ial 53. Bodily KD, Cloft HJ, Lan zin o G, Fiorella DJ, W h ite PM, Kallm es DF. Sten t-
an eur ysm s: com parison w ith 3D rot at ion al angiography. World Neuro- assisted coiling in acu tely ru pt u red in t racran ial an eu r ysm s: a qu alit at ive,
su rg 2011;76:105–113 system at ic review of t h e literat u re. AJNR Am J Neu rorad iol 2011;32:
39. Serbin en ko FA. Balloon cath eterizat ion an d occlusion of m ajor cerebral 1232–1236
vessels. J Neu rosu rg 1974;41:125–145 54. Dalyai RT, Ran dazzo C, Gh obrial G, et al. Redefin ing Onyx HD 500 in th e
40. Higashida RT, Halbach VV, Cah an LD, Hiesh im a GB, Kon ish i Y. Det ach able flow diversion era. Int J Vasc Med 2012;2012:435490
balloon em bolizat ion th erapy of posterior circulat ion in t racran ial an eu- 55. Fiorella D, Kelly ME, Albuquerque FC, Nelson PK. Curat ive recon st ruct ion
r ysm s. J Neu rosurg 1989;71:512–519 of a giant m idbasilar t r un k an eur ysm w ith th e pipelin e em bolizat ion de-
41. Hodes JE, Aym ard A, Gobin YP, et al. En dovascu lar occlu sion of in t racra- vice. Neurosurger y 2009;64:212–217, discussion 217
n ial vessels for cu rat ive t reat m en t of un clippable aneur ysm s: repor t of 16 56. Siddiqui AH, Abla AA, Kan P, et al. Pan acea or problem : flow diver ters
cases. J Neurosurg 1991;75:694–701 in th e t reat m en t of sym ptom at ic large or gian t fusiform vertebrobasilar
42. Hart m ann A, Con olly ES, Duong DH, et al. Dysarth ria during basilar arter y an eur ysm s. J Neurosurg 2012;116:1258–1266
balloon occlusion . Neu rology 1999;53:421–423 57. McDougall CG, Sp et zler RF, Zabram ski JM, et al. Th e Bar row Ru pt u red
43. Pisapia JM, Walcot t BP, Nah ed BV, Kah le KT, Ogilvy CS. Cerebral revascu- An eu r ysm Trial. J Neu rosu rg 2012;116:135–144
larizat ion for th e t reat m en t of com p lex in t racran ial an eu r ysm s of th e 58. Molyn eu x A, Kerr R, St rat ton I, et al; In tern at ion al Subarach n oid An eu-
posterior circulat ion : m icrosu rgical an atom y, tech n iqu es an d outcom es. r ysm Trial (ISAT) Collaborat ive Group. In tern at ion al Subarach n oid An eu-
J Neu roin ter v Su rg 2011;3:249–254 r ysm Trial (ISAT) of neu rosurgical clipping versus en dovascular coiling in
44. Guglielm i G, Viñ uela F, Sepetka I, Macellari V. Elect roth rom bosis of sac- 2143 pat ien t s w ith ru pt u red in t racran ial an eur ysm s: a ran dom ised t rial.
cular aneurysm s via endovascular approach. Part 1: Electrochem ical basis, Lan cet 2002;360:1267–1274
tech nique, an d experim en t al result s. J Neurosurg 1991;75:1–7 59. Peerless SJ, Jern esniem i JA, Gu t m an , FB, Drake CG. Early su rger y for ru p -
45. Lefkow it z MA, Gobin YP, Akiba Y, et al. Balloon -assisted Guglielm i det ach - t ured ver tebrobasilar aneu r ysm s. J Neu rosurg 1994;80(4):643–649.
able coiling of w ide-n ecked an eur ysm s: par t II—clin ical resu lt s. Neu ro- 60. Sam son D, Batjer HH, Kopit n ik TA Jr. Curren t resu lt s of th e su rgical m an -
surger y 1999;45:531–537, discu ssion 537–538 agem en t of an eur ysm s of th e basilar apex. Neurosu rger y 1999;44:697–
46. Moret J, Cogn ard C, Weill A, Cast aings L, Rey A. Th e “rem odelling tech - 702, d iscu ssion 702–704
n iqu e” in t h e t reat m en t of w id e n eck in t racran ial an eu r ysm s. An gio - 61. Gr uber DP, Zim m erm an GA, Tom sick TA, van Loveren HR, Lin k MJ, Tew JM
grap h ic resu lt s an d clin ical follow -u p in 56 cases. In ter v Neu rorad iol Jr. A com parison bet w een en dovascu lar an d su rgical m an agem en t of basi-
1997;3:21–35 lar ar ter y ap ex an eu r ysm s. J Neu rosu rg 1999;90:868–874
47. Fiorella D, Woo HH. Balloon assisted t reat m en t of in t racran ial an eur ysm s: 62. Molyn eu x AJ, Kerr RS, Birks J, et al; ISAT Collaborators. Risk of recurren t
th e conglom erate coil m ass tech n iqu e. J Neu roin ter v Su rg 2009;1:121– subarachn oid h aem orrh age, death , or dependen ce an d st andardised m or-
131 t alit y rat ios after clipping or coiling of an in t racran ial an eur ysm in th e
48. Fiorella D, Kelly ME, Moskow it z S, Masar yk TJ. Delayed sym ptom at ic coil In tern at ion al Su barach n oid An eu r ysm Trial (ISAT): long-term follow -u p .
m igrat ion after in it ially successful balloon -assisted an eur ysm coiling: Lan cet Neurol 2009;8:427–433
technical case report. Neurosurger y 2009;64:E391–E392, discussion E392

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56 Surgical Therapies for Vertebral
Artery and Posterior Inferior
Cerebellar Artery Aneurysms
Ana Rodríguez-Hernández, Mat thew B. Pot t s, and Michael T. Law ton

Th e p oster ior circu lat ion h arbors 15 to 18% of all in t racran ial u llar y, th e p4 or teloveloton sillar segm en t , an d th e p5 or cor t ical
an eur ysm s,1 w ith th e vast m ajorit y of th em at th e basilar ar ter y segm en t (Fig. 56.1). Th e an terior m edullar y (p1) segm en t begin s
ap ex. Th e poster ior in fer ior cerebellar ar ter y (PICA) an d t h e at th e PICA’s origin , lies an terior to th e m edu lla, an d exten ds past
in t rad u ral segm en t of t h e ver tebral ar ter y (VA) are th e p aren t th e hyp oglossal rootlet s at t h e m edial edge of th e in ferior olive.
ar ter ies of 18 to 20% of in fraten tor ial an eu r ysm s, m akin g t h em Th e lateral m edu llar y (p2) segm en t is a sh or t segm en t th at ex-
t h e m ost frequ en t locat ion after th e basilar apex. VA an eu r ysm s ten ds from th e olive to th e rootlets of cran ial n er ves (CNs) IX, X,
can be located dist al or p roxim al to th e PICA origin or, m ore com - an d XI at th e lateral edge of th e olive. Th e ton sillom edullar y (p3)
m on ly, in corporate th e VA-PICA bifu rcat ion . PICA an eur ysm s can segm en t begin s w h ere th e PICA p asses u n d er or bet w een th e
arise at th e PICA origin or, n ot in frequ en tly, at a dist al locat ion root let s of t h e CN IX to XI t r iad , d escen d s to t h e in fer ior p ole of
along th e p 2 to p5 segm en ts of th e ar ter y. Th is ch apter discu sses th e cerebellar ton sil, reverses cou rse in t h e cau dal or in fraton -
t h e m icrosu rgical an atom y, clin ical p resen t at ion , p reop erat ive sillar loop , an d ascen d s along t h e m ed ial ton sil to it s m id p oin t .
evalu at ion , m an agem en t opt ion s, an d su rgical tech n iqu es for Th e teloveloton sillar (p4) segm en t begin s at th e m idp oin t of th e
th ese lesion s. PICA’s ascen t along th e m edial ton sil, con t in u es tow ard th e roof
of th e four th ven t ricle, t urn s aroun d again to form a cran ial or
supratonsillar loop, and courses dow nw ard and posteriorly to the
ton sillobiven t ral fissure. Th e teloveloton sillar segm en t derives
■ Microsurgical Anatomy its n am e from its bran ch es to th e ch oroid plexus of th e four th
ven t r icle (tela ch oroid ea) an d it s associat ion w it h t h e roof of
Th e ver tebral ar ter y can be con cept u ally divided in to fou r seg-
th e four th ven t ricle (in ferior m edu llar y velum ). Th e cor t ical (p5)
m en t s. Th e V1 or ext raosseous segm en t courses posterosuperi-
segm en t begin s as th e PICA em erges from th e ton sillobiven t ral
orly from its origin from th e su bclavian ar ter y to it s en t ran ce
fissu re w h ere th e ton sil, verm is, an d biven t ral lobu le of th e cer-
in to th e t ran sverse foram en of C6. Th e V2 or foram in al segm en t
ebellar h em isph ere m eet . Th is segm en t con sist s of n um erous
t ravels from C6 to C1 w ith in th e t ran sverse foram in a of th e six
t ru n ks an d bran ch es, w ith a m ed ial t r u n k su pp lying th e verm ian
u pp er cer vical ver tebrae. Th e V3 or su boccip ital segm en t begin s
su r face an d a lateral t r u n k su p p lying t h e ton sillar an d h em i-
as th e VA em erges from th e t ran sverse foram in a of C1, cu r ves
sph eric su rfaces.
backw ard arou n d th e atlan to-occipit al join t to car ve a h orizon t al
Th e an ter ior sp in al ar ter y is t h e last VA bran ch p roxim al to
groove in t h e p oster ior arch of C1 (ver tebral su lcu s or su lcu s
th e VBJ. It join s t h e con t ralateral ar ter y to form a single m idlin e
ar teriosus), an d ben ds m edially an d superiorly to en ter th e skull
an terior sp in al ar ter y t h at d escen d s t h rough t h e foram en m ag-
through th e foram en m agn um right beh ind the occipital condyle.
n u m on th e ven t ral su r face of th e m edu lla an d spin al cord in or
Fin ally, th e V4 or in t radu ral segm en t exten ds from th e low er lat-
n ear th e an terior m edian fissu re. It su pp lies th e pyram ids an d
eral to th e u pp er an terior su rface of th e m edu lla, giving off m ed-
th eir decu ssat ion , th e m edial lem n iscu s, an d th e hyp oglossal
u llar y perforators along th e w ay. In it ially it passes over th e roots
n u clei an d n er ves.
of th e first cer vical n er ve, an d crosses an terior to th e den tate
ligam en t an d th e sp in al p or t ion of th e accessor y n er ve. Later, it
passes across th e pyram id, join s th e con t ralateral V4 at or n ear
th e p on tom edu llar y su lcu s, an d form s th e ver tebrobasilar ju n c-
Anatomic Triangles
t ion (VBJ) an d basilar ar ter y. Th e surgical anatom y of this particular region can be concept ual-
Th e posterior sp in al ar ter y is th e first in t racran ial bran ch ized in th ree an atom ic t riangles th at clarify th e dissect ion routes
from th e VA, alth ough it som et im es arises ext radu rally an d t rav- to PICA an eur ysm s 2,5 : th e vagoaccessor y t riangle, th e su prahy-
els w ith th e VA th rough th e du ral ring in to th e su barach n oid poglossal t riangle, an d th e in frahypoglossal t riangle (Fig. 56.2a).
space. Th e posterior spin al ar ter y courses m edially beh in d th e Th e vagoaccessor y t riangle is defin ed by th e vagu s n er ve su p eri-
den tate ligam en t an d bran ch es in to ascen ding an d descen ding orly, th e accessor y n er ve laterally, an d th e m edulla m edially. Th is
ar teries th at supply dorsal colu m n s an d por t ion s of dorsal cer vi- t r ian gle is t h e n at u ral w orkin g w in d ow for t h e far-lateral ap -
cal sp in al cord. proach . It is divid ed in to t w o sm aller t riangles by th e hypoglossal
Th e PICA is th e n ext , th e largest , an d th e m ost clin ically sig- n er ve. Th e suprahypoglossal t riangle is th e area in th e vagoac-
n ifican t bran ch . It h as five segm en t s defin ed by its relat ion sh ip cessor y t riangle above th e hypoglossal n er ve, bet w een CNs X, XI,
to low er cran ial n er ves as it w in ds aroun d th e m edu lla an d th e an d XII. Th e in frahypoglossal t r iangle is t h e area below t h e hy-
posterior su rface of th e cerebellu m 2–4 : th e p1 or an terior m edu l- p oglossal n er ve, bet w een CNs XI an d XII an d t h e m ed u lla. Th e
lar y segm en t , th e p 2 or lateral m edullar y, th e p 3 or ton sillom ed- glossopharyngeal, vagus, and accessor y ner ves originate from th e

647

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648 V Cerebral and Spinal Aneurysms

Fig. 56.1a,b Microsurgical anatomy of the posterior inferior


cerebellar artery (PICA). Lateral (a) and posterior (b) views of
PICA segm ent s and their relationship to the m edulla, lower
cranial nerves, and cerebellum . ASA, anterior spinal artery; BA, b
basilar artery; VA, vertebral artery; Vent., ventricle.

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 649

a b

Fig. 56.2a,b Anatom ic triangles and m edullary zones for posterior infe- tery (VA) can m ove the aneurysm into the anterior m edullary zone (aneu-
rior cerebellar artery (PICA) aneurysm s. (a) Three anatom ic triangles are rysm A), the lateral m edullary zone (aneurysm B), or the tonsillom edullary
defined by the lower cranial nerves as exposed by the far-lateral approach: zone (aneurysm C). Distal PICA aneurysm s are usually not involved in the
the vagoaccessory triangle, the suprahypoglossal triangle (SHT), and the lower cranial nerves (aneurysm D). BA, basilar artery; Ch. Pl., choroid plexus.
infrahypoglossal triangle (IHT). (b) The PICA origin along the vertebral ar-

ret ro-olivar y su lcus an d course to th e jugular foram en , w h ereas


th e hyp oglossal n er ve origin ates from th e preolivar y su lcu s an d
■ Pathophysiology and Natural History
cou rses to th e hyp oglossal foram en . Con sequ en tly, th e course Nat u ral h istor y st u dies h ave dem on st rated th at posterior circu -
an d depth of th e hypoglossal n er ve differs from th at of th e vagus lat ion an eu r ysm s h ave a h igh er risk of r u pt u re an d a h igh er as-
an d accessor y n er ves. As a result , th e supra- an d in frahypoglos- sociated m ortalit y than their anterior circulation coun terparts.6–8
sal areas are n ot sim ple, t w o-d im en sion al t riangles, bu t rath er An eu r ysm s arising from th e cerebellar ar teries, esp ecially th e
are th ree-dim en sion al corridors. Non eth eless, th ese corridors are PICA, are at yp ical, w ith an in creased in ciden ce of fusiform or
easiest to con cept u alize as t riangles. dolich oect at ic m orph ology, m ult iple lobu lat ion s, an d a dist al lo-
Alth ough th e an atom ic t riangles defin e th e surgical corridors cat ion beyon d t h e ar terial origin .4 Th ese at ypical feat u res h ave
to PICA an eu r ysm s, t h e m ed u llar y zon es d efin e h ow d eep an been im p licated in th e h igh er r u pt u re r isks, esp ecially m u lt i-
an eu r ysm lies w ith in th at su rgical corridor.2,5 Th ese m edullar y lobulat ion s an d daugh ter sacs. Fusiform m orph ology an d a dist al
zon es h ave th e sam e boun daries th at defin e th e PICA’s early seg- locat ion m ay or m ay n ot be associated w ith an in creased risk of
m en t s, n am ely th e preolivar y an d ret ro-olivar y su lci. Th e t h ree rupt ure, but th ey suggest th at th e h em odyn am ics of posterior
zon es are sim ilarly referred to as th e an terior m edullar y zon e, circulat ion an eur ysm s are differen t from th ose of an terior circu -
th e lateral m edu llar y zon e, an d th e ton sillom edu llar y zon e (Fig. lat ion an eu r ysm s. Based on com put at ion al flu id dyn am ics, tor-
56.2b). An eur ysm s in th e an terior m edullar y zon e are deep to all t uous arteries like th e PICA h ave com plex flow s w ith h igh w all
th e low er cran ial n er ves; an eu r ysm s in th e lateral m edu llar y sh ear st ress, t u rbu len ce, an d p ressure variat ion s th at m igh t lead
zon e are on ly deep to CNs IX, X, an d XI; an eu r ysm s in th e lateral to an eur ysm form at ion . Th ese st udies also dem on st rate jets of
m edu llar y zon e are su p erficial to th e low er cran ial n er ves. Vari- in flow im pinging on th e an eur ysm dom e w ith h igh sh ear st ress,
abilit y in t h e origin of t h e PICA from t h e VA, t h e tor t u osit y of suggest ing a m ech an ism of ru pt ure.
th e paren t ver tebral ar ter y, an d th e an eu r ysm locat ion along th e Ver tebral ar ter y dissect ion is considered th e cause of m ost VA
PICA can place a PICA an eu r ysm in any of th ese m edu llar y zon es. an eur ysm s. Pat ien ts w ith th ese aneur ysm s presen t eith er w ith

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650 V Cerebral and Spinal Aneurysms

h em orrhage or isch em ic sym ptom s, an d th eir presen t at ion de- t ien t s. CTA h as 100% sen sit ivit y an d specificit y for an eu r ysm s
term in es th e clin ical course an d t reat m en t . Repor ts in th e litera- greater than 3 m m in diam eter.16,17 It can m iss sm aller aneur ysm s
t u re var y w idely, w ith som e ch aracterizing VA dissect ion as a and m ay not provide inform ation about collateral blood flow from
dangerous disease w ith a 46% m or t alit y rate,9–11 w h ereas oth ers th e con t ralateral ver tebral ar ter y. CTA does dem on st rate th e an -
suggest it is both com m on an d ben ign .12,13 Pat ien t s presen t ing eu r ysm ’s relat ion sh ip to th e bony an atom y of th e foram en m ag-
w ith VA dissect ion an d a su barach n oid h em orrh age (SAH) h ave a n um an d clivu s.
risk of rebleeding as h igh as 71%, an d th erefore sh ou ld be aggres- Angiography con t in u es to be the gold stan dard for diagn osis
sively m an aged to exclu de th e dissect ion from th e circu lat ion by an d preoperat ive evalu at ion . Pat ien ts w ith SAH an d a n egat ive
en d ovascu lar or su rgical m ean s. Pat ien t s presen t ing w ith VA dis- CTA sh ould be st udied w ith a conven t ion al fou r-vessel angiogra-
sect ion an d isch em ic sym ptom s h ave lit tle risk of h em orrh age, phy to en su re th e diagn osis. Fu r th erm ore, th e angiograp hy pro-
have a benign course, and can be m anaged m edically w ith aspirin vides a detailed im aging of th e an eur ysm th at w ill allow u s to
an d radiograph ic su r veillan ce.14,15 d elin eate t h e an eu r ysm n eck, d efin e t h e p resen ce an d locat ion
of p er forat in g bran ch es, an d evalu ate collateral flow p at ter n s
t h at m ay be im p or tan t w h en paren t ar ter y occlu sion is plan n ed.
VA d issect ion s are bet ter visu alized angiograph ically th an w ith
■ Clinical Presentation CTA because angiography can clearly visualize t w o ch an n els
(dou ble lu m en ), tapered n arrow ings w ith reduced flow (st ring
Both PICA an d VA an eu r ysm pat ien t s p resen t m ost com m on ly
sign ), an d fu siform d ilatat ion s or an eu r ysm al ou t pou ch ings w ith
w ith SAH an d th e classic sudden , severe th un derclap h eadach e.
proxim al or distal n arrow ing (pearl an d st ring sign ). Th is angio-
Th e close proxim it y of t h e an eu r ysm to th e m edu lla can lead to
grap h ic pat tern of focal vasospasm w ith post-sten ot ic fusiform
su dden loss of con sciou sn ess an d resp irator y or cardiac arrest
d ilat at ion is a com m on p resen t at ion of in t rad u ral VA d issec-
w ith rupture. An SAH from m ore distally located PICA aneur ysm s
t ion associated w ith SAH. VA sten osis or occlu sion m ay sim ply
m ay cause h eadach e localized to th e n eck an d occipital region s
be ath erosclerosis, but th is disease does n ot t ypically presen t
w ith m en ingism us. In ou r exp erien ce, 64% of p at ien t s w ith PICA
w ith h em orrh age. Ch anges in th e angiograph ic feat u res of th e VA
an eu r ysm s an d 55% of th ose w ith VA an eu r ysm s presen ted w ith
over t im e, in th e set t ing of SAH, sh ould raise su spicion for VA
SAH.
dissect ion .18
Un rupt ured an eu r ysm s m ay be in ciden tally discovered after
a brain im aging obtain ed for oth er un related reason s. Large an d
gian t an eur ysm s can cau se m ass effect an d sign s or sym ptom s of Preoperative Evaluation
brain stem com pression , low er cran ial n europath ies (e.g., dysar-
An eur ysm m orph ology, togeth er w ith th e clin ical con dit ion of
th ria an d dysp h agia), or hydroceph alu s from obst ru ct ion of th e
th e p at ien t , is an im p or t an t factor to con sider w h en p lan n ing
fou rth ven t ricle. Pat ien ts w ith th rom bot ic an eur ysm s an d som e
m an agem en t st rategy. An eur ysm s are evaluated for th eir clip -
w ith dissect ing VA an eur ysm s can also presen t w ith isch em ic
pabilit y or coilabilit y, an d com p lex an eu r ysm s are evaluated for
sym ptom s or st rokes. In t ralu m in al th rom bu s in th rom bot ic an -
alternative options. Aneur ysm size, neck size, dom e-to-neck ratio,
eu r ysm s or on dissect ion flaps can em bolize dist ally. Flow in th e
m orp h ology, locat ion , in t ralu m in al th rom bus, calcificat ion , an d
PICA can be com prom ised to cau se a ch aracterist ic lateral m ed-
th e relat ion sh ip of th e PICA to th e n eck are all im p or t an t an a-
u llar y (Wallen berg) syn drom e.
tom ic factors affect ing clipp abilit y an d coilabilit y. PICA an eu -
r ysm s are n otoriou s for th e bran ch arter y origin at ing from th e
n eck or sid e w all rat h er t h an from th e p aren t ver tebral ar ter y,
w h ich often m akes t h em d ifficu lt to t reat en d ovascu larly. Th is
■ Diagnostic Imaging and an atom y can be su ccessfu lly m an aged w it h t an d em clip p in g.
Preoperative Evaluation Oth er im por tan t angiograph ic details in clu de th e presen ce of a
du p licated PICA; th e size of th e con t ralateral PICA w h en an in -
Diagnosis sit u bypass is con sidered ; th e an terior in ferior cerebellar ar ter y
Bot h PICA an d VA an eu r ysm s can be d iagn osed n on invasively (AICA) supplying th e PICA territor y (AICA-PICA); an d th e size of
w it h m agn et ic reson an ce angiograp hy (MRA) or com p u ted to- th e con t ralateral VA an d th e p osterior com m u n icat ing ar teries,
m ographic angiography (CTA). Magnetic resonance im aging (MRI) in cases w h ere ver tebral ar ter y sacrifice is con sidered.
an d MRA are t ypically preferred in pat ien ts w ith un r upt ured Th e PICA’s origin on th e VA sh ou ld be carefu lly localized be-
presen tat ion s becau se brain im aging w ith MRI is su p erior to th at cau se a dist al origin p redict s deep dissect ion th rough th e supra-
w ith com pu ted tom ography (CT). With in t raven ous gadolin iu m hypoglossal t riangle. A distal an eur ysm locat ion aw ay from th e
adm in ist rat ion , con t rast-en h an ced im aging provides excellen t PICA’s origin p redict s a m ore sh allow dissect ion ou tside th e va-
visualization of th e in tracran ial vasculat ure. In patien ts w ith rup - goaccessor y t riangle or th e in frahypoglossal t riangle.5 Angiogra-
t u red p resen t at ion s, CT w ith CTA is preferred for its sp eed an d phy p rovides som e in dicat ion of th e t riangu lar locat ion of a PICA
ease of acquisit ion , its in creased an atom ic resolut ion , an d th e an eur ysm , w h ich m igh t in form th erapeut ic decisions an d pa-
abilit y to view th e an atom y in m ult iple cross-sect ion al plan es. t ien t select ion for surger y. PICA an eur ysm s th at can be accessed
CTA w ith th ree-dim en sion al (3D) recon st ruct ion h as becom e via sh allow dissect ion are favorable for surger y; th ose en t angled
a fron t-lin e tech n ology for evalu at ing SAH p at ien t s an d h as sup - in th e low er cran ial n er ves an d requ iring deep dissect ion m igh t
plan ted cath eter angiograp hy in a sign ifican t percen tage of p a- be m ore favorable for en d ovascu lar coiling.

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 651

W h en dealing w ith dist al PICA an eu r ysm s, rem ote from th e


■ Management Strategy ar ter y origin , a m idlin e suboccipital approach m ay be adequate.
Th e m an agem en t st rategy for PICA an d VA an eu r ysm s, as w ith The m idline suboccipital approach provides w ide exposure of the
oth er in t racran ial an eu r ysm s, is m ad e w ith a m ult idisciplin ar y posterolateral m ed u lla an d p osterior p on s, bu t gives on ly lim ited
team of n eu rosu rgeon s, n eu roin ter ven t ion al rad iologist s, an d access to m ore anterom edially located aneur ysm s. This approach,
n eu rovascular n eurologists, an d is in dividualized. Decision s to com bin ed w ith th e rem oval of t h e p osterior atlan t al arch , is su it-
treat m icrosurgically or endovascularly are m ade considering an - able for th e rare an eur ysm s involving th e p3 (ton sillom edullar y),
eur ysm locat ion , m orph ology, p resen t ing n eu rologic con dit ion , p4 (teloveloton sillar), or p5 (cor t ical) segm en t s of th e ar ter y.4
m ed ical com orbid it ies, p red icted t reat m en t r isks, p referen ces An eur ysm s associated w ith a PICA th at origin ates dist ally on
of t h e t reat m en t team , an d , u lt im ately, t h e p referen ces of t h e th e VA, an d an eu r ysm s located on th e dist al VA or VBJ, m ay be
p at ien t an d fam ily.19 bet ter exposed th rough an exten ded ret rosigm oid approach th an
In gen eral, an eur ysm s selected for m icrosurgical clipping are th rough a far-lateral ap p roach . Th e p aren t ar ter y is n ot in fre-
t h ose w it h broad n ecks, aber ran t bran ch es, or fu sifor m m or- qu en tly tor t u ou s, w h ich sh ift s th e an eu r ysm s laterally in to th e
ph ology th at m akes th em less favorable for en dovascu lar coiling. cerebellopon t in e angle. Th e exten ded ret rosigm oid approach is
Su rgical p at ien t s ten d to be you nger an d h ave low er Hu n t-Hess ideal for th ese cases, bu t provides m ore lim ited exp osure w h en
grades an d less com orbid it y. How ever, p oor-grade pat ien t s w ith th e path ology lies in th e m idlin e.4,27
elevated in t racran ial p ressu re requ iring h em atom a evacu at ion
or decom pressive cran iectom y are also selected for su rger y. Cal-
Far-Lateral Approach
cified an eu r ysm s or th ose in locat ion s th at are difficu lt to access
(like t h e d ist al VA) are selected for en d ovascu lar m an agem en t , Th e pat ien t is p osit ion ed in a m odified park-ben ch or th ree-
as are pat ien t s w ith delayed p resen t at ion s an d angiograph ic va- qu ar ter pron e p osit ion w ith th e an eu r ysm side u pw ard. Th e de-
sosp asm th at requ ires im m ediate en dovascu lar th erapy. Large or pen den t arm h angs over th e en d of th e t able, crad led in a p added
gian t PICA an d VA an eur ysm s often require debulking of th e an - sling th at allow s th e sh ou lder to drop dow n an d posit ion th e
eu r ysm , eith er th rough deflat ion or th rom bectom y, to relieve h ead properly. Th e h ead is first flexed an teriorly to bring th e
brain stem com pression an d are bet ter m an aged su rgically. ch in on e fingerbreadth from t h e stern u m . Next , th e n ose sh ou ld
Dissect ing VA an eur ysm s are preferen t ially t reated en dovas- be or ien ted d ow n to t h e floor by rot at ing t h e h ead 45 d egrees
cularly. VA dissect ing an eu r ysm s located p roxim al or distal to aw ay from t h e an eu r ysm sid e. Fin ally, t h e h ead is laterally
th e PICA can be t reated sim p ly w ith coil occlu sion of both th e flexed 30 degrees tow ard th e floor. Th ese th ree m an euvers p u t
an eur ysm an d th e VA, as long as th e con t ralateral VA can supply th e clivu s perp en dicu lar to th e floor, p roviding a visu al field
th e p osterior circu lat ion .19–22 VA occlu sion can n ot be perform ed dow n to th e axis of th e ver tebral an d basilar ar teries an d th rough
safely w h en th e con t ralateral VA term in ates in th e PICA or h as a t h e low er cran ial n er ves. Th e ip silateral m astoid p rocess be-
hypoplast ic dist al VA, an d oth er surgical opt ion s are often n eeded com es th e h igh est p oin t in t h e operat ive field an d th e cer vical-
th at t yp ically involve a byp ass. In con t rast , dissect ing VA an eu - su boccip it al angle is open ed m axim ally by tap ing th e p at ien t’s
r ysm s in corporat ing th e PICA origin are difficult to t reat en do- u p sh oulder.
vascu larly becau se coil occlu sion com prom ises th e PICA an d can A “h ockey-st ick” in cision is m ade begin n ing in th e cer vical
resu lt in PICA in farct ion . Th ese an eu r ysm s requ ire byp ass to re- m idlin e over th e C4 spin ous process, exten ding upw ard to th e
vascu larize th e PICA’s territor y an d th erefore sh ould be m an aged inion, laterally along the superior nuchal line to the m astoid bone,
m icrosu rgically.23 an d fin ish ing in feriorly at th e m astoid t ip. Th e m yocutan eou s
Fin ally, VA dissect ion s in it ially p resen t ing w ith ou t SAH are flap is m obilized in ferolaterally, leaving a 1-cm fascia cuff over
th ough t to h ave a ben ign n at u re.12,13,18 Th ese lesion s are at risk th e su perior n u ch al lin e for later reat tach m en t .
for addit ion al isch em ia an d can be m an aged m edically w ith con - Bon e rem oval con sist s of a C1 lam in otom y, a lateral suboc-
t rol of th e system ic blood p ressu re, adm in ist rat ion of an t ip late- cip ital cran iotom y, an d a con dylectom y. Th e su boccipital cran i-
let agen t s, an d brain im aging to m on itor an eu r ysm grow th or otom y is exten ded u n ilaterally from th e foram en m agn um in th e
com plete resolu t ion of th e dissect ion .24,25 m idlin e u p to th e m u scular cuff at th e t ran sverse sin us level,
as far laterally as possible an d th en back aroun d to th e foram en
m agn um . Th e lateral aspect of th e foram en m agn um an d th e
posterom edial t w o-th irds of th e occip ital con dyle are rem oved
w ith a roun d 3-m m diam on d-t ipped drill bit . Th e an terior ex-
■ Discussion of Various Approaches ten t of th e con dylectom y is reach ed w h en th e du ra begin s to
Th e far-lateral app roach , also referred to as th e lateral su boc- cur ve an terom edially, giving a t angen t ial view along th is dural
cip it al app roach or ext rem e lateral ap proach , is th e p referred plan e. Con dyle resect ion sh ou ld en able th e du ral flap to reflect
exp osu re for th e m ajorit y of PICA an d VA an eu r ysm s.21,26 Th e far- flat again st th e con dyle w ith n o bony prom in en ce obst ruct ing
lateral ap p roach accesses lesion s th at are ven t rolateral to th e th e view of t h e lateral m edu lla. Th e du ral in cision cu r ves from
m edu lla an d below th e m idclival region . Th is ap proach visu al- th e cer vical m idlin e, across th e circu lar sin u s, an d to th e lateral
izes th e ipsilateral ver tebral ar ter y from it s du ral ring p roxim ally edge of th e cran iotom y. An in ferior du ral in cision laterally un der
to th e VBJ, w ith d im in ish ing access distally. Som e of th e con t ra- C1 m obilizes th e flap laterally again st th e m argin of th e cran iot-
lateral VA is also accessible th rough th is exposu re for addit ion al om y. Th e dura is tacked to h old th e flap u n der ten sion again st
proxim al con t rol. th e con dyle.

Neurosurgery Books Full


652 V Cerebral and Spinal Aneurysms

Suboccipital Approach of th e occipital bon e an d th e cran iotom y is cut as far posteriorly


as th e scalp in cision allow s.
Th e pat ien t is p osit ion ed pron e on ch est rolls w ith th e h ead fixed Th e du ral op en ing is p erform ed u n d er th e m icroscop e to be
in t h e Mayfield h ead h old er. Th e h ead is flexed an ter iorly to ready to release CSF from th e cistern a m agn a an d relax th e cer-
bring t h e ch in on e fingerbread t h from t h e ch est to op en t h e ebellum quickly. A sem icircu lar flap based on th e sigm oid sin us
angle bet w een th e foram en m agn um an d th e C1 posterior arch . is op en ed an d th e flap is reflected an teriorly w ith st ay sut u res.
Both sh oulders can be t ap ed dow n to fu r th er op en th is angle an d Th e p u ll of th ese su t u res m obilizes th e sigm oid sin u s an teriorly
in crease th e w orking space for th e su rgeon’s h an ds. an d op en s an un obst r u cted surgical corridor.
A m idlin e skin in cision is m ade begin n ing at th e level of C3
spin ous process an d ascen ding to just above th e in ion . Th e pos-
terior cer vical fascia is exposed to m ake a Y-sh aped fascial in ci-
sion th at gen erates th ree t riangu lar leaflet s for th e closu re. Th e ■ Microsurgical Technique
su p erior leaflet p rovides a cu ff along th e su perior n u ch al lin e to
facilitate th e m uscle closu re. Th e paraspin al m uscles are m obi- Aneurysm Dissection
lized laterally to expose the occipital bone, the foram en m agn um ,
Th e cister n a m agn a is op en ed as soon as t h e m icroscop e is
C1, an d C2.
brough t in to t h e field to rem ove CSF an d rela x t h e brain . Th e
Th e cran iotom y exten ds as far laterally as th e skin in cision
d issect ion of PICA an eur ysm s is relat ively sim ple becau se both
allow s. Su periorly, th e edge of th e cran ial flap is just below th e
th e PICA an d th e VA are iden t ifiable lan dm arks, even w ith exten -
torcular an d th e t ran sverse sin uses. Th e in ferior exposure ex-
sive SAH, th at lead directly to th e an eu r ysm . Th e dissect ion st rat-
ten ds dow n to th e posterolateral aspect of th e foram en m agn um .
egy for th ese an eu r ysm s can be con cept ually divided in to six
Th e posterior arch of C1 is also rem oved to im prove th e w orking
steps. Th ese step s are th e sam e w h et h er th e an eu r ysm lies in th e
space an d access to th e cistern a m agn a. Th e du ral flap is open ed
su p rahypoglossal or th e in frahyp oglossal t riangle, bu t th e corri-
in a Y-sh ap ed fash ion an d t acked to th e bony edge of th e cran i-
dors bet w een th e cran ial n er ves are differen t dep en ding on th e
otom y. Fin ally, t h e arach n oid of t h e cister n a m agn a is w id ely
zon e. Step 1 con sists of cut t ing th e den tate ligam en t , exposing
op en ed to d rain cerebrosp in al flu id (CSF) before st ar t ing t h e
t h e in it ial in t racran ial segm en t of th e VA, an d d issect in g it d is-
m icrosurgical dissect ion .
t ally or in an an tegrad e d irect ion . Th e d en t ate ligam en t h as a
characteristic pure w hite color, different from the off-w hite color
of th e cran ial n er ves. Th is w h ite fibrous st ruct ure th at at t ach es
Extended Retrosigmoid Approach to th e lateral dura an d to th e lateral m argin of th e spin al cord is
cut to det ach th e upper cer vical spin e, open th e surgical corridor,
Th e p at ien t is p osit ion ed su p in e w ith bolsters u n der t h e ip silat -
an d develop a clear path to th e poin t of proxim al con t rol on th e
eral sh ou ld er to rot ate th e sh ou lders an d ch est in to a sem ilateral
VA. Th e VA p ierces th e du ra u n der th e den t ate ligam en t , an d th is
posit ion . Th e h ead is fixed in th e Mayfield clam p w ith th e sagit-
step provides p roxim al con t rol early on . Next , th e cau dal loop
tal m idlin e parallel to th e floor, th e n eck exten ded laterally to
of th e PICA is iden t ified an d t raced proxim ally or in a ret rograde
low er th e ver tex, an d th e h ead flexed sligh tly in th e an terior-
direct ion th rough th e cerebellom edu llar y fissu re (step 2). Th e
posterior p lan e to op en th e angle bet w een th e occip u t an d th e
cau dal loop is fou n d below t h e in ferior ton sil or w ith ton sillar
n eck. As in th e far-lateral approach , th e ipsilateral sh ou lder is
ret ract ion . As th e ton sil ret racts su periorly, th e cerebellom edu l-
pu lled d ow n w ith tape to fu r th er open th is angle an d in crease
lar y fissu re w iden s to exp ose th e p roxim al p 3 segm en t of t h e
th e w orking sp ace. Th e m astoid t ip sh ou ld be th e h igh est poin t
PICA. Dissect ion along t h e VA an d PICA lead s to t h e PICA-VA
in th e su rgical field.
convergen ce (step 3), an d th e an eu r ysm lies ju st beyon d th is
A C-sh ap ed skin in cision begin s at th e m astoid t ip, arcs p oste-
convergence. Most PICA aneur ysm s project superiorly, and there-
riorly, an d en ds just above th e pin n a. Th e scalp flap an d th e u n -
fore th e t ypical view is up th e a xis of th e dom e, w ith th e PICA
derlying m u scles are m obilized an teriorly an d elevated u n t il th e
recu rring tow ard th e n eurosu rgeon . Step 4 iden t ifies th e dist al
dep ression in th e cran iu m lead ing to th e extern al au ditor y can al
VA beyon d th e an eu r ysm by follow ing t h e m edial w all of th e VA
is ap preciated.
aroun d th e an terolateral m edulla tow ard th e VBJ. Th is m ay re-
Bon e dissect ion involves a lim ited p osterior m astoidectom y
quire som e lateral traction on the aneur ysm base or som e m edial
an d skeleton izat ion of th e sigm oid sin u s, from its origin at th e
t ract ion on th e m edu lla. Next , th e an eu r ysm n eck is dissected to
t ran sverse–sigm oid sin u s ju n ct ion to th e jugu lar bu lb. With a
open a plan e for th e clip blades. Th e m edial or m edullar y side of
h igh -speed drill an d cut t ing bur, an in it ial cut is exten ded from
th e n eck is dissected first (step 5) an d th e lateral or clival sid e is
t h e tem p oral lin e d ow n to t h e m astoid t ip , ap p roxim ately on e
dissected n ext (step 6).
fin gerbread t h an ter ior to t h e aster ion an d on e fin gerbread t h
beh in d th e extern al auditor y can al. Mastoid air cells are en tered
an d bony t rabecu lae are rem oved rap id ly. Th e t h in n in g bon e
acqu ires a solid , com p act ap p earan ce an d a blu e color ing as t h e
Clipping Technique
ven ou s sin u s is u n covered . Th e cu t t in g bu r is t h en rep laced Sim ple clip p ing is u sed w ith sm all an eu r ysm s an d th ose located
w it h a d iam on d bit , w h ich d oes n ot cu t soft t issu e an d en ables in feriorly in th e vagoaccessor y t riangle. Dist al PICA an eu r ysm s
t h e rem ain ing bon e to be d r illed aw ay safely. Th e sin u s is ex- can be exposed w idely, an d clips can be m an euvered easily.
posed along its cou rse from th e t ran sverse sin u s to th e jugu lar Deep er an eu r ysm s in th e su p rahypoglossal t riangle an d an terior
bu lb, an d from its an terior edge to its border posteriorly. Th e m edullar y zon e can be clipped sim ply w h en th ey are sm all an d
su boccip it al du ra is dissected blu n tly aw ay from th e in n er table th e m orp h ology p erm it s. Mu lt ilobu lated PICA an eu r ysm s can be

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 653

rep aired by sim ply clip p ing each lobe as a dist in ct an eu r ysm . A con st r u ct ive tech n iqu e is ap p licable w h en t h ere is ju st on e af-
fen est rated clip in a t an d em con figu rat ion is a ver y com m on feren t ar ter y an d on e efferen t ar ter y, n ot w h en th ere is bifu r-
clipp ing tech n iqu e w ith PICA an eu r ysm s. Th e fen est rat ion can cated an atom y. Reim plan tat ion is especially u seful w h en th e clip
en circle t h e PICA or igin , w h ich frequ en t ly ar ises from t h e base applicat ion can n ot preser ve th e PICA origin . Th e ar ter y can be
of th e an eu r ysm . Bu t it can also en circle any cran ial n er ve t h at recon st it uted w ith an en d-to-side reim p lan t at ion on to t h e prox-
is adh ering to th e dom e of th e an eur ysm . A stacked st raigh t clip im al VA.
over th e fen est rat ion w ill com plete th e an eu r ysm closure.
Direct clipping is preferred, but th e un usual an atom y often
associated w ith PICA an eu r ysm s calls for altern at ive tech n iques
in on e-th ird of cases.21 Trap p ing or p roxim al occlu sion of t h e ■ Illustrative Cases
an eu r ysm w it h or w it h ou t revascu lar izat ion is t h e alter n at ive
Case 1
t reat m en t w h en direct clip ping is n ot feasible. Th ere are a w ide
variet y of excellen t bypass opt ion s for th e PICA, an d tem porar y A 35-year-old w om an presen ted w ith sudden , severe h eadach e
occlusion is w ell tolerated in th is territor y, yielding favorable th at began 3 days earlier. Sh e h ad a n orm al n eu rologic exam . A
resu lt s. CT scan revealed t h e p resen ce of blood in t h e p oster ior fossa
Th e occipital arter y can be used as a donor for an ext racranial- cistern s an d th e fourth ven t ricle. Angiography sh ow ed a 6-m m
to-in t racran ial bypass opt ion . How ever, in t racran ial-to-in t racra- fu siform righ t ver tebral ar ter y an eu r ysm arising from th e PICA
nial bypasses elim inate the need for har vesting this artery, are less origin (Fig. 56.3). Th e con t ralateral PICA an d VA w ere n orm al.
vuln erable to injur y or occlusion , an d use don or an d recipien t Th e su rgical plan w as to t rap th e an eu r ysm an d revascu larize
arteries w ith w ell-m atched diam eters. Intracranial-to-intracranial th e PICA territor y w ith eith er PICA reim plan t at ion or a PICA–
opt ion s in clude th e side-to-side PICA–PICA bypass, an eur ysm PICA byp ass. A far-lateral cran iotom y exposed both PICAs in th e
excision w ith en d-to-en d rean astom osis, an d t rap p ing w ith en d- m idlin e, an d th e vertebral arter y w as follow ed to th e an eur ys-
to-side reim plan t at ion of th e PICA on to th e proxim al VA. Th e m al por t ion of th e ar ter y. Th e an atom y seem ed m ost favorable
PICA–PICA byp ass t akes advan t age of t h e an atom ic p roxim it y for a PICA–PICA bypass rath er th an a reim plan t at ion . A side-to-
of th e t w o cau dal loop s of t h ese ar ter ies an d join s t h em w it h a side PICA–PICA an astom osis w as p erform ed w ith a 9-0 m on o-
side-to-side anastom osis.28 The anterograde flow that is lost from filam en t sut ure. In docyan in e green (ICG) in t raoperat ive video-
on e PICA w ith th e an eur ysm clipping is replaced by ret rograde angiograp hy con fir m ed t h e p aten cy of th e an astom osis. Th e
flow from th e con t ralateral PICA th rough th e an astom osis. Re- an eur ysm w as th en com pletely t rapped by applying perm an en t
an astom osis is ideal for fusiform an eur ysm s th at are sm all or clips to th e distal VA, th e PICA origin , an d th e p roxim al VA.
m ediu m in size an d d ist ally located from th e PICA’s origin . Th e Postoperat ive angiography dem on st rated com plete occlusion
PICA often h as redu n dan cy th at facilit ates d et ach ing th e afferen t of th e an eur ysm al segm en t an d a paten t PICA–PICA bypass. Th e
an d efferen t en ds of th e vessel from th e an eur ysm an d pu lling p at ien t w as disch arged h om e 3 w eeks after h er SAH an d re-
th em back togeth er w ith th e en d-to-en d an astom osis. Th is re- m ain ed n eu rologically in tact at 6-m on th follow -up.

b
a
Fig. 56.3a–f Case 1. (a) Cerebral angiography, right vertebral artery injection, lateral view. A fusiform 6-m m aneurysm is observed at the origin of
posterior inferior cerebellar artery (PICA) on the vertebral artery (VA). (b) The t wo PICAs are exposed in the m idline. (continued on page 654)

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654 V Cerebral and Spinal Aneurysms

c d

e f

Fig . 56.3a–f (continued) (c) A side-to-side p3–p3 bypass is perform ed. the dist al VA, PICA origin, and proxim al VA. (f) Postoperative angiography
(d) Intraoperative indocyanine green (ICG) videoangiography shows by- shows the aneurysm occlusion and a patent PICA–PICA bypass.
pass patency. (e) The aneurysm is com pletely trapped by applying clips to

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 655

Case 2 elevated sligh tly, an d a good view of th e an eur ysm w as obt ain ed.
Th e in flow an d ou tflow ar teries w ere carefu lly dissected . Th e
Th is 74-year-old w om an com p lain ed of several w eeks of h ead- an eur ysm w as clip recon st ructed w ith a series of stacked st raigh t
ach e an d back pain . Sh e h ad n o n eu rologic deficits. CT angiogra- Yaşargil clip s th at closed t h e an eu r ysm an d n icely p reser ved
phy revealed a vertebral ar ter y an eu r ysm , an d fu r th er evalu at ion flow in th e PICA. An in t raoperat ive ICG videoangiography con -
w ith cath eter angiography sh ow ed a 6-m m broad-based an eu- firm ed paten cy of th e paren t vessel an d n o fur th er filling of th e
r ysm arising from th e left PICA just dist al to its origin along th e an eur ysm . An addit ion al m in i-clip w as applied to close a sm all
ver tebral ar ter y. “dog ear.”
Th e su rgical p lan w as to clip -recon st r u ct t h e an eu r ysm Postoperat ive angiography dem on st rated com plete occlusion
t h rough a far-lateral cran iotom y (Fig. 56.4). Th e left ver tebral of th e an eur ysm an d a paten t paren t vessel. Th e pat ien t w as dis-
ar ter y w as t raced an tegrad e to th e PICA or igin an d th e an eu - ch arged h om e 4 days after su rger y an d rem ain ed n eu rologically
r ysm w as seen in th e ton sillom edu llar y fissu re. Th e ton sil w as in tact at 6-m on th follow -up .

Fig. 56.4a–c Case 2. (a) This left posterior inferior cerebellar artery (PICA)
aneurysm sat superior to the hypoglossal rootlets, in the suprahypoglossal
triangle and lateral to the lower cranial nerves, in the tonsillomedullary zone.
(b,c) Its broad base required several stacked clips to close the neck.

b c

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656 V Cerebral and Spinal Aneurysms

Case 3 in th e space u n dern eath t h e ton sil an d t raced to th e an eur ysm


(Fig. 56.5). The in flow and outflow arteries w ere w idely exposed.
Th is 68-year-old w om an h ad a left PICA an eu r ysm th at w as in ci- The aneurysm had a broad base, but w as reconstructed using t w o
den tally diagn osed during th e evalu at ion for a pu lm on ar y in fec- st raigh t in tersect ing clip s. An ICG in t raoperat ive videoangiogra-
tion. Her neurologic exam ination was com pletely norm al. Catheter phy dem on st rated th e com p lete occlu sion of th e an eu r ysm an d
angiography show ed a distal, broad-based 5-m m PICA aneurysm . th e preser ved paten cy of th e p aren t ar ter y.
An u n su ccessfu l at tem pt w as m ade at en dovascu lar t reat m en t . Postoperat ive angiography con firm ed com plete occlu sion of
Th e su rgical p lan w as to clip t h e an eu r ysm t h rough a far- th e an eu r ysm an d paten cy of th e p aren t ar ter y. Th e pat ien t w as
lateral cran iotom y, w ith excision /rean astom osis as th e altern a- disch arged h om e on p ostoperat ive day 4 an d w as n eu rologically
t ive p lan . Th e p osterior in ferior cerebellar ar ter y w as id en t ified in tact at th e 6-w eek follow -u p evaluat ion .

a b

c d

Fig. 56.5a–d Case 3. (a) This distal posterior inferior cerebellar artery nine green (ICG) videoangiography demonstrated complete occlusion of the
(PICA) aneurysm was located outside the vagoaccessory triangle. (b,c) Clip aneurysm and patency of the parent vessel.
reconstruction required t wo intersecting clips. (d) Intraoperative indocya-

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 657

Outcomes
■ Literature Review
Clinical Outcomes
Treat m en t of PICA an d VA an eur ysm s h as sign ifican tly advan ced
Review ing ou r experien ce at th e Un iversit y of Californ ia, San in th e p ast t w o decades th an ks to im provem en t s in m icrosurgi-
Fran cisco,5,21 w e h ad n o surgical m or t alit y w ith PICA an eur ysm s. cal tech n iqu e, refin em en t in th e sku ll base app roach es, advan ced
Tw o p at ien t s w ere n eu rologically w orse p ostop erat ively an d at preoperative im aging, and endovascular treatm ent options. Table
late follow -u p . On e of t h em h ad a large, ath erosclerot ic an eu - 56.2 provides a sh or t su m m ar y of th e m ost recen t clin ical result s
r ysm w ith a w ide n eck th at requ ired stacked fen est rated clip s to p u blish ed by several au t h ors w it h exp er ien ce t reat ing t h ese
close th e n eck an d preser ve PICA flow. Desp ite good PICA flow an eur ysm s.29–33
m easu red in t raop erat ively by Dop p ler u lt rasou n d an d p ostop -
erat ively by angiograp hy, h e su ffered a PICA territor y in farct . Th e
oth er p at ien t develop ed ven t riculit is an d a w ou n d in fect ion th at
requ ired op erat ive d ebr idem en t . Tw o ad d it ion al p at ien t s h ad
t ran sien t n eu rologic w orsen in g, bu t t h eir d eficit s resolved at
■ Discussion
late follow -up. On e of th em h ad h em isen sor y n um bn ess postop - Th e In tern at ion al Su barach n oid An eu r ysm Trial (ISAT) ch anged
erat ively w ith ou t MRI eviden ce of m edu llar y in farct ion th at re- th e m an agem en t of brain an eu r ysm s in developed cou n t ries,34,35
solved com pletely. Th e oth er pat ien t deteriorated du e to severe legit im izing en dovascu lar coiling as a safe altern at ive to surgical
vasospasm requiring angioplast y an d in t ra-ar terial verapam il, clip p in g an d su p p lan t in g clip p in g as t h e an eu r ysm t reat m en t
but m ade a good recover y at late follow -up. Good outcom es of ch oice. On e respon se to th ese result s h as been th e adopt ion of
(Glasgow Ou tcom e Scale [GOS] scores of 4 an d 5) w ere obser ved a “coil-first” policy w h ereby all an eur ysm s are con sidered for
in 41 p at ien t s (80%; Table 56.1). Th ere w ere n o sign ifican t d if- coiling, reser ving su rger y for th ose w ith u n favorable an atom y or
feren ces in pat ien t outcom es w ith PICA an eur ysm s in th e supra- failed coiling at tem pts.
hyp oglossal t rian gle versu s t h e in frahyp oglossal t r iangle. In Th is m an agem en t p olicy raises ser iou s con cer n s. First , al-
con t rast , w e obser ved th at p at ien t s w ith PICA an eu r ysm s ou t - t h ough ISAT exam in ed a sm all su bset of eligible p at ien t s w ith
side th e vagoaccessory triangle had n o neurologic or cranial ner ve rupt ured an eur ysm s (2,143/9,559, 22.4%), th e result s h ave been
m orbidit y. ext rap olated to ju st ify en dovascu lar t reat m en t of all an eu r ysm s,
En dovascular th erapy w as in it ially con sidered for m ost VA an - rupt ured an d un ru pt ured. Secon d, ISAT’s advan tages in outcom e
eu r ysm s an d dissect ion s. How ever, VA an eu r ysm s in corporat ing w ith coiling h ave van ish ed in 5-year follow -up st udies, due to
th e PICA origin requ ired byp ass, an d p at ien ts w ith large or gian t aneurysm recurrences, rehem orrhages, and m orbidit y associated
an eur ysm s presen t ing w ith sym ptom s an d sign s of brain stem w ith ret reat m en t .36,37 Th ird, n ew devices like in t ralum in al an d
com p ression requ ired su rgical d ebu lkin g. Th e on ly d eat h oc- in t rasaccu lar flow diver ters are quickly expan ding th e feasibilit y
curred in a 74-year-old pat ien t w ith an en larging VA an eur ysm of en dovascu lar th erapy, but th eir safet y, efficacy, an d du rabilit y
w h o p resen ted w ith h em orrh age (Hun t-Hess grade V). Tw o sep - h ave n ot been an alyzed sufficien tly an d th ere are n o ran dom ized
arate at tem pt s at sten t -assisted coiling w ere u n su ccessfu l an d t rials com paring th em w ith su rger y.
com p licated by a VA dissect ion w ith an occip it al in farct ion . Th e W h en it com es to th e p osterior circu lat ion , on ly 58 pat ien t s
pat ien t failed to im prove after an u n com p licated m icrosu rgical (2.7%) from a coh or t of 2,143 h ad p oster ior circu lat ion an eu -
clipp ing. We obser ved good ou tcom es (GOS scores of 4 an d 5) in r ysm s, an d com p arat ive ou tcom e dat a w ere n ot p resen ted for
eigh t p at ien ts (72%; Table 56.1). th is grou p .34 Th erefore, th e p ercept ion th at en dovascu lar th er-
apy is bet ter w ith posterior circulat ion an eur ysm s is n ot based
on ISAT d at a. Poor ou tcom es w it h p oster ior circu lat ion an eu -
Table 56.1 Neurologic Outcomes After Surgical Management of r ysm s correlate w it h an eu r ysm size, locat ion , an d p at ien t age.
PICA and VA Aneurysms A pract ice that con siders a select ive approach to an eur ysm sur-
No. (%) ger y in th e posterior circulat ion , w ith m icrosu rger y playing a
Glasgow Outcome prim ar y role w ith som e an eu r ysm s (P1 PCA, su perior cerebellar
Scale Score Preop Early Late Follow -Up ar ter y [SCA], distal AICA an d PICA) an d a secon dar y role w ith
PICA aneurysms oth ers (basilar t run k, p roxim al AICA, VBJ, an d VA) yields th e best
5 13 (25) 21 (41) 28 (55) result s both angiograph ically an d n eurologically.21
4 20 (39) 15 (29) 13 (25) Th e PICA an eu r ysm s are p erh aps th e best exam p le of an an -
3 12 (24) 12 (24) 10 (20) eu r ysm for w h ich m icrosu rger y con t in u es to p lay a prim ar y role.
2 6 (12) 3 (6) 0 (0) An u n u su ally large p or t ion of PICA an eu r ysm h ave broad n ecks,
1 0 (0) 0 (0) 0 (0) m ultiple lobules, efferent arteries originating from the base, non-
Total 51 51 51 saccu lar m orph ology, in t ralum in al th rom bus, or distal locat ion
VA aneurysms th at m akes en dovascu lar th erapies su bopt im al.4,21 Microsurger y
5 1 (9) 5 (45) 7 (64) for PICA an eur ysm s is par t icu larly w ell su ited because exposure
4 2 (18) 1 (9) 1 (9) th rough a far-lateral cran iotom y is excellen t , p roxim al con t rol is
3 3 (27) 4 (36) 2 (18) im m ediately accessible, an d m in im al m icrodissect ion is n eeded
2 0 (0) 1 (9) 0 (0)
to op en t h e ton sillom ed u llar y fissu re an d follow t h e PICA an d
1 5 (45) 0 (0) 1 (9)
VA tow ard th eir convergen ce on th e an eu r ysm n eck. Th e low er
Total 11 11 11
cran ial n er ves an d m edu llar y perforators are located th rough th e

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658
V Cerebral and Spinal Aneurysms

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56 Surgical Therapies for Vertebral Artery and PICA Aneurysm s 659

field, but th ey are easily avoided an d protected. Microsurgical t u re, an d con t rol of th e distal VA can be elu sive. Th ese an eu r ysm s
opt ion s for un usu al PICA an eur ysm an atom y are exten sive. Th eir t ypically lack a n eck, an d t h e arterial t issue m ay n ot resp on d
w ide n ecks can often be recon st r ucted w ith t an dem clipping h ospitably to clip applicat ion . Microsurger y sh ould be reser ved
tech n iqu es by u sing t h e fen est rated clip blad e to close t h e bu lk for VA an eu r ysm s involving th e PICA th at require revascu lariza-
of t h e n eck an d t h e fen est rat ion to rebu ild th e PICA or igin . t ion . Microsu rger y is also in d icated for th rom bot ic an eu r ysm s
W h en th e PICA can n ot be saved, revascularizat ion opt ion s in - com p ressing th e brain stem an d cau sing p rogressive n eu rologic
clude ext racranial-to-intracran ial bypass w ith th e occipital artery, deteriorat ion . Th ese an eu r ysm s can be debu lked in tern ally an d
an d in t racran ial-to-in t racran ial bypasses w ith th e con t ralateral th en closed w ith clip recon st ru ct ion or t rapping of th e VA.
PICA (PICA–PICA bypass), end-to-end reanastom osis, or reim plan-
tat ion of th e PICA on to th e VA. Perform ing th ese tech n iqu es in
th is deep su rgical corridor is tech n ically ch allenging, bu t visu al-
ization is excellent , tem porar y arterial occlusion is w ell tolerated,
■ Conclusion
an d resu lts are favorable. Alth ough en dovascular tech n iques are useful for a m ajorit y of
Th e VA aneurysm s are suited for endovascular therapy because an eur ysm s, com plex an eu r ysm s, especially th ose w ith fusiform
th ey are frequ en tly dissect ing an eu r ysm s, are easily t reated w ith m orp h ology, m ay ben efit from m icrosu rgical recon st ruct ion or
ar terial sacrifice, an d a com peten t con t ralateral VA m akes th is cerebral revascularizat ion . Despite gen eralizat ion of th e result s
t reat m en t tolerable. In con t rast , m icrosu rgical exposu re th rough of ISAT to p oster ior circu lat ion an eu r ysm s, m icrosu rger y re-
a far-lateral approach deteriorates w ith m ore m idline aneurysm s m ain s a safe, durable, an d effect ive t reat m en t st rategy for th ese
beyon d PICA. Dissect ing an eur ysm s are friable an d pron e to r up - an eur ysm s.

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ger y 2013;72:763–775, discussion 775–776 r ysm s: an assessm en t of in t racran ial-in t racranial bypass. Neu rosurger y
9. Aoki N, Sakai T. Rebleeding from in t racran ial dissect ing an eur ysm in th e 2009;65:670–683, discu ssion 683
ver tebral ar ter y. St roke 1990;21:1628–1631 24. Kim BM, Kim SH, Kim DI, et al. Outcom es an d progn ost ic factors of in t ra-
10. Berger MS, Wilson CB. In t racran ial dissect ing an eur ysm s of th e posterior cran ial un rupt ured ver tebrobasilar ar ter y dissect ion . Neurology 2011;76:
circu lat ion . Repor t of six cases an d review of th e literat u re. J Neu rosu rg 1735–1741
1984;61:882–894 25. Kim C-H, Son Y-J, Paek SH, et al. Clin ical an alysis of ver tebrobasilar dissec-
11. Blicken st aff KL, Weaver FA, Yellin AE, St ain SC, Fin ck E. Tren d s in t h e t ion . Act a Neuroch ir (Wien ) 2006;148:395–404
m an agem en t of t raum at ic vertebral arter y injuries. Am J Surg 1989;158: 26. Krayen buh l N, Guerrero C, Krish t AF. Tech n ical st rategies to approach an -
101–105, d iscussion 105–106 eu r ysm s of th e ver tebral an d posterior in ferior cerebellar arteries. Neuro-
12. Hosoya T, Adach i M, Yam agu ch i K, Haku T, Kayam a T, Kato T. Clin ical an d su rg Focus 2005;19:E4
n euroradiological feat ures of in t racranial ver tebrobasilar ar ter y dissec- 27. Quiñ on es-Hin ojosa A, Chang EF, Law ton MT. Th e exten ded ret rosigm oid
t ion . St roke 1999;30:1083–1090 ap p roach : an altern at ive to radical cran ial base ap p roach es for posterior
13. Yoshim oto Y, Wakai S. Unruptured intracranial vertebral artery dissection. fossa lesion s. Neurosurger y 2006;58(4, Suppl 2):ONS-208–ONS-214, dis-
Clinical course and serial radiograph ic im agings. Stroke 1997;28:370–374 cussion ONS-214
14. Mizut an i T, Aruga T, Kirin o T, Miki Y, Saito I, Tsuch ida T. Recurren t su b- 28. Korja M, Sen C, Langer D. Operat ive n uan ces of side-to-side in sit u poste-
arachnoid hem orrhage from untreated rupt ured vertebrobasilar dissecting rior in ferior cerebellar ar ter y-posterior in ferior cerebellar ar ter y bypass
aneur ysm s. Neurosurger y 1995;36:905–911, discussion 912–913 procedu re. Neu rosu rger y 2010;67(2, Su pp l Operat ive):471–477

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660 V Cerebral and Spinal Aneurysms

29. Albu querque FC, Fiorella DJ, Han PP, Deshm u kh VR, Kim LJ, McDougall CG. 34. Molyn eu x AJ, Kerr RS, Yu LM, et al; In tern at ion al Subarach n oid An eur ysm
En dovascular m anagem en t of in t racran ial vertebral arter y dissect ing an - Trial (ISAT) Collaborat ive Group. In tern at ion al subarach n oid an eur ysm
eur ysm s. Neurosurg Focus 2005;18:E3 t rial (ISAT) of n eurosu rgical clipping versus en dovascu lar coiling in 2143
30. Al-kh ayat H, Al-Khayat H, Besh ay J, Man n er D, W h ite J. Ver tebral ar ter y- pat ien t s w ith rupt ured in t racran ial an eur ysm s: a ran dom ised com pari-
p osteroin fer ior cerebellar ar ter y an eu r ysm s: clin ical an d low er cran ial son of effect s on sur vival, depen den cy, seizures, rebleeding, su bgrou ps,
nerve outcom es in 52 patients. Neurosurger y 2005;56:2–10, discussion 11 an d an eur ysm occlu sion. Lan cet 2005;366:809–817
31. D’Am brosio AL, Kreiter KT, Bush CA, et al. Far lateral suboccipit al approach 35. Tah a MS, Patel UJ. Clipping versus coiling for r upt ured int racran ial an eu-
for the t reat m en t of proxim al posteroinferior cerebellar ar ter y an eu- r ysm s after th e in tern at ional su barach n oid an eur ysm t rial. Un ited King-
r ysm s: su rgical result s an d long-term outcom e. Neurosurger y 2004;55: dom exp erien ce. Neu roscien ces (Riyadh ) 2009;14:118–123
39–50, discu ssion 50–54 36. Bakker NA, Met zem aekers JDM, Groen RJM, Mooij JJA, Van Dijk JMC. In -
32. Mericle RA, Reig AS, Burr y MV, Eskioglu E, Firm en t CS, San t ra S. En dovas- ter n at ion al subarach n oid aneu r ysm t rial 2009: en dovascular coiling of
cu lar su rger y for p roxim al p osterior in ferior cerebellar ar ter y an eu r ysm s: ruptured intracranial aneur ysm s has no significant advantage over neuro-
an an alysis of Glasgow Outcom e Score by Hun t-Hess grades. Neu rosur- surgical clipping. Neu rosurger y 2010;66:961–962
ger y 2006;58:619–625, discu ssion 619–625 37. Raper DMS, Allan R. In tern at ion al subarach noid t rial in th e long r un : crit i-
33. Peerless S, Hern esn iem i JA, Drake C. Posterior circulat ion an eur ysm s. In : cal evaluat ion of th e long-term follow -up dat a from th e ISAT t rial of clip -
Wilkin s R, Rengach ar y SS, eds. Neurosu rger y. New York: McGraw -Hill; ping vs coiling for rupt ured in t racran ial an eur ysm s. Neurosurger y 2010;
1996:2341–2356 66:1166–1169, discussion 1169

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57 Microsurgical Management
of Aneurysms of the Posterior
Cerebral, Superior Cerebellar, and
Anterior Inferior Cerebellar Arteries
Jonathan J. Russin and Robert F. Spet zler

Su rgical t reat m en t of p at ien t s w ith p osterior circu lat ion an eu - m ake prim ar y clipping difficult , an d in several publish ed series,
r ysm s presen t s un ique ch allenges. Surgical exposure of m any of t rapp ing th ese an eu r ysm s w as com m on .8,12 Lu xurious an asto-
th ese an eu r ysm s requ ires com p lex sku ll base ap p roach es. Th e m ot ic n et w orks bet w een cerebellar ar teries frequ en tly en able
posterior circu lat ion is in t im ately involved w ith th e brain stem , paren t vessel occlu sion w ith lim ited in farct ion , especially w h en
an d isch em ic com plicat ion s th at arise w h en t reat ing pat ien ts dealing w ith distal an eu r ysm s. An eu r ysm s of th e AICA are t ypi-
w ith th ese an eur ysm s frequen tly result in clin ically sign ifican t cally t reated via a ret rosigm oid app roach bu t can requ ire a m ore
deficit s. Becau se p osterior circu lat ion an eu r ysm s are rare, on ly a an terior exposure.
h an dful of cen ters w orldw ide h ave clin ically relevan t experien ce
w ith large n um bers of th ese pat ien ts. Th is ch apter sum m arizes
t h e p earls of m an agin g p at ien t s w ith an eu r ysm s of t h e p oste-
r ior cerebral, su p er ior cerebellar, or an ter ior in fer ior cerebellar ■ Relevant Embryology
ar teries.
Posterior Cerebral Artery
Th e paired posterior cerebral ar teries (PCAs) are th e term in al
bran ch es of th e basilar t run k. As such , th e proxim al por t ion s of Th e PCA form s in th e develop ing fet al brain relat ively late. Sev-
th ese ar teries are frequ en tly involved w ith an eu r ysm s of th e eral em br yon ic vessels located distally on th e posterior com m u-
basilar t ip. (Th ese specific an eur ysm s are th e topic of Ch apters n icat ing ar ter y (PCoA) fuse to form th e PCA. Th is fet al m orph ol-
54 an d 55.) An eur ysm s of th e PCA itself are less com m on an d ogy, w h ere th e PCA is prim arily su pplied by th e PCoA, frequen tly
rep resen t bet w een 0.7%an d 2.3%of all in t racran ial an eur ysm s.1–4 p ersist s, m aking t h e PCA t h e m ost m or p h ologically var iable
Th e m ajor it y of PCA an eu r ysm s occu r on t h e p roxim al p or t ion cerebral arter y. Several differen t t ypes of PCA m orph ology are
of th e ar ter y, an d pat ien ts w ith th ese an eu r ysm s u su ally presen t defin ed by th e relat ive con t ribu t ion of th e p roxim al PCA an d th e
w ith su barach n oid h em orrh age.3,5–8 W h en m an aging th ese PCA PCoA to th e distal PCA. Th e form er t w o ar teries (proxim al PCA
aneurysm s, circum flex as w ell as direct perforating arteries m ust an d PCoA) provide equal con t ribut ion s to th e dist al PCA in th e
be preser ved. In addit ion , exposure of th e various segm en ts of t ran sit ion al t ype. Th e PCoA is th e m ain con t ribu tor in th e fet al
th e PCA requ ires a flexible assor t m en t of su rgical skills. t ype, an d th e proxim al PCA is th e dom in an t con t ribu tor in th e
Su p erior cerebellar ar ter y (SCA) an eu r ysm s are also rare le- adult t ype.13 Prior to th e m at u rat ion of th e PCA, th e an terior ch o-
sion s w ith a reported in ciden ce of 1.5 to 1.7%.8–10 Th e m ajorit y of roidal arter y ser ves th e m ajorit y of th e territor y th at th e adu lt
SCA an eu r ysm s are located p roxim ally, t ypically at th e basilar PCA irrigates. Rarely th is m orph ology can persist post n at ally.14
jun ct ion .8 Th e m ost com m on presen tat ion for p at ien t s w ith SCA Th e m orphological t ype of PCA can be im portant w hen consider-
an eur ysm s is subarach n oid h em orrh age, but th e close associa- ing proxim al con t rol, collateral perfusion , an d th e poten tial n eed
t ion to cran ial n er ves (CNs) III, IV, an d V also resu lts in presen ta- for revascu larizat ion w h en t reat ing PCA an eu r ysm s.
t ion s secon dar y to m ass effect , su ch as cran ial n er ve p alsies.10
Th e com m on in corp orat ion of th e proxim al SCA in to th e n eck of
Superior Cerebellar Artery
th ese an eu r ysm s m akes preser vat ion of th e p aren t ar ter y ch al-
lenging, an d, in som e cases, su rgical or en dovascu lar sacrifice of In th e m ajorit y of pat ien ts, th e SCA origin ates from th e basilar
th e p aren t ar ter y is n ecessar y. Given th e cou rse of th e SCA, su rgi- ar ter y just proxim al to or w ith in 2.5 m m of th e PCAs an d h as th e
cal ap p roach es ten d to p arallel th ose u sed to exp ose an eu r ysm s m ost con sisten t m orp h ology of th e cerebellar ar teries.15 It is n ot
of th e PCA. u n u su al to see du plicat ion of th e SCA off of th e basilar ar ter y.
An eur ysm s of th e an terior in ferior cerebellar ar ter y (AICA) are An atom ic dissect ion s h ave also revealed single SCA t ru n k origin s
m ost com m on ly located dist al on th e p aren t ar ter y.8 Th is p redi- off of th e proxim al PCA or duplicat ion s of th e SCA w ith th e ros-
lect ion dictates th e p resen tat ion of p at ien t s w ith th ese an eu - t ral t r u n k origin at ing off of th e PCA.16 In addit ion , th ere are rare
r ysm s, w h ich can p rodu ce acu te sym ptom s of cran ial n er ve dys- case rep or t s of th e SCA origin at ing off of th e in tern al carot id ar-
fu n ct ion along w ith su barach n oid h em orrh age or ch ron ic cran ial ter y in th e cavern ous sin us w ith out any con n ect ion to th e basilar
n er ve sym ptom s, m im icking a cerebellopon t in e m ass.11,12 AICA ar ter y. Th is m orph ology is believed to be a variat ion of a persis-
an eur ysm s are ext rem ely rare, represen t ing 0.22% to 0.5% of all ten t t r igem in al ar ter y.17 In som e cases, t h is var iat ion can ser ve
an eur ysm s.9,12 Th e relat ively sm all caliber of th e dist al AICA can n ot on ly th e SCA bu t also th e AICA territor y.18 Th ese m orph ologi-

661

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662 V Cerebral and Spinal Aneurysms

Fig . 57.1 An axial illustration of the posterior


cerebral artery (PCA) and the local anatom ic rela-
tionships of its segments (P1, P2a, P2p, P3, and
P4). a., artery; aa., arteries; CN, cranial nerve; SCA,
superior cerebellar artery. (Courtesy of Barrow
Neurological Institute.)

cal variations can im pact clinical decision m aking w hen dealing brain to th e an terior lim it of th e calcarin e fissure is referred to as
w ith SCA or PCA an eur ysm s, as can th e proxim it y of th e SCA to th e P3 segm en t . Th e rem ain der of th e PCA is com m on ly referred
th e PCA as th ey t raverse th e p erim esen ceph alic cistern s. to as th e P4 segm en t or cor t ical segm en t . Du e to th e differen ce in
su rgical ap proach to th e an terior versu s posterior m idbrain , th e
P2 segm en t is fu r th er d ivided in to P2a an d P2p segm en ts. Th ese
Anterior Inferior Cerebellar Artery segm en t s are divided by th e p osterior border of th e cerebral pe-
An atom ic st udies of th e AICA h ave sh ow n th at it origin ates off of du n cle (Fig. 57.1).21
th e basilar ar ter y as a single t ru n k in m ore th an 70% of cases, Alth ough th e above an atom ic descript ion is th e m ost w idely
alth ough th e AICA can con sist of m u lt iple t ru n ks. Th e origin of accepted, oth er au th ors h ave described th e PCA an atom y based
th e AICA can be alm ost anyw h ere along th e basilar ar ter y t r un k, solely on su rgical ap proach . Th e su rgical segm en ts of th e PCA
but it is m ost com m on ly fou n d on th e low er h alf.15 A single t ru n k h ave been defin ed as th e S1 or an terior, S2 or m iddle, an d S3 or
off of th e basilar ar ter y th at ser ves both th e AICA an d posterior posterior.7 Th ese segm en t s are defin ed in Table 57.1. Lesion s of
in ferior cerebellar arter y (PICA) territories h as been reported, as th e S1 segm en t are t yp ically app roach ed via a pterion al, orbito-
h ave an eur ysm s of th is t ype of varian t .19 Sim ilar to th e SCA, th e zygom atic, tem poral-polar, or subtem poral craniotom y. Pathology
AICA can also h ave it s origin off of th e intern al carot id ar ter y in in th e S2 segm en t is com m on ly accessed th rough a subtem poral
th e cavern ou s sin u s.20 Th ese m orp h ological varian ts are im por- cran iotom y. An occipital in terh em isph eric approach is best suited
tan t to appreciate w hen plan n ing t reat m en t st rategies for th e for th e S3 segm en t .7
ext rem ely rare an eu r ysm s of th e AICA. Th e variou s segm en t s of th e PCA h arbor im p or t an t vascu la-
t ure th at m ust be appreciated w h en m aking treatm en t plan s. Th e
text box describes th e m ost com m on arteries origin at ing from
th e PCA.21
■ Surgically Relevant Anatomy
Posterior Cerebral Artery Table 57.1 Surgical Segments of the Posterior Cerebral Artery
(PCA)
Zeal an d Rh oton 21 in 1978 described th e an atom y of th e PCA an d
divided it in to four segm en ts. Th e P1 segm en t is from th e origin S1 Basilar bifurcation to the lateralmost aspect of the PCA
S2 Lateralm ost aspect of PCA to the collicular point
of th e PCA to th e in sert ion of th e PCoA. Th e P2 segm en t exten ds
S3 Collicular point to the distal branches in the calcarine and
from th e PCoA arou n d to th e posterior m argin of th e m idbrain .
parieto-occipital sulci
Th e por t ion of th e PCA from th e p osterior m argin of th e m id-

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 663

Posterior Cerebral Artery Perforating and Th ese p er forat in g an d cor t ical ar ter ies requ ire at ten t ion
Branch Arteries d u ring d irect su rgical clip p ing, as w ell as w h en con sid er ing
t rap p in g w it h or w it h ou t revascu lar izat ion p roced u res. Failu re
P1: Basilar bifurcation to PCoA to preser ve t h ese ar ter ies, esp ecially in t h e p roxim al segm en t s,
Branches can resu lt in isch em ic com p licat ion s w it h d evast at in g clin ical
• Thalamoperforating resu lt s.
• Long and short circumflex arteries
P2a: PCoA to posterior border of peduncle
Branches
Superior Cerebellar Artery
• Peduncular perforating arteries
• Thalamogeniculate arteries Rh oton 15 defin ed th e fou r segm en ts of th e SCA (Fig. 57.2). Th ese
• Medial posterior choroidal are t h e an ter ior p on tom esen cep h alic, lateral p on tom esen ce-
• Hippocampal arteries p h alic, cerebellom esen cep h alic, an d cor t ical segm en t s, w h ich
• Anterior temporal artery are det ailed in Table 57.2.15 Th e surgical exposure of th e p roxi-
P2p: Posterior border of peduncle to calcarine fissure m al SCA is sim ilar to th at of th e ipsilateral PCA. How ever, m ore
Branches dist al p or t ion s pass u n der th e ten toriu m an d th u s requ ire t ran s-
• Thalamogeniculate arteries ten torial or in fraten torial su rgical approach es.
• Lateral posterior choroidal
• Middle temporal artery
• Posterior temporal artery
Anterior Inferior Cerebellar Artery
P3: Posterior border of the midbrain to calcarine fissure
Branches (equate to P4 segments) Th e segm en t s as w ell as th e relevan t bran ch es of th e AICA are
• Parieto-occipital artery d escr ibed in Table 57.2. Th e fou r segm en t s are t h e an ter ior
• Calcarine artery p on t in e, lateral p on t in e, floccu lop ed u n cu lar, an d cor t ical (Fig.
• Splenial arteries* 57.3).15 Given th at th e m ajorit y of AICA an eur ysm s are located
arou n d t h e in ter n al acou st ic m eat u s, st an dard su rgical ap -
*Typically arise as secon dar y bran ch es.
PCoA, posterior com m u nicat ing ar ter y.
proach es to th e cerebellop on t in e angle gen erally su ffice to t reat
th ese lesion s.

Fig. 57.2 Illustration of the anatom ic segm ents (s1 to s4) of the SCA in the axial plane. Their relationship to the brainstem and cerebellum is dem on-
strated. PCA, posterior cerebral artery; SCA, superior cerebellar artery. (Courtesy of Barrow Neurological Institute.)

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664 V Cerebral and Spinal Aneurysms

Table 57.2 Superior Cerebellar Artery (SCA) and Anterior Inferior Cerebellar Artery (AICA) Segmental Anatomy

SCA AICA

Anterior pontomesencephalic segment Anterior pontine segment


s1: Origin to anterolateral margin of brainstem a1: Origin to midpoint of the inferior olive
Branches Branches
Direct perforating arteries Perforating arteries
Long and short circumflex
Lateral pontomesencephalic segment Lateral pontine segment
s2: Anterolateral margin of brainstem to cerebellomesencephalic fissure a2: Inferior olive to the flocculus
Branches Branches
Direct perforating arteries Labyrinthine arteries
Long and short circumflex Recurrent perforating
Marginal branch (50%) Subarcuate artery
Cerebellosubarcuate
Cerebellomesencephalic segment Flocculopeduncular segment
s3: Within the cerebellomesencephalic fissure a3: Flocculus to cerebellopontine fissure
Branches Branches
Direct perforating arteries Perforating arteries
Long and short circumflex Choroidal arteries
Precerebellar arteries
Hem ispheric arteries
Vermian arteries
Cortical segment Cortical segment
s4: Distal to the cerebellomesencephalic fissure a4: Distal to the cerebellopontine fissure
Branches Branches
Cortical arteries Cortical arteries

Fig. 57.3 Anatomic illustration of the anterior inferior cerebellar artery segm ents (a1 to a4) showing their relationships to the brainstem , cranial nerves,
flocculus, and cerebellar hem isphere. (Courtesy of Barrow Neurological Institute.)

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 665

■ Clinical and Radiographic Presentation


Th e m ajorit y of p at ien t s w ith an eu r ysm s involving th e PCA, SCA,
an d AICA presen t w ith subarach n oid h em orrh age.3,6,9,10,12,22,23
Characteristic clinical presentations of patients w ith posterior cir-
culat ion an eur ysm s, aside from th ose t ypical for subarach n oid
hem orrhages, are discussed below for each of the three m ajor ves-
sels. Generally, know ledge of the relat ionship of the paren t vessel
to th e brain stem an d exit ing cran ial n er ves is h elpful w h en diag-
nosing these an eur ysm s. Post traum atic an eur ysm s of th e PCA an d
SCA have also been reported in the literature and m ust be included
in th e differen t ial diagn osis w h en su barach n oid h em orrh age is
presen t in both pen et rat ing an d n onpen et rat ing injuries.24,25

Posterior Cerebral Artery


As exp ected, th e clin ical presen t at ion for p at ien t s w ith PCA an -
eu r ysm s cor relates w it h w h at segm en t is involved . Drake an d
Am ach er 6 in 1969 d escr ibed a con sisten t clin ical p resen t at ion
for th eir pat ien ts w ith proxim al PCA an eur ysm s. Alth ough th eir
pat ien ts w ith distal an eu r ysm s h ad n o con sisten t clin ical p re-
sen tat ion , th ose w ith saccu lar p roxim al an eu r ysm s all presen ted
w ith con t ralateral h em ip aresis an d a th ird cran ial n er ve palsy. Fig. 57.4 A superior cerebellar artery (SCA) aneurysm can be seen origi-
Oth er case series describe visual path ology from direct com pres- nating from the junction of the basilar artery and the SCA in this intraop-
sion or distal em boli, m em or y deficit s, an d seizu res as p resen t- erative photo. The posterior cerebral artery is in view above the dom e of
ing sym ptom s of PCA an eu r ysm s.22,23,26,27 the aneurysm , and cranial nerve III is visible on the right side just superficial
to the aneurysm . (Courtesy of Barrow Neurological Institute.)

Superior Cerebellar Artery


Th e an atom ic relat ion sh ip of th e PCA, SCA, an d CN III m akes a
cran ial n er ve deficit possible w h en proxim al an eur ysm s exist on
eith er of th ese vessels; th is deficit h as been repor ted as a p resen -
tat ion for pat ien t s w ith proxim al SCA an eur ysm s (Fig. 57.4).28 In
addit ion , th e SCA h as close an atom ic relat ion sh ips to CNs IV and
V, placing th ese n er ves at risk for com pression from an eu r ysm
form at ion . Trigem in al n eu ralgia h as been repor ted as a presen ta-
t ion of an u n r u pt u red SCA an eu r ysm .10 Lesion s localizing to th e
pon s h ave also been rep or ted as cau sing p resen t ing sym ptom s
sim ilar to an SCA an eu r ysm . Fu r th er, ocu lar bobbing, w h ich con -
sists of rapid conjugate dow nw ard deviat ion of th e eyes follow ed
by slow ret urn to m idposit ion , is a n onspecific fin ding th at h as
been repor ted as a p resen tat ion of an SCA an eur ysm .29

Anterior Inferior Cerebellar Artery


Many of th e p resen t at ion s u n iqu e to p at ien t s w ith AICA an eu -
r ysm s are a result of th e an eur ysm ’s in t im ate relat ion sh ip w ith
the internal acoustic m eat us. Pat ients w ith AICA aneur ysm s have
been repor ted to presen t w ith facial w eakn ess, h earing loss, ab -
norm al auditor y phenom ena, an d inappropriate lacrim ation . They
h ave also presen ted w ith com pressive sym ptom s of CNs V an d
XII.30 These cranial ner ve sym ptom s can h ave a sudden onset, t yp -
ically associated w ith a severe h eadach e in th e case of an eur ys-
m al hem orrh age, or sym ptom s m ay h ave a m ore in sidious course
as a result of m ass effect .
Th e radiograph ic presen t at ion for AICA an eu r ysm s is dich oto-
m ized based on w h eth er th ey are rupt ured or n ot . Pat ien ts w ith
Fig. 57.5 An axial noncontrast computed tom ography im age of the head
rupt ured an eur ysm s t ypically presen t w ith com puted tom ogra- showing hyperdensit y in the interpeduncular and ambient cisterns as well
p hy (CT) fin d ings of d iffu se hyp erd en sit y in t h e su barach n oid as the bilateral sylvian fissures, which is m ost consistent with aneurysm al
space an d basal cistern s (Fig. 57.5). Th is can be associated w ith subarachnoid hem orrhage. (Courtesy of Barrow Neurological Institute.)

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666 V Cerebral and Spinal Aneurysms

in t raparen chym al or in t raven t ricu lar hyp erd en sit y con sisten t
w ith acute hem atom a. The distribution of the subarachnoid hem -
■ Preoperative Evaluation
orrh age can occasion ally poin t to th e region of th e an eur ysm . In A neurologic exam ination of a patient w ith a posterior circulation
th e cases of PCA, SCA, an d AICA an eu r ysm s, th e su barach n oid aneurysm is required to have a com plete clinical picture on w hich
h em orrhage m ay be m ore prom in en t in th e posterior fossa. More to base t reat m en t recom m en dat ion s. Th e m ajorit y of pat ien ts
dist al an eu r ysm s m ay resu lt in in t rap aren chym al h em orrh age in w ith th ese an eu r ysm s presen t w ith su barach n oid h em orrh age,
th e occipit al lobe or cerebellu m , or in t raven t ricu lar h em orrh age an d it is im por tan t to un derst an d th e pat ien t’s fun ct ion al st at us
in th e four th or lateral ven t ricles. Mu ch less com m on ly, an eur ys- before m aking t reat m en t decision s.
m al h em orrh age can result in isolated in t racran ial h em orrh age, All an eur ysm pat ien ts require bilateral vessel im aging of th e
in t raven t ricu lar h em orrh age, or rarely su bdu ral h em atom a for- an terior an d posterior circulat ion before in ter ven t ion . An atom ic
m at ion . How ever, pat ien t s w ith rupt ured an eur ysm s do n ot al- variat ion s th at w ere described earlier in th is ch apter can h ave
w ays p resen t w ith large am ou n t s of su barach n oid h em orrh age. a sign ifican t im pact on t reat m en t decision s. In addit ion , it can
In su ch cases, m agn et ic reson an ce im aging (MRI) can be h elpfu l be valu able to in clude th e n eck as w ell as th e extern al carot id
du e to its su p erior sen sit ivit y over CT. In addit ion , MRI p rovides circulat ion in im aging st udies w h en dealing w ith com plex poste-
bet ter visualizat ion of th e brain paren chym a, skull base an at- rior circu lat ion an eu r ysm s. Th ese st u dies can be h elpfu l w h en
om y, an d par t ially or com pletely th rom bosed an eu r ysm s. t r ying to evalu ate th e pat ien t for poten t ial ext racran ial-to-in t ra-
Cerebral angiograp hy is st ill th e gold stan dard for th e diagn o- cran ial bypass opt ion s. Cerebral angiography can often provide
sis of in t racran ial an eu r ysm s (Fig. 57.6). How ever, tech n ological m ore valuable in form at ion th an CT an d m agn et ic reson an ce an -
im p rovem en t in dat a acqu isit ion as w ell as t h e p ost p rocessing giograp hy regard in g t h e flow dyn am ics in , as w ell as d ist al to,
of CT angiograp hy h as sh ifted th e diagn ost ic paradigm for spon - an an eu r ysm . In un ique cases, paren t vessel occlusion can also be
tan eous subarach n oid h em orrh age. Com parison s bet w een CT tested prior to open surgical t reat m en t . All pat ien ts sh ould also
angiography an d digit al subt ract ion angiography h ave sh ow n CT h ave st an dard CT or MRI to evaluate cistern al spaces, ven t ricle
angiography to be a reliable an d cost-effect ive diagn ost ic tool.31,32 size, any ch anges in th e brain p aren chym a, an d bony an atom y.
Many in st it u t ion s n ow rou t in ely u se CT an giograp hy for th e Decision s regarding cerebrosp in al flu id diversion an d sku ll base
in it ial evalu at ion of sp on t an eou s su barach n oid h em orrh age (Fig. approach es can be in flu en ced by in form at ion from th ese preop -
57.7). erat ive im ages. MRI can be of p ar t icu lar assist an ce w h en th ere
Unrupt ured aneur ysm s var y in appearan ce on im aging st udies are in dicat ion s th at th e an eur ysm m ay be par t ially th rom bosed
based on th e size, th e presen ce of th rom bu s, an d th e exten t of or t h ere is con cer n abou t em bolic com p licat ion s related to an
calcificat ion . PCA an d SCA an eu r ysm s are t ypically located p rox- an eur ysm .
im ally an d can p resen t as isod en se or hyp erd en se, t yp ically Preoperat ive m edical evalu at ion of all crit ically ill p at ien t s is
sm ooth , rou n d m asses located n ear th e ten torial in cisu ra. W h en advised prior to su rgical in ter ven t ion . Pat ien t s u n dergoing elec-
large or gian t th ey can exert a m ass effect on adjacen t brain an d t ive p rocedu res sh ou ld also be evalu ated by an in tern ist w h en
poten t ially cau se edem a. An eu r ysm s of th e AICA are m ore com - in dicated by age or m edical h istor y. Opt im izat ion of th e pat ien t’s
m on distally an d h ave been reported to m im ic cerebellopon t in e m edical com orbidit ies can reduce in t raoperat ive an d postopera-
angle t u m ors or in t ram eat al m asses.33,34 t ive risk.

a b

Fig. 57.6a,b (a) An anteroposterior angiogram of the posterior circulation with a large right S2-segm ent posterior cerebral artery aneurysm . (b) A lat-
eral angiogram of the sam e patient. (Courtesy of Barrow Neurological Institute.)

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 667
Fig. 57.7a,b (a) An axial computed tom ography (CT) angiogram showing
a large fusiform aneurysm of the right S2 segm ent of the posterior cerebral
artery. (b) A three-dim ensional reconstruction using the CT angiogram of
the sam e aneurysm . (Courtesy of Barrow Neurological Institute.)

a b

Plan n ing sh ou ld also in clu d e p rep arat ion s for in t raop erat ive sificat ion of th e PCA w as p u blish ed 7 ; th is classificat ion is easily
m on itor in g an d im agin g w h en in d icated . An eu r ysm p at ien t s defin able on digit al su bt ract ion angiograp hy an d provides gu id-
are rou t in ely m on itored w it h elect roen cep h alography as w ell as an ce for surgical m an agem en t (Table 57.1). Th e approach es best
som atosen sor y an d m otor evoked p oten t ials. Brain stem au d i- su ited for each su rgical segm en t of th e PCA are su m m arized in
tor y evoked resp on ses an d facial n er ve m on itor ing m ay also Table 57.3.
provid e valu able in t raop erat ive in form at ion d u ring ap p roach es
to th e p osterior fossa t h rough t h e cerebellop on t in e angle. Visu al
S1 Segment
evoked p oten t ials h ave been sh ow n to be of lim ited u t ilit y bu t
are opt ion al. W h en con sid er in g vascu lar access for in t raop era- W h en app roach ing th e S1 segm en t of th e PCA along th e sph e-
t ive an giograp hy, a rad iolu cen t sku ll clam p an d flu oroscop e n oid w ing, th e cran ial-caudal locat ion of th e an eur ysm gen erally
m u st be available. In an t icip at ion of in docyan in e green (ICG) d ict ates w h eth er or n ot rem oval of th e orbit al bar an d zygom a
angiograp hy, it is h elp fu l to review t h e op erat ing m icroscop e is n ecessar y. Lesion s w ith in 5 m m of th e dorsum sellae are gen -
filter set t ings an d en su re th at th e ICG is available in th e operat- erally ap proach able w ith a st an dard pterion al ap proach . High er
ing room . lesion s can requ ire an orbitozygom at ic ap p roach , an d low er
Th e m ost im p or t an t con sid erat ion w h en evalu at in g t h ese lesion s are ap p roach ed via a tem p orop olar or t ran scaver n ou s
an eur ysm pat ien ts preoperat ively is to un derstan d th e an atom y exp osu re. How ever, w it h t h e d eep w orking d ist an ce for a PCA
of th e segm en t of th e paren t ar ter y involved. Th is is crit ical for an eu r ysm , in alm ost all cases it can be h elp fu l to rem ove t h e
in terpret ing th e risk of differen t t reat m en t opt ion s to exclu de
th e an eur ysm from th e circu lat ion .
Table 57.3 Surgical Approaches to the Posterior Cerebral Artery
Segments

■ Surgical Approaches Segment Surgical Approach

S1 Pterional
Posterior Cerebral Artery Orbitozygomatic
Th e an atom ic segm en t s of th e PCA pu blish ed by Zeal an d Rh o- Transzygom atic
ton 21 are invalu able for u n derst an ding an d com m u n icat ing th e Temporopolar
locat ion of an eur ysm s in relat ion to th e cerebrum as w ell as th e S2 Subtemporal
n orm al irrigat ion of th e PCA. How ever, th ese segm en ts do n ot Transsylvian transchoroidal
t ran slate w ell in to surgical division s of th e PCA w h en discu ssing Transtemporal transchoroidal
S3 Occipital interhemispheric
exposure ach ieved w ith var ying ap p roach es. Addit ion ally, th e
Supracerebellar infratentorial
an atom ic segm en ts are based on relat ion sh ips th at are difficu lt
Supracerebellar transtentorial
to define on angiography. For this reason, as noted, a surgical clas-

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668 V Cerebral and Spinal Aneurysms

orbital bar an d fron t al process of th e zygom a, via th e m odified bilizing th e tem poral pole w ith out com prom ising th e drain age
orbitozygom at ic ap p roach .35 Th is m od ificat ion p rovid es m ore of th e sylvian vein s in to th e sph en opariet al sin u s.36 To begin , an
ligh t as w ell as sligh tly bet ter angles for in sert ion of su ct ion , dis- orbitozygom at ic cran iotom y is perform ed w ith par ticular at ten -
sectors, an d clip ap pliers. t ion paid to exten d ing th e bony rem oval over th e tem p oral t ip
For both pterion al an d orbitozygom at ic cran iotom ies, th e p a- an d dow n to th e m iddle fossa floor. Th e du ra is th en elevated off
t ien t posit ion ing is th e sam e. Th e pat ien t is su pin e on a st an dard th e m iddle fossa floor to th e foram en sp in osu m . Th e m iddle
su rgical table w ith th e h ead t u rn ed 15 to 20 d egrees to th e con - m en ingeal ar ter y is coagu lated an d divided at th e sku ll base an d
t ralateral sid e an d exten ded. On ce th e cran iotom y is com p leted, th e du ra is fu r th er elevated u p to th e foram en ovale. An terolater-
a w ide open ing of th e sylvian fissure is n ecessar y to create an ally, th e dura is elevated u p to th e m en ingo-orbit al ar ter y, w h ich
aper t ure for deeper dissect ion w ith out sign ifican t ret ract ion of t yp ically cor respon ds to th e begin n ing of th e su per ior orbit al
eith er th e fron t al or tem poral lobes. In t rad u ral rem oval of th e fissure an d th e foram en rot u n dum . An terom edially, th e dura is
an terior clin oid is alm ost un iversally perform ed for an eu r ysm s elevated off t h e floor of t h e fron t al fossa to t h e opt ic can al. A
of th e basilar apex or p roxim al PCA. Th e clin oidectom y provides d iam on d bu r is th en used to flat ten th e sph en oid w ing an d any
th e surgeon access to open the distal du ral ring an d im prove th e irregularit ies in th e fron t al fossa, orbit al roof, an d m iddle fossa.
m obilit y of t h e in ter n al carot id ar ter y. Th is can h elp to red u ce Th e opt ic can al is u n roofed, an d an ext radu ral an terior clin oidec-
t h e n eed for m an ip u lat ion of t h e ocu lom otor n er ve if t h e in - tom y is perform ed. Th e superior orbit al fissure is skeleton ized,
ter n al carot id ar ter y m obilizes w ell an d is n ot burden ed w ith as is th e secon d division of th e t rigem in al n er ve in th e foram en
ath erosclerosis. On ce th e clin oidectom y is p erform ed, th ere are rot un du m . All of th is bony rem oval en ables m obilizat ion of th ese
th ree m ain corridors th at can be explored to gain access to th e skull base st r u ct ures on ce th e d ura is op en .
basilar t ru n k an d PCAs (Fig. 57.8). Th e m ost lu xu riou s exp osu re After th e ext radural drilling is com plete, at ten t ion is ret urn ed
is u su ally obt ain ed by w orkin g lateral to t h e in ter n al carot id to th e m en ingo-orbital ar ter y, w h ich is coagulated an d divided,
ar ter y. Un for t u n ately, t h is requ ires t h at t h e t h ird cran ial n er ve creat ing a plan e at th e apex of th e superior orbital fissure be-
be m an ip u lated an d t ypically h eld laterally to gain access to th e t w een th e du ra p rop ria an d th e p eriorbital fascia. Th is dissect ion
PCA. Th e opt icocarot id t riangle can be explored, bu t it t ypically plan e is open ed sh arp ly along th e su p erior orbit al fissu re over
is a lim ited sp ace com pared w ith th at bet w een th e in tern al ca- th e foram en rot u n du m to th e p osterolateral border of foram en
rot id ar ter y an d ocu lom otor n er ve. Above th e bifu rcat ion of th e ovale. Th e dura is elevated posteriorly along th e w all of th e cav-
in tern al carot id ar ter y is an oth er p oten t ial sp ace, bu t it is t ypi- er n ou s sin u s, leavin g t h e n er ve sh eat h s an d caver n ou s m em -
cally crow ded w ith perforat ing ar teries th at sh ou ld n ot be seri- bran e in t act (Fig. 57.9). Any ven ou s bleeding from th e cavern ou s
ally m an ipulated. After th e intern al carot id ar ter y is m obilized, sin u s can be con t rolled w ith h em ostat ic produ cts. Du ral dissec-
th e PCoA can be t raced an d u pon op en ing Liliequ ist’s m em bran e t ion is com p lete on ce th e th ird d ivision of th e t rigem in al n er ve,
th e P1-P2 ju n ct ion can be iden t ified. Th e PCA can th en be fol- w h ich exits th e foram en ovale posteriorly, an d th e m edial edge
low ed back to t h e basilar ar ter y an d th e con t ralateral PCA can of th e ten torium h ave been exposed. Th e m edial ten torial in ci-
be dissected out . If a m ore in ferior exposure is n ecessar y, th en a su ra is open ed sh arp ly n ext to th e th ird n er ve to discon n ect it
posterior clin oidectom y can be perform ed. Fu r th er exposu re can from th e cavern ou s sin u s m em bran e. Th e tem p oral lobe is n ow
be ach ieved by drilling of th e dorsu m sellae. m obilized, an d th e du ra over th e sylvian fissu re is op en ed dow n
Th e tem p orop olar ap p roach to PCA an eu r ysm s u ses a t ran s- to th e opt ic n er ve an d t h en fron t ally for 2 to 3 cm . Th e carot id
cavern ous exposure th at in creases th e su rgical exposu re by m o- du ral ring is in cised laterally to m obilize th e ar ter y. Th e sylvian

Fig. 57.8 Illustration of the three m ain surgical corridors


available to access the posterior circulation via a trans-
sylvian approach. ACA, anterior cerebral artery; CN, cranial
nerve; ICA, internal carotid artery; MCA, middle cerebral
artery; PCA, posterior cerebral artery; PCoA, posterior
com m unicating artery; SCA, superior cerebellar artery.
(Courtesy of Barrow Neurological Institute.)

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 669
Fig. 57.9 Illustration of right-sided orbitozygom atic crani-
otomy and extradural dissection for a temporopolar approach.
CN, cranial nerve. (Courtesy of Barrow Neurological Institute.)

fissure is th en split w idely, an d th e cavern ou s sin u s is op en ed S2 Segment


bet w een th e oculom otor an d t roch lear n er ves. Th is en ables th e
oculom otor n er ve to be m obilized from its origin all th e w ay to Approaches along the sph enoid ridge are less favorable for access-
th e su p erior orbit al fissu re (Fig. 57.10). A p osterior clin oidec- ing the second surgical segm ent of the PCA. Instead, accessing th e
tom y, w ith or w ith ou t drilling of th e dorsu m sellae, can be p er- S2 segm en t requ ires a m ore lateral app roach . Th e su btem poral
form ed w h en n ecessar y.36,37 Th e sam e aper t ures used du ring th e exp osu re of th e PCA for th e m an agem en t of an eu r ysm s w as u sed
pterion al or orbitozygom at ic ap proach are available to access t h e exten sively by Drake an d Am ach er.6 Th e p at ien t is p osit ion ed su -
S1 segm en t of th e PCA. pin e an d th e h ead is t u rn ed alm ost com p letely lateral. A tem p o-

Fig. 57.10 Illustration of the surgical view provided by a


temporopolar approach. Mobilization of the temporal lobe
and rem oval of the anterior and posterior clinoid pro-
cesses provides a larger window to access the posterior
circulation. BA, basilar artery; CN, cranial nerve; ICA, inter-
nal carotid artery; PCA, posterior cerebral artery; PCoA,
posterior communicating artery. (Courtesy of Barrow Neu-
rological Institute.)

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670 V Cerebral and Spinal Aneurysms

Fig. 57.11 A subtemporal exposure is illustrated showing


access to the basilar tip, PCA, and SCA. A basilar tip aneu-
rysm is shown in relationship to cranial nerve III, the PCoA,
and proximal perforators off of the PCA. CN, cranial nerve;
PCA, posterior cerebral artery; PCoA, posterior com m uni-
cating artery; SCA, superior cerebellar artery. (Courtesy of
Barrow Neurological Institute.)

ral cran iotom y is perform ed ju st in fron t of th e ear an d th e bony su re of th e am bien t cistern is p erform ed w ith th e sam e tech n iqu e
rem oval is exten ded dow n to be flush w ith th e m iddle fossa described above. W h en op erat ing th rough th e ven t ricu lar sys-
floor. W h en n ecessar y, th e bon e of th e posterom edial t riangle tem , h em ost asis is essen t ial to preven t in traven t ricular h em or-
can be rem oved to im p rove exp osu re in to th e posterior fossa. rh age an d p ostop erat ive hyd rocep h alu s. Care m u st be t aken to
Th e du ra is th en op en ed an d th e tem poral lobe is elevated (Fig. avoid excessive m an ip u lat ion of t h e h ip p ocam p u s, w h ich can
57.11). Th e m ain con cern w ith th is approach is th e risk of avu l- resu lt in su bep en dym al h em or rh age. Th e an ter ior ch oroidal
sion inju r y to th e vein of Labbé w h en it en ters th e t ran sverse ar ter y m u st also be given p rop er at ten t ion to avoid inju r y or
sigm oid ju n ct ion . Dissect ion along th e m iddle fossa floor to th e vasospasm .
edge of th e ten toriu m en ables iden t ificat ion of th e fou r th cran ial
n er ve. The ten toriu m can th en be in cised an d coagu lated to gain
S3 Segment
bet ter access to th e PCA in th e am bien t cistern .38
Du e to t h e r isk of ven ou s inju r y an d t h e associated com p li- Th e S3 segm en t of t h e PCA is t yp ically exp osed w it h an occip i-
cation s w ith th e su btem poral ap proach , t ran stem p oral opt ion s t al in terh em isph eric approach . Th e ideal posit ion ing is th e park
h ave gain ed p op u lar it y. Th ese in clu d e t h e t ran ssylvian t ran s- ben ch posit ion , w h ich en ables th e pat ien t to be rotated m ore
ch oroidal an d th e t ran scor t ical t ran sch oroidal ap p roach es (Fig. pron e for th e open ing an d m ore lateral for th e in t radural dissec-
57.12). Th e m ain crit icism of th ese approach es is th e h igh risk of t ion . Th e cran iotom y sh ou ld cross th e su perior sagit t al, t ran s-
injur y to p or t ion s of th e opt ic radiat ion s foun d in th e w all of th e verse, an d con flu en ce of sin uses (Fig. 57.13). Th is en ables th e
tem poral h orn . du ral op en ing to parallel th e falx an d th e ten toriu m , lim it ing any
For th e t ran ssylvian t ran sch oroidal ap p roach , th e p at ien t is ret ract ion on th e prim ar y visu al cortex. As a gen eral rule, th e
posit ion ed su pin e w ith th e h ead t u rn ed ~ 20 degrees. A fron to- side of in terest is depen den t to allow th e occip ital lobe to fall
tem poral cran iotom y is perform ed exposing th e sylvian fissu re aw ay from th e falx an d facilitate visualizat ion . Th e falx can be
an d m ore of th e tem poral lobe th an is rou t in e for a pterion al cra- follow ed dow n to the tentorial incisura w here the arachnoid over
n iotom y. Th e sylvian fissu re is sp lit w idely from th e lim en in su la th e qu adrigem in al cistern can be op en ed to exp ose th e proxim al
as far posteriorly as p ossible. Th e in su lar bran ch es of th e m iddle p or t ion of t h e S3 segm en t .40 Th e in tern al cerebral vein s m u st
cerebral ar ter y are m obilized an d t h e p ia of t h e tem p oral stem be id en t ified an d p reser ved du r ing t h is d issect ion , an d p reop -
is coagu lated an d open ed sh arp ly. A 2- to 3-cm cor t ical op en ing erat ive plan n ing sh ou ld aim to m in im ize th e n eed for su rgical
is m ade in to th e tem poral h orn of th e lateral ven t ricle. Th e ch o- m an ipu lat ion of th ese crit ical ven ou s st ruct ures.
roidal p oin t is iden t ified, an d th e am bien t cistern is en tered by Depen ding on th e locat ion of th e S3-segm en t p ath ology in re-
open ing th e ch oroidal fissure bet w een th e h ippocam pal fim bria lat ion to th e ten torial in cisu ra, th e su p racerebellar ap proach m ay
an d th e ch oroid plexus. Exposure can be exten ded an teriorly to be applicable. Th e pat ien t can be posit ion ed pron e w ith th e h ead
view th e cru ral cistern by m aking a sm all op en ing th rough th e flexed or in th e park ben ch posit ion w ith a m ilitar y ch in t uck.
un cus just an terior to th e ch oroidal poin t .39 Th e cran iotom y exp oses th e ipsilateral t ran sverse sin u s an d th e
Th e t ran scor t ical t ran sch oroidal ap p roach to th e am bien t cis- torcula. Dissect ion is along the su perior surface of th e cerebel-
tern avoid s exten sive sylvian fissu re d issect ion w it h t h e vascu - lu m u p to t h e ten tor ial in cisu ra. Th e ten tor iu m m ay be in cised
lar m an ipu lat ion th at is in h eren t w ith th is tech n ique. Cort ical or resected to p rovid e exp osu re of t h e an eu r ysm .41,42 Pat ien t
w indow s can be created in th e in ferior or m iddle tem poral gyrus select ion an d posit ion ing is crit ical for th is exposure to provide
or su lcu s. Th e cor t icotom y is m ad e 3 to 4 cm back from t h e an adequ ate aper t u re for m icrosurger y. Preop erat ive im ages can
tem poral t ip an d th e ven t ricle is at a depth of ~ 2.5 cm from th e reveal w h en an atom y is n ot favorable, such as a ver y steep ten to-
lateral cort ical surface.39 On ce th e ven t ricle is en tered, th e expo- riu m or low -lying torcula.

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 671

Fig. 57.12 A coronal illustration of the temporal lobe through the anterior sylvian transchoroidal approach (arrow A) and a transcortical transchoroidal
portion of the temporal horn of the lateral ventricle. Trajectories toward the approach (arrow B). (Courtesy of Barrow Neurological Institute.)
posterior cerebral artery (PCA) in the ambient cistern are shown from a trans-

Superior Cerebellar Artery Sp ecial at ten t ion m u st be paid to th e cran ial-cau dal locat ion of
t h e SCA an eu r ysm in relat ion to t h e d orsu m sellae w h en evalu -
Th e segm en t s of t h e SCA w ere d escr ibed earlier an d are su m -
at ing pat ien t s for m icrosurgical m an agem en t . Lesion s w ith in
m arized in Table 57.2. It is p ossible to exp ose th e m ajorit y of th e
5 m m of t h e d orsu m sellae are t yp ically can d idates for a pteri-
SCA th rough a single approach . A com bin ed supraten torial an d
on al, m od ified orbitozygom at ic, or orbitozygom at ic ap p roach .
in fraten torial presigm oid t ran sp et rosal app roach provides ac-
As t h e p ath ology descen ds, it becom es n ecessar y to m od ify t h e
cess to th e SCA origin , an terior an d lateral pon tom esen ceph alic,
approach to m atch th e locat ion of th e lesion . A tem poropolar
cerebellom esen cep h alic, an d p roxim al cor t ical segm en t s (Fig.
t ran scavern ou s app roach w ith resect ion of th e posterior clin oid
57.14).43 How ever, th is ap proach h as a h igh risk of com p rom is-
an d drilling of th e dorsum sellae m ay be required for low er lying
ing th e ven ous drain age of th e ip silateral tem p oral an d occipit al
an eur ysm s or th ose n ear th e s1–s2 ju n ct ion .
lobes. Approaches th at are m ore tailored to th e specific segm ents
of th e SCA offer adequ ate exposure w h ile redu cing risk; th ey are
s2 Segment
su m m arized in Table 57.4.
Th e s2 segm en t of th e SCA can be accessed u sing a su btem p oral
approach an d t ypically requires drilling of th e posterom edial t ri-
s1 Segment
angle, as m en t ion ed above. Th e pet rosectom y an d division of th e
Su rgical app roach es to th e s1 segm en t of th e SCA are th e sam e as ten torium provides m ore cau dal exposu re. Th e s2 segm en t can
th ose for th e p roxim al PCA, w h ich are discu ssed above in d et ail. also be exposed w ith a ret rosigm oid cran iotom y. Depen ding on

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672 V Cerebral and Spinal Aneurysms

Fig. 57.13 A craniotomy for an occipital interhemispheric approach


is illustrated. Clear visualization of the venous sinuses enables the
surgeon to m axim ize the dural opening and reduce the need for
retraction on eloquent cortex. (Courtesy of Barrow Neurological
Institute.)

Fig. 57.14 The exposure provided by a com bined subtempo-


ral and presigmoid approach is illustrated. The temporal bone
has been rem oved along with cranial nerve VIII. Cranial nerve
VII has been transposed and the tentorium resected after sac-
rifice of the superior petrosal sinus. The basilar trunk, anterior
inferior cerebellar, and SCA are visualized. BA, basilar artery;
CN, cranial nerve; ICA, internal carotid artery; SCA, superior
cerebellar artery. (Courtesy of Barrow Neurological Institute.)

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 673

Table 57.4 Surgical Approaches to the Superior Cerebellar Artery to allow brain sh ift to com plem en t th e su rgical exposu re. Th e
Segments ten torium can be in cised or a por t ion resected to visualize th e
Segment Surgical Approach
n ecessar y cor t ical segm en t of th e SCA.

s1 Pterional
Orbitozygom atic Anterior Inferior Cerebellar Artery
Temporopolar
Typ ically or igin at ing an ter ior to t h e p on s, t h e AICA is closely
s2 Temporopolar
associated w it h t h e foram en of Lu sch ka, cerebellop on t in e fis-
Subtemporal with/without anterior petrosectomy
su re, m idd le cerebellar p ed u n cle, an d p et rosal su r face of t h e
Retrosigm oid
cerebellum . Th e segm en ts of th e AICA are detailed in Table 57.2.
s3 Retrosigm oid
Supracerebellar infratentorial An eur ysm s of th e AICA are gen erally classified based on th eir
s4 Supracerebellar infratentorial relat ion sh ip to th e in tern al acou st ic m eat u s (IAM). Lesion s in -
Occipital transtentorial volving th e basilar–AICA jun ct ion , AICA bifurcat ion , an d com -
bin ed AICA–PICA origin are proxim al or prem eat al.44 An eur ysm s
of th e m eat al loop or segm en t are subclassified based on th eir
relat ion sh ip to th e IAM. Type I an eu r ysm s are en t irely ou t side of
th e pat ien t an d th e h an dedn ess of th e su rgeon , th is can be d on e th e IAM. Typ e II an eu r ysm s are p ar t ially w ith in th e IAM. Type III
w ith th e pat ien t in th e su pin e or lateral posit ion . Exposing th e an eur ysm s are en t irely w ith in th e IAM.45 Th e m ore of th e an eu -
con t ralateral side to th e h an dedn ess of th e su rgeon is t yp ically r ysm th at resides in side th e IAM, th e m ore drilling is required to
acceptable in th e supin e posit ion . Lateral is preferable w h en th e exp ose th e lesion , an d th e m ore tech n ically difficu lt t h e case be-
side of exp osu re is th e sam e as t h e h an d ed n ess of t h e su rgeon com es. Post m eat al an eu r ysm s are all th ose dist al to th e m eat al
or w h en th e pat ien t h as lim ited n eck m obilit y. Th e cran iotom y loop. Surgical approach es to th e segm en ts of th e AICA are pre-
sh ou ld exp ose th e t ran sverse sigm oid ju n ct ion , an d th e su rgeon sen ted in Table 57.5. Given th e variabilit y in th e locat ion of th e
m ust be prepared to address any violat ion s in to th e m astoid air origin of th e AICA, careful in spect ion of preoperat ive im aging is
cells. Typically bon e w ax or a local m uscle/fat graft along w ith n ecessar y to ch oose th e appropriate approach . In par t icular, th e
t igh t d u ral closu re is su fficien t to p reven t p ostop erat ive cere- cran ial cau dal locat ion of th e an eur ysm in relat ion to th e clivus
brospin al fluid leaks. In t radu ral dissect ion is along th e pet roten - an d th e m edial lateral locat ion from m idlin e m u st be t aken in to
torial jun ct ion . Th e arach n oid of th e t rigem in al cistern can be con siderat ion .
open ed w ith care to preser ve th e superior pet rosal vein . Th is An eur ysm s of th e AICA origin off of a m idlin e basilar ar ter y
provides access to th e lateral pon tom esen cep h alic (s2) an d cer- can be app roach ed d irectly th rough th e clivu s. Th is t ran sfacial
ebellom esen ceph alic (s3) segm en ts of th e SCA. With brain relax- t ran sclival ap p roach h as been d escribed for vascu lar lesion s of
at ion or ret ract ion on th e cerebellu m , bridging vein s often tear. th e basilar t r u n k bu t is gen erally reser ved for cases in w h ich a
Th is bleeding is t ypically from th e su p erior su rface of th e cere- com bin ed su btem p oral-presigm oid or a far-lateral ap p roach are
bellu m an d can best be d ealt w it h u sing top ical h em ost at ics u n favorable. Pat ien t s are posit ion ed supin e. Typ ically a lateral
an d ligh t pressure. In cases in w h ich th e superior pet rosal vein is rh in otom y in cision is m ade, an d th e n ose is disar t icu lated an d
severely lim it ing exposu re, it can be sacrificed w ith a relat ively folded laterally. Th e m idlin e sin uses are resected as n eeded to
low risk of ven ou s com plicat ion s. Th is is p referable to risking gain access to th e clivus. Har vest of a n asal septal m ucosal flap is
avulsion from th e su perior pet rosal sin us w h ile at tem pt ing an - u seful for recon st ruct ion . Th e clivus can be resected w ith a dia-
eu r ysm al d issect ion . W h en ever p ossible, th e arach n oid arou n d m on d bur an d rongeu rs to gain access to th e basilar t run k.46
the seventh and eighth cranial ner ve com plex is left intact to help Clival resect ion is lim ited laterally by th e carot id arteries superi-
preven t t ract ion injur y. orly an d th e hypoglossal can als in feriorly. Inju r y w ith th e dural
open ing to th e basilar ar ter y an d an eur ysm m ust be avoided.
s3 and s4 Segments Lim it ing coagulat ion of th e dura or a du ral graft can assist in ob -
tain ing a w ater t igh t closu re.
In addit ion to the retrosigm oid approach, the s3 and s4 segm ents
can be exp osed u sing a su p racerebellar in fraten torial app roach .
Th e p osit ion ing is th e sam e as m en t ion ed above for S3-segm en t Table 57.5 Surgical Approaches to the Anterior Inferior Cerebellar
PCA an eur ysm s. Th e cran iotom y sh ould cross th e ipsilateral Artery Segments
t ran sverse sin us an d visu alize th e torcula. W h en n ecessar y, th is
Lesion Location Surgical Approach
approach can be t ran slated laterally w ith a param edian in cision
th at en ables visu alizat ion of th e su p erior su rface of th e cerebel- Premeatal Transclival
lum as w ell as th e petrotentorial junction. Th is exposure can h elp Pterional or orbitozygom atic with or without
facilitate obtain ing proxim al con t rol for m ore distal an eur ysm s posterior clinoidectomy
of th e SCA. Subtemporal with petrosectomy and division of
In cases w h ere a su p er ior t rajector y to th e s4 segm en t is the tentorium
favorable, th is segm en t can be exposed via an occipit al t ran sten - Meatal Translabyrinthine
torial ap proach . Th is is p ar t icu larly su ited for m idlin e path ology, Retrosigmoid
Combined presigmoid
but exposure for m ore lateral cor t ical an eur ysm s is possible w ith
Postmeatal Retrosigmoid
a con t ralateral t ran sfalcin e t ran sten torial m odificat ion . As m en -
Far lateral
tion ed for distal PCA aneur ysm s, th e patient position ing is lateral

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674 V Cerebral and Spinal Aneurysms

For AICA an eu r ysm s th at are par t icu larly h igh riding on th e


clivus, the pterional, orbitozygom atic, and subtem poral approaches
■ Microsurgical Technique
h ave been used. Th e pterion al an d orbitozygom at ic approach es Modern vascu lar n eu rosu rger y h as requ isite in st ru m en t at ion
t ypically require a p osterior clin oidectom y, w h ereas a pet rosec- beyon d w h at is requ ired for a basic cran iotom y. Most n otable is
tom y is t ypically paired w ith th e subtem poral exposure. Th ese th e op erat ing room m icroscop e. Facilit y w ith th is tool is crit ical
approaches are det ailed in th e previous discussion of su rgical for perform ing n eu rosu rgical procedures safely an d efficien tly.
approaches to PCA an eur ysm s. Th e addit ion of paired n eu ron avigat ion an d in d ocyan in e green
In som e cases, a com bin ed su btem p oral-p resigm oid ap p roach angiography dem an d th at th e n eurosu rgeon’s un derst an ding of
can be u sed to access th e p rem eat al an d m eat al segm en t s of th e th ese tools evolve along w ith th e tech n ology. Th e recording ca-
AICA (Fig. 57.14). Pat ien t s can be p osit ion ed su p in e w it h a pabilit ies of th ese in st ru m en ts h ave also con t in u ed to im prove,
sh ou lder roll, or in th e lateral or park ben ch p osit ion , depen ding and high-definition or three-dim ensional video is a pow erful tool
on surgeon preferen ce. A lin ear ret rom astoid in cision is exten ded for teach ing residen t s an d for providing con t in uing m edical edu-
cran ially an d cur ved an teriorly to provide adequate exposure. cat ion . Alth ough a th orough discu ssion of m icrosu rgical in st ru -
Th e m astoid is drilled out w ith a com bin at ion of cut t ing an d dia- m en tat ion is out side th e scope of th is ch apter, it is w or th n ot ing
m on d bu rs to expose Trau t m an n’s t riangle. If a t ran ssigm oid ap - th at th e prop er p rep arat ion an d kn ow ledge of th is in st r u m en -
proach is requ ired , th e cran iectom y is exten ded p osteriorly to t at ion is crit ical w h en perform ing vascu lar n eu rosurger y.
th e ret rosigm oid du ra. A su btem p oral cran iotom y is p erform ed, Su rgical ap proach es to t h e variou s segm en t s of th e PCA, SCA,
an d th e dura is open ed an terior to th e sigm oid sin u s up to th e an d AICA w ere discu ssed above. Gen eral prin ciples of vascular
sin odu ral angle. Th e su perior p et rosal sin u s is sacrificed, an d th e dissect ion app ly w h en exp osing cerebral an eu r ysm s. W h en ever
ten torium is divided w ith care to preser ve th e four th cran ial possible, sh arp dissect ion is p referred to redu ce th e risk of avu ls-
n er ve at th e ten torial edge.47 Th is provides adequ ate visu aliza- ing a fresh clot or to redu ce th e t ract ion pu t on arach n oid adh e-
t ion of th e p rem eat al an d m eatal segm en ts. W h en a su btem p oral sion s to th e an eur ysm d om e, w h ich can cau se r upt u re. Proxim al
cran iotom y is n ot requ ired, the presigm oid alon e or a t ran slaby- con t rol sh ou ld be th e p riorit y in all early dissect ion s, bu t esp e-
rin th in e ap p roach can p rovide access to th e m eat al segm en t of cially so in th e case of ru pt ured an eur ysm s.
th e AICA. An eu r ysm n eck d issect ion is u su ally facilit ated by t racing
An eu r ysm s of th e p ost m eat al segm en t of th e AICA are acces- proxim al vessels. On ce th e an eu r ysm n eck is iden t ified, it is t ypi-
sible th rough a ret rosigm oid or far-lateral ap proach (Fig. 57.15). cally preferable to proceed to iden t ify ou tflow vessels p rior to
Th e ret rosigm oid ap p roach is d iscu ssed above. Th e far-lateral aggressive an eu r ysm dissect ion . After defin ing th e p roxim al an d
exp osu re exten d s t h e ret rosigm oid bony rem oval t h rough t h e dist al an atom y, dissect ion of th e an eu r ysm itself is perform ed,
foram en m agn u m an d skeleton izes th e sigm oid sin u s all t h e taking special care to iden t ify an d preser ve bran ch or perforat ing
w ay dow n to th e jugu lar bu lb. Th e ext radu ral ver tebral ar ter y ar teries. In th e case of an un ru pt ured an eur ysm , it is best to
m ust be iden t ified in th e suboccipit al t riangle. Part ial rem oval of com p letely m obilize th e an eu r ysm an d obt ain m axim al visu al-
the occipital condyle and jugular t ubercle constit utes the extrem e izat ion prior to clip ligat ion . For a r u pt u red an eu r ysm , it is often
lateral in ferior t ran scon dylar t ran st u bercu lar exposu re (ELITE) im possible to com pletely dissect ou t th e an eur ysm w ith ou t re-
an d provides m ore an terior exposure at th e level of th e foram en rupt uring it . In th ose cases, it is vital to h ave a com preh en sive
m agn um . u n derst an ding of th e pat ien t’s an atom y based on preoperat ive
im aging. Th is en ables th e surgeon to m in im ize t h e exten t of dis-
sect ion requ ired to defin e th e an eu r ysm n eck an d to facilitate
safe clipping. Preoperative im aging can also be used to at tem pt to
an t icipate clip con figurat ion s. How ever, th e larger th e an eur ysm ,
th e m ore difficu lt it can be to m ain t ain th e p aten cy of th e p aren t
vessel w h en t r ying to clip ligate it . Many differen t perm utat ion s
of clip placem en t h ave been described, an d it is im por tan t to
m ain tain flexibilit y du ring th e process of an eu r ysm occlu sion so
th at th e best result is obtain ed .

Revascularization
Large or fu siform an eur ysm s of th e proxim al PCA are often n ot
am enable to prim ar y clipping. Perforating arteries are frequently
em bedded in th e w alls of th ese an eu r ysm s, an d at tem pt s at clip -
ping or clip recon st ru ct ion can resu lt in brain stem or posterior
th alam ic in farct ion . Th ese lesion s are in dicat ion s for ext racra-
n ial-to-in t racran ial or in t racran ial-to-in t racran ial bypass proce-
du res.48,49 Revascu larizat ion distal to th e an eu r ysm an d th en
proxim al occlu sion en ables th e PCA p erforators to fill ret rograde
via th e bypass an d rem oves th e an terograde pressu re, decreasing
Fig. 57.15 Intraoperative photo of an anterior inferior cerebellar artery
aneurysm . The sixth cranial nerve is visible to the right of the suction tip th e risk of ru pt u re. Several don or vessels h ave been u sed to re-
and, m ore superficially, the seventh and eighth cranial nerves are visual- vascu larize th e PCA in cluding th e superficial tem poral ar ter y
ized. (Courtesy of Barrow Neurological Institute.) (STA), in tern al carot id ar ter y, m iddle cerebral ar ter y (MCA), SCA

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57 Microsurgical Managem ent of PCA, SCA, and AICA Aneurysm s 675

via a side-to-side an astom osis, an d m axillar y ar ter y.50–54 Bypass vein or rad ial ar ter y graft s to be u sed for an astom osis to t h e
procedu res from th e MCA, carot id ar ter y, an d m axillar y ar ter y SCA.57 Ad d it ion ally, t h e sid e-to -sid e an astom osis w it h t h e PCA
are t ypically perform ed u sing a radial ar ter y or saph en ous vein is a viable opt ion for revascularizat ion of eith er vessel.
graft s. An astom oses are t ypically p erform ed in a run n ing or in - Revascu larizat ion of th e AICA territor y is ver y rarely required
terrupted fash ion w ith 9-0 or 10-0 nylon su t u re. (Det ailed tech - given th e robu st an astom ot ic n et w ork of th e cerebellar arteries.
n ical descript ion s h ave been publish ed for bypasses using th e How ever, occipit al ar ter y byp ass is an opt ion in cases w h en th e
various don or vessels above.) More dist al an eu r ysm s of th e PCA AICA sup plies a larger-th an -n orm al territor y.58
th at are n ot t reat able w ith clip ligat ion are frequ en tly m an aged
w ith proxim al occlusion . How ever, th ere are robust collaterals to
th e PCA territor y, an d p ostop erat ive h em ian opsia occu rs in 10%
to 20%of pat ien t s un dergoing PCA occlu sion .55 Th e fur th er along ■ Clinical Outcomes
th e PCA th e occlu sion is p erform ed, th e h igh er th e rate of p ost-
Poster ior circu lat ion an eu r ysm s are tech n ically ch allen gin g le-
operat ive h em ian opsia. Th e PCA con n ect ion to th e posterior in -
sion s th at are id eally m an aged by a m u lt id iscip lin ar y n eu ro-
ferior tem poral lobe is believed to provide im por tan t collateral
vascular team . Th e con t in ual im provem en ts in tech n iques an d
circulat ion , an d occlusion beyon d th ose tem poral bran ch es also
m aterials en able con t in ued expan sion of th erapeut ic capabili-
resu lt s in h igh er p ercen t ages of p ostop erat ive visu al d eficit s.
t ies for en dovascu lar n eu rosu rgeon s. Th is environ m en t dem an ds
Revascularizat ion w ith th e occipital ar ter y for dist al PCA an eu-
th at th e clin ical ou tcom es from m icrosu rgical m an agem en t of
r ysm s is associated w ith a relat ively h igh com plicat ion rate an d
th ese an eu r ysm s rivals or exceeds th ose ach ievable w ith en do-
is cu rren tly n ot recom m en ded.55
vascu lar th erapy. Th e outcom es for th e m icrosurgical m an age-
An eur ysm s of th e proxim al SCA th at can n ot be m an aged w ith
m en t of PCA, SCA, an d AICA an eu r ysm s are listed in Table 57.6.
p r im ar y clip p ing m ay also be can didates for revascu lar izat ion .
St u dies of th e ou tcom es for PCA an eu r ysm s w ere p u blish ed
In gen eral, t h e SCA h as even bet ter collateralizat ion t h an t h e
from 1969 to 2005. Th e defin it ion of good ou tcom es var y from
PCA, an d t rapping or proxim al ligat ion is an opt ion for m an aging
st udy to st u dy, bu t , in gen eral, pat ien t s m u st h ave ret urn ed to
t h ese an eu r ysm s. How ever, t h e p roxim al SCA h as been sh ow n
act ivit ies of daily living w ith m in im al to n o assistan ce to be in -
to con t ain brain stem perforat ing ar teries in m ore th an 80% of
cluded in th is categor y. Most com m on ly, good ou tcom es w ere
cases.56 W h en con sidering proxim al ligat ion or t rapping, it is ap -
classified as a Glasgow Ou tcom e Scale score of 4 or 5. Th e m icro -
propriate to exp lore th e an eu r ysm al segm en t for any sign ifican t
su rgical m an agem en t of PCA an eu r ysm s resu lted in a good ou t-
perforating ar teries an d to be prep ared to revascu larize th e SCA
com e in 85 of 116 (73.3%) p at ien t s. Th is n u m ber is all th e m ore
territor y. It is also reason able, given th e risk of cerebellar in farct
im pressive con sidering th at in th ese st u dies 61 of 94 (65%) pa-
an d th e presen ce of perforators, to plan a bypass in any case in
t ien ts p resen ted w ith su barach n oid h em orrh age. Poor ou tcom es
w h ich th e SCA w ill be occluded. Th e SCA is a sm aller caliber ves-
from m icrosu rgical m an agem en t of PCA an eu r ysm s w as n oted in
sel th an th e PCA w ith an average diam eter of 1.38 m m in on e
31 of 116 (26.7%) an d 10 of 116 (8.6%) pat ien ts died.3,6,9,22,23,27,59,60
cadaveric st u dy.56 Given th e relat ively sm aller size, th e STA is
Microsu rger y for SCA an eu r ysm s resu lted in good ou tcom es
often used to revascularize th e SCA territor y (Fig. 57.16). How -
in 32 of 44 (72.7%) p at ien t s from t h e literat u re review ed in Table
ever, m any of th e sam e don or vessels th at are can didates for PCA
57.6. Th e m or t alit y rate w as 6.8%an d p oor ou tcom es w ere n oted
bypasses can be used for th e SCA. Tech n iques to taper dow n th e
in 12 of 44 (27.3%) p at ien t s w ith SCA an eur ysm s.9,28,61,62 An eu -
larger don or vessels h ave been pu blish ed an d en able saph en ou s
r ysm s of th e AICA resulted in 40 of 56 (71.4%) pat ien t s w ith good
clin ical ou tcom es, 16 of 56 (28.6%) w ith poor ou tcom es, an d a
m ort alit y of 3.6%.9,12,63,64 Based on a review of th e literat u re an d
exten sive su rgical experien ce, San ai et al9 recom m en ded m icro-
su rger y as th e p rim ar y th erapy for SCA, P1 PCA, an d d ist al AICA
an eur ysm s an d as secon dar y th erapy for P2 PCA an d proxim al
AICA lesion s.

■ Treatment Decisions
Th e decision to offer t reat m en t for an in t racran ial an eu r ysm var-
ies greatly, dep en ding on w h eth er th e an eu r ysm h as ru pt ured.
Rupt ured an eu r ysm s h ave a ver y poor n at u ral h istor y; th erapy
to exclud e th e an eur ysm from th e cerebral circulat ion sh ould be
aggressive. Th is ap p roach m ay be tem p ered for p at ien t s w it h
serious m edical com orbidit ies or ver y poor n eurologic stat u s
u pon presen tat ion . How ever, p at ien t s w ith r upt ured an eu r ysm s
sh ou ld gen erally be evalu ated for t reat m en t in a t im ely fash ion
Fig. 57.16 Intraoperative photo of an end-to-end anastom osis of the su-
by a n eurovascu lar team .
perficial temporal artery (STA) to the superior cerebellar artery (SCA). The
STA is superior to the left and the SCA is inferior to the right. The anasto - A few ran dom ized t rials h ave at tem pted to com pare clip liga-
m osis is being perform ed with a 10-0 nylon suture, as is standard practice. t ion to coil em bolizat ion for th e m an agem en t of in t racran ial an -
(Courtesy of Barrow Neurological Institute.) eur ysm s, but non e h as show n a statistically significant differen ce

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676 V Cerebral and Spinal Aneurysms

Table 57.6 Surgical Outcomes of PCA, SCA, and AICA Aneurysms

SAH Good Outcome Poor Outcome Mortality


Study, Year n/ N (%) n/ N (%) n/ N (%) n/ N (%)

Posterior cerebral artery


Drake and Amacherl, 1969 6 8/8 (100) 6/8 (75) 2/8 (25) 1/8 (12.5)
Chang et al, 1986 22 8/10 (80) 6/10 (60) 4/10 (40) 2/10 (20)
Sakata et al, 1993 59 8/10 (80) 7/10 (70) 3/10 (30) 1/10 (10)
Kitazawa et al, 2001 60 5/11 (45.5) 10/11 (90.9) 1/11 (9.1) 0/11
Taylor et al, 2003 27 12/30 (40) 24/30 (80) 6/30 (20) 1/30 (3.3)
Honda et al, 2004 23 5/7 (71.4) 4/7 (57.1) 3/7 (42.9) 0/7
Hamada et al, 2005 3 15/18 (83.3) 12/18 (66.7) 6/18 (33.3) 3/18 (16.7)
Sanai et al, 2008 9 (–) 16/22 (72.7) 6/22 (27.3) 2/22 (9.1)
Superior cerebellar artery
Peerless et al, 1996 62 (–) 9/10 (90) 1/10 (10) 1/10 (10)
Sanai et al, 2008 9 (–) 15/22 (68.2) 7/22 (31.8) 2/22 (9.1)
Jin et al, 2012 28 8/12 (66.7) 8/12 (66.7) 4/12 (33.3) 0/12
Anterior inferior cerebellar artery
Gonzalez et al, 2004 63 21/34 (61.8) 22/34 (64.7) 12/34 (35.3) 2/34 (5.9)
Sanai et al, 2008 9 (–) 6/8 (75) 2/8 (25) 0/8
Li et al, 2012 64 5/6 (83.3) 6/6 (100) 0/6 0/6
Tokimura et al, 2012 12 7/8 (87.5) 6/8 (75) 2/8 (25) 0/8
Abbreviations: PCA, posterior cerebral artery; SCA, superior cerebellar artery; AICA, anterior inferior cerebellar artery; SAH, subarachnoid hem orrhage

in clin ical outcom es at th e m ost recen t follow -up .65–67 W h en Outcom es from com bin ed approach es for th e m an agem en t of
com paring obliterat ion rates, th e pu blish ed literat u re est im ates com plex in t racran ial an eu r ysm s h ave been p resen ted in t h e lit-
th at en d ovascu lar t reat m en t ach ieves com p lete obliterat ion in erat u re. W h en con sidering all in t racran ial an eu r ysm s, a good
52 to 66% of cases.67–69 In con t rast , clip ligat ion ach ieves com - clin ical ou tcom e can be expected in m ore th an 80% of pat ien t s
plete an eu r ysm obliterat ion 80 to 90% of th e t im e.67,68 In addi- w h en a com bin ed ap proach is n ecessar y.73,74
t ion , several large cen ters h ave p u blish ed recan alizat ion rates
for en d ovascu lar t reat m en t of an eu r ysm s t h at range from 26 to
33%.70–72 Th e rer u pt u re rate of p ar t ially t reated or recan alized
an eu r ysm s after en d ovascu lar t reat m en t ap p ears to be low .
■ Conclusion
How ever, in p eer-review ed literat u re it h as been sh ow n to be An eur ysm s of th e PCA, SCA, an d AICA en t ail un iqu e con sider-
h igh er than th e rer upt ure rate for an eur ysm s t reated w ith clip at ion s for t reat m en t . Un d erstan d ing th e an atom ic segm en ts, lo-
ligat ion .66,67 cation of perforat ing vessels, anastom otic net w orks, and irrigation
Several variables are cr u cial to con sider w h en evalu at ing pa- en ables th e surgeon to ch oose th e correct ap proach an d surgical
t ien ts for t reat m en t . Based on data from th e In tern at ion al St u dy plan . Revascu larizat ion procedu res requ ire exten sive p reop era-
of Un rupt u red In t racran ial An eur ysm s (ISUIA), pat ien ts older t ive evalu at ion of im aging, an d con siderat ion s for don or vessels
th an 50 years, th ose w ith an eu r ysm s larger th an 12 m m , an d m ust be m ade on a case-by-case basis. An aggressive t reat m en t
th ose w ith p osterior circu lat ion an eu r ysm s w ere at a st at ist i- strategy is indicated for all patients w ith aneur ysm s w ho present
cally sign ifican t risk of w orse ou tcom e after cran iotom y th an w ith acute su barach n oid h em orrh age. Pat ien t s w ith u n rupt ured
other patients.69 For patients undergoing endovascular treatm ent, an eur ysm s m ust be assessed for t reat m en t based on th e pat ien t’s
an eur ysm s > 12 m m an d pat ien ts w ith posterior circulat ion an - age, sym ptom s, size of th e an eu r ysm , an eur ysm m orph ology,
eu r ysm s h ad w orse ou tcom es com p ared w ith p at ien t s w h o h ad fam ily h istor y, an d com orbid con dit ion s. Th e literat ure does n ot
an eur ysm s ≤ 12 m m or an eu r ysm s located in th e an terior circu- su p por t th e su p eriorit y of en dovascu lar or m icrosu rgical t reat-
lat ion .69 Clearly, th ere is n o ideal t reat m en t for large p osterior m en t for an eu r ysm s of t h e PCA, SCA, or AICA. Th ese com p lex
circulat ion an eu r ysm s; th us, a review by an experien ced m ult i- lesion s requ ire review by an exp er ien ced m u lt id iscip lin ar y
discip lin ar y n eu rovascu lar team is requ ired for all p at ien t s w ith n eu rovascular team , an d com bin ed approach es are an evolving
posterior circu lat ion an eu r ysm s. st rategy for t reat m en t .

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1011 44. Bam bakidis NC, Manjila S, Dash t i S, Tarr R, Megerian CA. Man agem ent
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diat rics 2011;42:204–206 88, discussion 88
25. Paiva WS, An drade AF, Sterm an Neto H, de Am orim RL, Caldas JG, Teixeira 46. Ogilvy CS, Barker FG II, Joseph MP, Ch en ey ML, Sw earingen B, Crow ell RM.
MJ. Traum at ic pseudoan eur ysm of th e su perior cerebellar arter y. J Traum a Tran sfacial t ran sclival ap p roach for m idlin e p osterior circu lat ion an eu -
Acu te Care Surg 2012;72:E115 r ysm s. Neu rosurger y 1996;39:736–741, discussion 742
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48. Kalan i MY, Ram ey W, Albuquerque FC, et al. Revascularizat ion an d an eu- 61. Wilkin s RH, Rengach ar y SS. Neurosu rger y. New York: McGraw -Hill; 1996
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era. Neu rosurger y 2014;74:482–497, discussion 497–498 Wilkin s R, Rengachar y SS, eds. Neurosurger y. New York: McGraw -Hill;
49. Kalan i MYS, Elh adi AM, Ram ey W, et al. Revascularizat ion an d pediat ric 1996:2341–2356
an eur ysm surger y. J Neurosurg Pediat r 2014;13:641–646 63. Gon zalez LF, Alexan der MJ, McDougall CG, Spet zler RF. Anteroin ferior cer-
50. Russell SM, Post N, Jafar JJ. Revascularizing th e upper basilar circulat ion ebellar ar ter y an eur ysm s: surgical approach es an d outcom es—a review of
w ith saph en ous vein graft s: operat ive tech n iqu e an d lesson s learn ed. 34 cases. Neurosurger y 2004;55:1025–1035
Surg Neu rol 2006;66:285–297 64. Li X, Zh ang D, Zh ao J. An terior in ferior cerebellar ar ter y an eur ysm s: six
51. Zador Z, Lu DC, Arn old CM, Law ton MT. Deep bypasses to th e dist al poste- cases an d a review of th e literat u re. Neu rosurg Rev 2012;35:111–119,
rior circu lat ion : an atom ical an d clin ical com parison of pretem poral an d discu ssion 119
subtem poral approach es. Neurosurger y 2010;66:92–100, discussion 100– 65. Koivisto T, Van n in en R, Hurskain en H, Saari T, Hern esn iem i J, Vapalaht i M.
101 Ou tcom es of early en d ovascu lar versu s su rgical t reat m en t of r u pt u red
52. Rodríguez-Hern án dez A, Huang C, Law ton MT. Superior cerebellar ar ter y- cerebral an eu r ysm s. A p rosp ect ive ran d om ized st u dy. St roke 2000;31:
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arter y revascularizat ion . J Neu rosurg 2013;118:1053–1057 66. Molyn eu x AJ, Kerr RS, Birks J, et al; ISAT Collaborators. Risk of recurrent
53. Sh i X, Qian H, K C KI, Zh ang Y, Zh ou Z, Sun Y. Bypass of th e m axillar y to subarach n oid h aem orrh age, death , or depen den ce an d st an dardised m or-
proxim al m iddle cerebral ar ter y or p roxim al p osterior cerebral ar ter y t alit y rat ios after clipping or coiling of an in t racran ial an eur ysm in th e
w ith radial arter y graft . Act a Neuroch ir (Wien ) 2011;153:1649–1655, In tern at ion al Subarach n oid An eur ysm Trial (ISAT): long-term follow -up.
discu ssion 1655 Lan cet Neurol 2009;8:427–433
54. Vish teh AG, Sm ith KA, McDougall CG, Spet zler RF. Dist al posterior cere- 67. Spet zler RF, McDougall CG, Albu querqu e FC, et al. Th e Barrow Rupt u red
bral arter y revascularizat ion in m ult im odalit y m an agem en t of com plex An eur ysm Trial: 3-year result s. J Neurosurg 2013;119:146–157
periph eral posterior cerebral arter y an eur ysm s: tech n ical case report . 68. Molyn eu x A, Kerr R, St rat ton I, et al; In tern at ion al Subarach noid An eu-
Neurosurger y 1998;43:166–170 r ysm Trial (ISAT) Collaborat ive Group. In tern at ion al Su barach n oid An eu-
55. Ch ang SW, Abla AA, Kakarla UK, et al. Treat m en t of dist al posterior cere- r ysm Trial (ISAT) of n eurosurgical clipping versus en dovascular coiling in
bral ar ter y an eu r ysm s: a cr it ical ap p raisal of t h e occip it al ar ter y-to- 2143 pat ien t s w ith rupt ured in t racran ial an eur ysm s: a ran dom ised t rial.
posterior cerebral arter y bypass. Neurosurger y 2010;67:16–25, discu s- Lancet 2002;360:1267–1274
sion 25–26 69. W iebers DO, W h isn an t JP, Hu ston J III, et al; In ter n at ion al St u dy of Un -
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tom ical st udy on th e “perforator-free zon e”: recon sidering th e proxim al an eu r ysm s: n at ural h istor y, clinical outcom e, an d risks of surgical an d
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using saph en ous vein bypass graft s for in t racran ial revascularizat ion pro- grap h ic recu rren ce. Rad iology 2007;243:500–508
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58. Fujim ura M, In oue T, Sh im izu H, Tom in aga T. Occipit al ar ter y-an terior in - after select ive en dovascular t reat m en t of an eur ysm s w ith det ach able
ferior cerebellar ar ter y byp ass w ith m icrosu rgical t rapp ing for exclu sively coils. St roke 2003;34:1398–1403
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subarachn oid h em orrhage. Case repor t . Neu rol Med Ch ir (Tokyo) 2012; lizat ion of cerebral aneu r ysm s: 11 years’ experience. J Neurosu rg 2003;
52:435–438 98:959–966
59. Sakat a S, Fujii K, Mat su sh im a T, et al. An eur ysm of th e posterior cerebral 73. Pon ce FA, Albu querqu e FC, McDougall CG, Han PP, Zabram ski JM, Spet z-
arter y: report of eleven cases—surgical approach es an d procedures. Neu- ler RF. Com bin ed en dovascular an d m icrosurgical m an agem en t of gian t
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J Clin Neu rosci 2001;8:23–26 eur ysm s. Neurosurger y 2003;52:263–274, discu ssion 274–275

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58 Endovascular Treatment of Vertebrobasilar
Circulation Aneurysms
Daniel W. Zum ofen, Eytan Raz, Mak sim Shapiro, Tibor Becske, Peter Kim Nelson, and How ard A. Riina

Ver tebrobasilar (VB) circulat ion an eur ysm s represen t 8 to 15%of from th e su boccip it al du ral ring to th e VB ju n ct ion w h ere th e
cerebral an eur ysm s. Basilar ar ter y (BA) t ip an eur ysm s are by far paired VAs fuse to form th e BA t r un k.
th e m ost frequ en t su bgrou p , accou n t ing for 51% of cases.1 High Th e cer vical VA h as a variable n u m ber of segm en t al sp in al
predisposit ion for ru pt u re is a ch aracterist ic feat u re of p osterior an d cer vical m u scular bran ch es, th e n u m ber an d disposit ion of
circulat ion an eur ysm s. Th e cum ulat ive 5-year risk of r upt ure is these bran ches being in hem odyn am ic balance w ith counterparts
2.5% for an eur ysm s sm aller th an 7 m m , an d 15% for an eu r ysm s arising from th e thyrocer vical an d costocer vical t r un k (e.g., ra-
equ al to or larger th an 7 m m .2 In cases of r u pt u re, VB circu lat ion diculospin al ar teries, radicu lom edullar y ar ter y). More dist ally, a
an eur ysm s h ave a par t icularly dism al progn osis w ith a sur vival variable set of m en ingeal bran ch es takes off w h en th e VA passes
rate of on ly 32% at 48 h ou rs.3 the suboccipital dural ring (e.g., posterior m eningeal arter y, arter y
Saccu lar VB circu lat ion an eu r ysm s likely arise du e to ch ron ic of th e falx cerebelli). Regarding th e in t radural por t ion , th e poste-
st ress cau sed by hyper ten sion or du e to environ m en t al toxin s rior inferior cerebellar arter y (PICA) and the anterior spinal arter y
su ch as sm oking. In con t rast , fu siform VB an eu r ysm s em body a are constant side branches, the posterior and lateral spinal arteries
com plex an d h eterogen eou s variet y of segm en t al ar terial w all deriving m ore often than not from the PICA. Finally, the in tradural
disease, likely reflect ing diversit y in et iology an d clin ical p resen - VA harbors a variable set of sh ort brainstem perforators providing
tat ion . Both path oan atom ic an d clin ical eviden ce suggests a dis- vascu lar supply to th e m edulla, olives, in ferior cerebellar pedun -
sect ing su bp opu lat ion th at ten d s to p resen t w ith h em orrh age or cles, an d via th e sp in al ar teries to th e u pper cer vical spin al cord.
acute ischem ia.4 How ever, the m ajorit y com e to clin ical at ten tion Ver tebral ar ter y an eu r ysm s m akeu p n early 5% of cerebral an -
eith er in ciden tally, or secon dar y to isch em ic st roke or m ass ef- eu r ysm s.7 Berr y-t ype an eur ysm s arising at th e origin of th e PICA
fect . Th ese an eur ysm s span a broad spect r um from dolich oect ic are discussed separately (see Posterior In ferior Cerebellar Ar ter y
to com plex, giant , often par t ially th rom bosed an eur ysm s w ith An eur ysm s, below ). Dissect ion is a com m on et iology of n on sac-
circum feren t ial ar terial w all involvem en t as a com m on defin ing cular VA aneurysm s. VA dissections w ith or w ithout ectasia (pseu-
at t ribu te. doan eu r ysm ) are fou n d eith er in ciden t ally on im aging, resu lt
In 1961, C.G. Drake,5 in t rodu cing invasive th erapy, p ion eered from t rau m a, or relate to an u n derlying con n ect ive t issu e disor-
direct su rgical clip p in g of VB an eu r ysm s. Th e in t rod u ct ion of der (e.g., Eh lers-Dan los syn drom e). Clin ical m an ifestations com -
t h e su rgical m icroscope to n eu rosu rger y by M.G. Yaşargil an d m only include neck pain. Low er cranial nerve (CN) palsy gen erally
P. Don aghy in th e late 1970s greatly in flu en ced th e su rgical re- result s from m ass effect in th e p resen ce of an expanding hem a-
su lts. Sin ce th e 1990s, en dovascu lar tech n iqu es gradu ally be- tom a or pseu doaneur ysm form at ion. In con trast to in tern al ca-
cam e a com p elling altern at ive. Over th e last decade, several large rot id arter y dissect ion , VA dissect ion s m ore frequen tly involve
t rials led to su pp or t of th e en dovascu lar app roach .6 Now adays, th e in t radu ral segm en t , an d h en ce m ay cau se su barach n oid
endovascular strategies are w ell established for an ever-increasing h em orrh age in case of rupt ure. Con ser vat ive m an agem en t in -
su bset of r u pt u red an d u n r u pt u red p osterior circu lat ion an eu - clu des th erapeu t ic an t icoagu lat ion or an t ip latelet t h erapy in
r ysm s (Fig. 58.1). com bin at ion w it h ser ial im agin g. Invasive t h erapy is con sid -
ered above all in cases w it h flow relevan t sten osis (h em odyn am ic
im pairm en t), progressive sym ptom s, in t radu ral exten sion , an d
progression on follow -u p im aging of a p seu doan eu r ysm . Inva-
sive th erapy in clu des d econ st ru ct ive st rategies su ch as su rgical
■ Vertebral Artery Aneurysms proxim al ligat ion an d t rap ping, as w ell as en dovascu lar balloon
Th e p aired ver tebral ar teries (VAs) derive from a set of longit u d i- or coil occlusion .8 Many su rgeon s favor en dovascu lar paren t ar-
n al in tercon n ect ion s bet w een prim it ive segm en tal precursors ter y sacrifice, par ticularly in th e elderly. Prior to decon st ru ct ion ,
n am ed th e prim it ive longit udin al n eural ar teries. Th e VA sub - th e presen ce of a com p eten t n et w ork of collaterals an d th e loca-
divides in to five dist in ct segm en t s. V1 d efin es th e m ost proxim al t ion of th e an terior spin al ar ter y origin are determ in ed by selec-
segm en t from th e su bclavian ar ter y to th e en t r y in to th e t ran s- t ive angiography (Fig. 58.2). Altern at ively, en dolum in al recon -
verse foram en of th e sixth cer vical ver tebra. V2 describes th e st r u ct ion u sing h igh -porosit y sten t s en ables th e su rgeon to tack
foram in al por t ion bet w een th e foram en t ran sversarium of th e dow n th e endoth elial flap w hile preser ving the parent arter y (Fig.
sixth cer vical vertebra to th e foram en t ran sversariu m of th e axis. 58.3).9 Given th e lim ited potential of h igh -porosit y sten ts for en -
V3 design ates th e su boccip it al par t w h ere t h e VA loops arou n d doth elial overgrow th , ou r grou p cam e to favor low -porosit y de-
th e lateral m ass of th e atlas u p to it s p assage th rough th e du ra vices for endolum inal reconstruction in selected cases. We have
of the posterior cranial fossa. V4 delineates the intradural section con sisten t ly obser ved rap id regression of m ass effect–related

679

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680 V Cerebral and Spinal Aneurysms

a b

Fig. 58.1a,b Cerebral angiography of the vertebrobasilar circulation. Right vertebral artery injection in arterial phase in anteroposterior (a) and lateral
views (b). A right anterior inferior cerebellar artery (AICA)–posterior inferior cerebellar artery (PICA) disposition is seen.

a b c d

Fig. 58.2a–d Deconstructive approach for a vertebral artery (VA) dissect- (MRA). (b) The aneurysm had spontaneously throm bosed when angiogra-
ing pseudoaneurysm. A 53-year-old wom an presented with clinical and phy was perform ed (arrow). (c) Given the adequate filling of the posterior
radiological progression of bilateral VA dissections despite therapeutic an- inferior cerebellar artery (PICA) via backflow from the right VA, the left VA
ticoagulation. (a) On the left side, a V4 dissecting pseudoaneurysm is seen was obliterated (arrow) using detachable coils (d).
(arrow) on initial tim e of flight (TOF) m agnetic resonance angiography

a b c d

Fig. 58.3a–d Reconstructive approach for vertebral artery (VA) dissecting viously sacrificed, the intim al flap was tacked down by a high-porosit y stent
pseudoaneurysm . On the right side, a distal V2 dissection with an intim al (Neuroform EZ, Stryker Neurovascular, Frem ont, CA). (c) The stent m arkers
flap (arrow) is illustrated by tim e of flight m agnetic resonance angiography (arrows) are best seen on unsubtracted angiography. (d) Following stent de-
(MRA) (a) and by angiography (b). Given that the contralateral VA was pre- ployment, the flap is reduced (arrow) and the arterial lumen is stabilized.

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58 Endovascular Treatment of Vertebrobasilar Circulation Aneurysms 681

a c e g

b d f h

Fig . 58.4a–h Reconstructive approach for vertebral artery–posterior (e,f) Multiple low-porosit y stent devices are deployed across the aneurysm
inferior cerebellar artery (VA–PICA) aneurysm . (a,b) Arterial phase cere- neck leading to (g,h) alm ost complete aneurysm obliteration and preserva-
bral angiogram and (c,d) three dim ensional (3D) reconstruction illustrate tion of the dom inant PICA.
a VA–PICA aneurysm with the dom inant PICA originating from its base.

sym ptom s, p reser vat ion of eloqu en t side bran ch es, an d perm a- rat in g bran ch es t h at ar ise p roxim al to t h e ch oroidal p oin t (top
n en t obliterat ion of pseu d oan eur ysm s (Fig. 58.4). of th e cran ial PICA loop), an d ch oroidal-t ype perforat ing bran ch es
Ru pt u red VA dissect ing an eu r ysm s represen t a th erapeu t ic th at su pp ly th e ch oroidal p lexu s of th e fou r th ven t ricle.13 Th e
em ergen cy due to a par t icularly h igh risk of recurren t h em or- m edu llar y-t ype p erforat ing bran ch es are of par t icu lar im p or-
rh age.4 Classic proxim al paren t ar ter y occlusion h as been associ- tan ce, as im pairm en t m ay result in th e devast at ing lateral m ed-
ated w ith the risk of retrograde flow in to the an eur ysm , resulting u llar y syn drom e described by A. Wallen berg. A dom in an t m ed-
in p ersisten ce of th e an eu r ysm an d poten t ial rebleeding.10 Ou r u llar y perforator con sisten tly arises directly from th e in t radural
preferen ce, th erefore, is for en d ovascu lar segm en t al decon stru c- VA in cases of ext radu ral PICA origin , an an atom ic varian t p re-
t ion . In ou r exp erien ce, sparing th e an terior sp in al ar ter y (w h ich ven t ing lateral m edu llar y in farct ion in case of PICA injur y.
arises preferen t ially from th e side of th e dom in an t PICA) pre- Th e PICA an eu r ysm s accou n t for 2% of brain an eu r ysm s an d
ven t s quadriparesis an d respirator y failu re.11 Fin ally, overaggres- arise in th e large m ajorit y of cases from th e VA–PICA jun ct ion .14
sive decon st r u ct ion (e.g., in th e absen ce of a com peten t n et w ork Com p licat ion s of op en su rger y p rim arily relate to direct or in -
of collaterals) m ay result in a cerebellar st roke large en ough to d irect (isch em ic) injur y of low er cran ial n er ves an d m edullar y
requ ire lifesaving su rgical decom pression . perforators. Im pairm en t of th e ch oroidal por t ion of th e PICA
ch aracterist ically rem ain s silen t (du e to th e abu n dan ce of col-
laterals from th e d ist al AICA an d SCA).15 Over th e last decade,
en dovascu lar m eth ods h ave gain ed p op u larit y for an in creasing
■ Posterior Inferior Cerebellar su bset of ru pt u red an d u n r u pt u red PICA an eu r ysm s. Proxim al
PICA an eu r ysm s su it able for direct coil em bolizat ion are defin ed
Artery Aneurysms by an appropriate dom e-to-n eck rat io and th e absen ce of elo-
Th e PICA resu lt s from t h e fu sion of a p roxim al m ed u llar y sec- qu en t bran ch es arising from th e an eu r ysm dom e or base.16 Bal-
t ion (con cept u ally an en larged lateral sp in al ar ter y) an d a dist al loon or sten t-rem odeling tech n iques are h elpful adjun ct s for
cor t ical segm en t (con cept u ally a coron ar y-t ype vessel th at h as m ore com plex con figurat ion an d proxim al PICA an eur ysm s.17
en larged to su p p or t t h e cerebellu m ’s n eed s). Th e p roxim al Over th e last few years, th e adven t of flow -diver ter devices h as
m ed u llar y-t ype por t ion com p rises an an terior m ed ullar y, lateral led to a paradigm sh ift affect ing part icu larly com plex VA–PICA
m edullar y, and a tonsillom edullar y segm ent. The distal coronar y- an eur ysm s (Fig. 58.4). Dist al PICA an eu r ysm s are com m on ly of
t ype p or t ion is su bdivided in to a teloveloton sillar segm en t (be- a dissect ing n at ure.18 Th us, direct coiling n early invariably re-
t w een th e tela ch oroidea an d th e in ferior m ed u llar y velu m ) an d su lts in recu rren ce over t im e. En dolu m in al recon st r u ct ion u sing
h em isph eric segm en t , m ost com m on ly com prising t w o term in al low -p orosit y sten t devices, bu t also th e u se of com plex coiling
branches that expand over the suboccipital cerebellar hem isphere techn iques such as balloon - or stent-rem odeling, rem ains at pres-
form ing a leptom en ingeal n et w ork of collaterals w ith adjacen t en t lim ited in t h e distal PICA segm en t s, given it s sm all diam eter
an terior in ferior cerebellar ar ter y (AICA) an d superior cerebellar an d th e in h eren t ar terial tort u osit y. With regard to en dovascular
ar ter y (SCA) bran ch es.12 Th e PICA h arbors m edullar y-t ype perfo- th erapy, d ist al PICA an eu r ysm s are preferen t ially addressed by

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682 V Cerebral and Spinal Aneurysms

decon st ru ct ive st rategies in clu ding en dovascu lar paren t ar ter y w ith sign ifican tly in creased m orbidit y an d m or talit y. Pat ien ts
coil occlu sion .18 Alter n at ively, op en su rger y rem ain s a valid op - w h o do n ot present w ith h em orrhage h ave a ver y low annual risk
t ion given t h at d ist al PICA locat ion s are read ily accessible by of r upt ure (1% per year for stable disease); even pat ien t s w ith
cran iotom y. en larging lesion s are m ore likely to develop st roke or m ass effect
rath er th an h em orrh age. Up to 40% of pat ien t s w ith n on h em or-
rh agic VB disease w ill die from variou s n on n eu rologic cau ses
th at are n ot over w h elm ingly card iovascu lar in n at u re, th u s p lac-
■ Vertebrobasilar Junction Aneurysms ing a h eavy prem ium on th eir overall m edical m an agem en t .21
Open surgical an d en dovascular t reat m en t opt ion s con sist of
Th e BA resu lt s from th e fu sion in th e m idlin e of th e p aired dorsal
decon st r u ct ive (paren t vessel sacrifice w ith or w ith ou t byp ass or
longit u din al n eu ral ar teries. Th e adu lt BA is divided in to th e
tourn iqu et ligat ion ), recon st ru ct ive (sten t ing, flow diversion ,
jun ct ion al segm en t , t run k, an d t ip. Th e BA side bran ch es in clude
coiling, an eu r ysm orrh ap hy, clipping), an d com bin at ion of m eth -
th e AICA (proxim al BA t ru n k) an d th e SCA (p roxim al to th e BA
ods.23–28 Un dou btedly, th ese lesion s in clude som e of th e m ost
t ip). Th e BA p erforators in clu de th e sh or t m edian , p aram edian ,
com p lex n eu rovascu lar cases (Figs. 58.5 an d 58.6). Desp ite re-
an d lateral circum feren t ial perforat ing bran ch es. W h ereas th e
cen t advan ces in th e risk-ben efit st at ist ics, our un derst an ding
m edian an d param edian pon t in e perforators directly pen et rate
rem ain s lim ited w ith regard to w h ich p at ien t s, an d u n der w h at
th e p on s an d exten d to th e floor of th e fou r th ven t ricle, th e lat -
circum stan ces, sh ou ld be offered a par t icu lar t reat m en t.29 W h en
eral circum flex branches encircle the anterior and lateral borders
it com es to invasive th erapy, th e relat ive in frequen cy of the dis-
of th e brain stem , w ith n um erous sm all perorat ing bran ch es en -
ease greatly im pairs acquisit ion of a m ean ingfu l operat ive expe-
tering th e pon s at righ t angles. Th e occlusion of th e t ran sverse
rien ce. In ou r opin ion , th e en orm ou s variabilit y in ou tcom e likely
pon t in e ar ter y, a dom in an t perforator arising from th e m idbasi-
relates to differen ces in u n derlying et iology, locat ion , exten t of
lar trunk, results in ventral pontine infarction associated w ith the
lesion , an d m eth od of t reat m en t . Bu t th e inven tor y of determ i-
devast at ing locked-in syn drom e.
n an ts of success or failure rem ain s for n ow un der debate, w ith
An eur ysm s involving th e VB jun ct ion are com m on ly of th e
recen t experien ce w ith flow diversion con t in uing a t ren d for
nonsaccular t ype. The natural history of these often large to giant
h igh variabilit y of outcom e.25,27 Th u s, it is likely th at in ter ven t ion
lesion s is best kn ow n th rough longit u d in al st u dies of th e Mayo
for VB jun ct ion an eur ysm s w ill rem ain for th e years to com e pri-
Clinic19,20 and Passero and Rossi21 cohorts, w h ere m ultiple factors
m arily con fin ed to ter t iar y cerebrovascu lar cen ters w ith exten -
related to size, grow th , m ode of p resen tat ion , an d com orbidit y,
sive en dovascu lar exp erien ce, based on em piric case select ion
am ong others, w ere addressed in relation to outcom e. From these
an d variable ou tcom es.
obser vat ion s, it appears th at n at ural h istor y is closely related to
index clinical presentation. Patients presenting w ith hem orrhage
ten d to do badly, an d th ose w ith in dex isch em ia h ave a variable
cou rse m arked by recu rren t st roke, w h ereas m ass effect carries a
particularly dism al prognosis.21,22 Patien ts w ith an incidental pre-
■ Basilar Tip Aneurysms
sen t at ion h ave a relat ively ben ign cou rse as long as t h eir lesion s The BA tip aneur ysm s are by far the m ost frequent subgroup of VB
rem ain m or p h ologically st able, w h ereas grow t h is associated circulation aneur ysm s. Microsurgical clipping of these aneur ysm s

a c e g i

b d f h j

Fig. 58.5a–i Reconstructive approach for vertebrobasilar (VB) dolichoec- ployment of m ultiple overlapping low-porosit y stent devices across the
tasia. (a,b) Cerebral angiogram illustrates a large fusiform dilatation includ- ectatic segm ent (g,h) results in im m ediate flow redirection as noted on
ing the dom inant left vertebral artery (VA) and the basilar artery (BA) trunk. angiogram s. (i,j) Over tim e, thrombosis and rem odeling allow for signifi-
(c) Magnetic resonance im aging (MRI) axial T1 and (d) sagit tal T2 show cant reduction of m ass effect.
partial throm bosis of the aneurysm and significant m ass effect. (e,f) De-

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58 Endovascular Treatment of Vertebrobasilar Circulation Aneurysms 683

a c e g

b d f h

Fig. 58.6a–h Reconstructive approach for basilar artery (BA) aneurysm . origin. (d) A high-porosit y stent (Neuroform EZ, Stryker Neurovascular,
(a) Cerebral angiography and (b) 3D reconstruction illustrate a giant BA Frem ont, CA) is then deployed to protect the BA trunk. (e,f) Complete
aneurysm . (c) Balloon-assisted (Hyperform , ev3 Neurovascular, Irvine, CA) obliteration is achieved. (g,h) Follow-up tim e of flight m agnetic resonance
coiling with preservation of the anterior inferior cerebellar artery (AICA) angiography (MRA) shows a rem odeled BA.

faces th e ch allenge of poor visualizat ion of key an atom ic st ru c-


tures in an exceptionally deep and narrow operative field. Further
■ Anterior Inferior Cerebellar
ch allenges for op en su rger y in clu de th e lim ited opt ion s for safe Artery Aneurysms
proxim al con t rol, an d th e frequ en tly ver y in t im ate relat ion be-
t w een th e an eu r ysm ’s back side an d h igh ly eloqu en t brain stem From a develop m en t al p oin t of view, th e AICA is an en larged
perforators. Given its com plexit y, op en su rger y en t ails con sider- brainstem perforator that captures variable am ounts of the cere-
able m orbidit y even in exper t h an ds.30 bellum hem odynam ic needs. Its territorial supply is in hem ody-
BA t ip an eu r ysm s are bifu rcat ion -t yp e an eu r ysm s, in m any nam ic balance w ith coronar y-t ype distal SCA an d PICA branch es,
cases w ith a large base overlapping uni- or bilaterally on the prox- w ith th e ext rem es being th e PICA–AICA disposit ion an d AICA–
im al posterior cerebral ar ter y (PCA). Th erefore, recan alizat ion PICA varian t . Th e AICA crosses th e cerebellop on t in e cistern an d
an d recurren ce after coiling occurs in up to 30% of cases.31 Th e com es close to CNs VII an d VIII. Th e AICA is divided in to a p re-
in ciden ce of recurren ce fur th er correlates w ith large an eurysm m eatal, m eat al, an d post m eatal segm en t . Th e in tern al auditor y
size,32 previous r upt ure,32 an d in com plete in it ial coil occlusion .33 ar ter y an d a variable n um ber of recurren t perforat ing bran ch es
A variet y of com plex en d ovascu lar st rategies in clu ding balloon origin ate from th e prem eat al segm en t , w h ereas th e subarcu ate
rem odeling an d sten t-assisted coiling h ave been suggested over ar ter y m ore com m on ly arises from a post m eatal por t ion .36 Ter-
th e years (Fig. 58.7). Th e post u lated advan t ages of th ese tech - m in al AICA bran ch es con t ribu te to t h e m en ingeal su p p ly along
n iques in clude a sign ifican tly low er recan alizat ion rate w ith n o th e in ferior pet rosal an d t ran sverse-sigm oid territor y.
st at ist ically sign ifican t ad dit ion al m orbidit y.34 Nu m erou s sten t Th e AICA an eu r ysm s m ake u p 1 to 2% of in t racran ial an eu -
arrangem en t s (e.g., Y-sten t ing) h ave been advocated to in crease r ysm s.37 Proxim al AICA an eu r ysm s con sist of sidew all-t ype con -
t h e d en sit y of t h e coil m ass w h ile p rotect in g PCA flow .34,35 To gen it al lesion s, or altern at ively relate to basilar ect asia in corpo-
lim it t h e r isk of sten t kin king, op en -cell d esign d evices (e.g., rat ing the AICA origin . Su rgical m an agem en t of proxim al AICA
Neu roform EZ, St r yker Neu rovascu lar, Frem on t , CA) are gen er- an eur ysm s faces th e ch allenges of a com plex an atom y th at com -
ally preferred for closed-angle disposit ion s. In recen t years, our prises m u lt iple n eu rovascu lar st r u ct u res in a deep an d n arrow
group h as sh ifted tow ard th e u se of low -porosit y sten t s in th e su rgical field. Also, th e frequ en t absen ce of an easily defin able
t reat m en t of BA t ip an eu r ysm s. Th e com p arat ively h igh er m et al an eur ysm n eck im pedes direct clip recon st r uct ion in a sign ifi-
coverage fract ion redu ces th e h em odyn am ic pressu re on th e coil can t su bset of lesion s (e.g., n on –saccu lar-t yp e an eu r ysm s). From
m ass by redirect ing flow m ore efficien tly aw ay from th e an eu- an en dovascular poin t of view, sten t-assisted coiling is a com pel-
rysm al neck, thus theoretically lim iting coil com paction over tim e. ling st rategy to deal w ith th e n on r u pt u red saccu lar su bpop u la-
Moreover, th e low -p orosit y design ap p ears, in ou r exp erien ce, t ion . En dolu m in al recon st ru ct ion w ith low -p orosit y devices h as
par t icu larly valu able in p reven t ing th e coil loop from h ern iat ing proven effect ive in th e fu siform varian t ,37 alth ough con cern s
th rough th e st r u t s. W h en u sing low -porosit y sten t devices in th e n eed to be raised w h en residual AICA flow (an terograde or ret ro-
up per BA, w e carefu lly t u n e th e m et al coverage fract ion to lim it grade) p reven ts th e an eur ysm from th rom bosing. Addit ion ally,
th e risk of p oten t ially devastat ing brain stem perforator st roke. m ultiple device coverage in th e basilar arter y requires caut ion ,

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684 V Cerebral and Spinal Aneurysms

a d

b c e

Fig. 58.7a–e Reconstructive approach for large basilar artery (BA) tip an- dense coil packing. (d) Follow-up angiography shows complete obliteration
eurysm . (a) Angiography shows a broad aneurysm base including the right and preservation of unimpaired parent artery flow. (e) Three-dim ensional
P1. (b,c) A high-porosit y stent (Neuroform EZ, Stryker Neurovascular, Fre- reconstruction dem onstrates the final coil m ass.
m ont, CA) is deployed across the aneurysm neck allowing for subsequent

as it can cause devastat ing perforator st rokes.27 Distal AICA an - to th e su perior an d m iddle cerebellar pedun cles, as w ell as to th e
eu r ysm s are, in large par t , of th e dissect ing t ype. Th ey m ay be tectal collicu li.36
ch allen gin g to cat h eter ize d u e to t h e acu te an gle bet w een t h e Th e SCA an eu r ysm s m ake u p few er th an 2%of in t racran ial an -
AICA an d t h e basilar ar ter y. Th e u se of sm all m icrocat h eters eurysm s, but their discovery is associated w ith m ultiple aneurysm s
telescoped over a soft m icroguidew ire, in com bin at ion w ith an in up to 42% of cases.40 Literat u re on th e en dovascu lar m an age-
approach from th e opposite VA, m ay ease access in select cases. m ent of SCA aneurysm s is incorporated in reports on the treatm ent
En dovascu lar p aren t ar ter y occlu sion is th e p referred ap p roach of BA t ip an eur ysm s. Narrow -n eck proxim al SCA an eur ysm s are
for r upt ured dist al AICA an eur ysm s (Fig. 58.8). Neu rologic com - generally suitable for direct em bolization w ith detachable coils.41
plicat ion s largely resu lt from in adver ten t occlu sion of brain stem Com plex configuration aneurysm s t ypically require either balloon-
perforators an d eloqu en t bran ch es (e.g., in tern al au ditor y ar ter y or sten t -rem od eling st rategies. W it h in creasin g frequ en cy in
arising generally from the prem eatal segm ent).38 Post m eatal AICA recen t years, large or com p lex p roxim al SCA an eu r ysm s are ap -
sacrifice is gen erally w ell tolerated, given th e com p eten ce of th e proached w ith endolum inal reconstruction techniques (Fig. 58.9).
collateral n et w ork, in clu ding th e PICA an d th e SCA.39 In our experien ce, th e challenge is to lim it the m etal coverage over
th e h igh ly eloqu en t basilar ar ter y p erforators, w h ile m ain t ain ing
sufficient coverage for aneurysm throm bo-occlusion and ultim ately
an eur ysm cure on ce en doth elial overgrow th h as com pleted. En -
■ Superior Cerebellar Artery Aneurysms dovascu lar p aren t ar ter y occlu sion app ears safe an d effect ive for
distal SCA aneurysm s.41,42 An ischem ic sequela of deconstruction
Sim ilar to th e AICA, th e SCA is an en larged brain stem p erforator
is t ypically preven ted by a rich n et w ork of collaterals (e.g., dist al
t h at acqu ires in d evelop m en t a var iable fract ion of t h e cerebel-
AICA bran ch es an d long circu m flex PCA bran ch es).
lu m ’s h em odyn am ic n eed s. Th e SCA is su bd ivid ed in to t h e an -
ter ior p on tom esen cep h alic segm en t below CN III; t h e lateral
p on tom esen ceph alic segm en t below CN IV an d above CN V; th e
cerebellom esen ceph alic segm en t bet w een th e cerebellu m an d
th e u p per brain stem ; an d th e cor t ical segm en t s th at in clu de ver-
■ Posterior Cerebral Artery Aneurysms
m ian , h em isph eric, an d m argin al arteries. A variable set of m in - Plexifor m an astom oses bet w een t h e em br yon ic cer vical in ter-
u te p erforators arises from th e proxim al SCA, providing su pply segm en t al ar ter ies con st it u te t h e p recu rsors of t h e p oster ior

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58 Endovascular Treatment of Vertebrobasilar Circulation Aneurysms 685

a b

c d e

Fig. 58.8a–e Deconstructive approach for a ruptured distal anterior infe- t ypical blood clot distribution in the cerebellopontine angle. The coil m ass
rior cerebellar artery (AICA) aneurysm. (a) Cerebral angiogram shows a distal is seen on (d) nonsubtraction angiography and (e) noncontrast CT (bone
AICA aneurysm (circle). (b) Sparing of AICA branches during parent artery window).
coil obliteration (circle). (c) Noncontrast computed tom ography (CT) shows

a c e g

b d f h

Fig. 58.9a–h Reconstructive approach for large superior cerebellar artery large aneurysm neck, (e,f) resulting in significant intra-aneurysm al con-
(SCA) aneurysm . (a,b) Angiography illustrates the SCA origin in relation to trast stasis. (g,h) On follow-up angiography, the aneurysm progressively
the aneurysm neck. (c,d) A low-porosit y stent device is deployed across the regresses while the SCA rem ains patent.

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686 V Cerebral and Spinal Aneurysms

circulat ion . Blood supply is in it ially provided by a series of tem - t rapp ing h ave been described to p erm an en tly exclu de fu siform
porar y con n ect ion s (e.g., prim it ive t rigem in al, ot ic, hyp oglossal, PCA an eur ysm s from th e circu lat ion . Th ese approach es rely on
an d p roat lan t al ar ter ies) bet w een t h e p r im it ive carot id an d th e h em odyn am ic redu n dan cy of eloqu en t areas via a n et w ork
t h ese longit u d in al ch an n els. Th e p r im ord ial h em odyn am ic in - of leptom en ingeal collaterals an d provide a h igh level of perm a-
terd ep en d en ce bet w een t h e an ter ior an d p oster ior circu lat ion n en t p rotect ion from recu r ren ce.48 Th e ch allen ge ar ises above
is grad u ally su bst it u ted by th e d evelop in g p r im it ive p oster ior all in th ose cases w h ere collaterals are sparse or proven in ade-
com m u n icat ing ar teries (PCoA). W h en blood su p ply to th e ver te- qu ate (e.g., by balloon test occlu sion 44 ). Proxim al PCA segm en t s
brobasilar system from below becom es m at ure, th e PCoAs eith er are also less suitable for decon st r uctive m eth ods, as eloquen t
sign ifican tly decrease in size, or rem ain th e dom in an t sou rce of bran ch es alm ost invariably origin ate from , or are in im m ediate
blood supply to th e PCA in form of a fetal varian t . Th e PCA is proxim it y to, th e ect at ic p or t ion . Even th ough a variet y of ad-
su bdivided in to fou r dist in ct segm en ts.43 P1 d efin es t h e m ost jun ct revascularizat ion procedures h ave been suggested to over-
proxim al sect ion located in th e p rep on t in e cistern bet w een th e com e th e risk of isch em ia after vessel sacrifice, th ey all h arbor a
BA t ip an d th e PCoA in tersect ion . P1 p erforators in clu de th e p os- sizable periprocedural m orbidit y.49 Alternatively, endolum inal
terior thalam operforating arteries, short circum flex arteries, an d reconstruction (stent-w ith in -stent technique) w ith high -porosit y
long circu m flex ar teries. P2a dem arcates th e su bsegm en t sit u - devices en ables rein forcing th e diseased ar terial w all from th e
ated in th e cru ral cistern . P2a perforators prim arily con sist of a en d olu m in al side. Th e risk of recan alizat ion over t im e in relat ion
variable set of direct pedu n cular perforat ing ar teries. Bran ch es w ith th e lim ited poten t ial for en doth elial overgrow th rem ain s to
arising from th e P2a in clu de th e m edial posterior ch oroidal ar- be determ in ed, especially as early progression an d reru pt u re h as
ter y, h ipp ocam pal ar ter y, an d an terior tem poral ar ter y. P2b de- been repor ted.25,47 Fin ally, en dolum in al recon st ruct ion w ith
fin es th e subsegm en t foun d in th e am bien t cistern . P2p bran ch es low - p orosit y sten t devices h as an ecd otally been described in th e
com prise th e lateral p osterior ch oroidal ar ter y an d th e p osterior proxim al PCA territor y.27,50 Alth ough th ere h as been som e con -
tem p oral ar ter y. P3 delin eates th e sh or t PCA sect ion w ith in th e cern w ith h igh -m et al coverage of long perforators,50 such as th e
qu adrigem in al cistern . P4 covers th e dist al PCA bran ch es beyon d an terior ch oroidal ar ter y,51 recen t literat u re,52 as w ell as ou r ow n
th e qu adrigem in al cistern (e.g., calcarin e, parieto-occipit al, p os- exp erien ce in dicate t h at proxim al PCA p erforators can safely be
terior pericallosal fissu re). P3/P4 bran ch es in clu de th e calcarin e, covered by low -porosit y sten t devices (Fig. 58.10).
parieto-occipit al, an d splen ial ar ter y.
Th e PCA an eu r ysm s represen t 1%of discovered cerebral an eu -
r ysm s.44 For saccu lar PCA an eur ysm , su rgical tech n iques in clude
m icrosu rgical clip recon st ru ct ion via a variet y of ap p roach es
(e.g., pterion al, subtem poral,10 su p racerebellar t ran sten torial,
■ Conclusion
t ran s ch oroidal fissu re, or selective am ygdaloh ipp ocam p ectom y En dovascu lar th erapies p rovide a w ide variet y of tech n iqu es for
approach ). Microsurgical w rapping h as also been repor ted, but dealing w ith com p lex vascu lar lesion s of th e p osterior circu la-
th is m eth od h as n ever been sh ow n to im p act n at u ral h istor y by t ion . Th ese tech n iqu es h ave evolved con siderably from p u rely
p reven t ing an eu r ysm grow t h or h em or rh age.45 En d ovascu lar decon st ru ct ive m eth od s to cu rren t coil/sten t con st r u ct s an d th e
alter n at ives in clu d e d irect coil em bolizat ion ,46 w it h or w it h ou t u se of flow diverters. Th ese m eth ods are n ow w idely u sed for an
balloon rem odeling or sten t assist an ce.47 Alt h ough t h ese tech - ever-in creasing subset of rupt ured an d un r upt ured VB circula-
n iqu es lead to grat ifying resu lt s in saccular-t ype PCA an eur ysm s, t ion an eu r ysm s. Based on th e rapid advan ces m ade over th e last
fu siform -t ype an eu r ysm s are less su it able d u e to th e absen ce of 20 years in en dovascular th erapeut ic opt ion s, it is likely th at w e
a defin able n eck. A variet y of decon st ru ct ive m eth ods in cluding w ill develop addit ion al devices an d even m ore refin ed st rategies
su rgical an d en dovascu lar p roxim al p aren t ar ter y ligat ion an d w ith w h ich to bet ter h elp our pat ien ts in th e fu t ure.

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58 Endovascular Treatment of Vertebrobasilar Circulation Aneurysms 687

a c e g

b d f h

Fig. 58.10a–h Reconstructive approach for proximal posterior cerebral resonance im aging (MRI). (e,f) Low-porosit y stent device deploym ent
artery (PCA) aneurysm . (a,b) Angiography shows a giant proxim al P2A-P2P with overlap across the aneurysm neck. (g,h) Reconstructed PCA on early
aneurysm . (c,d) Mass effect is dem onstrated on T1-weighted m agnetic follow-up angiography.

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20. Flem m ing KD, W iebers DO, Brow n RD Jr, et al. Th e n at u ral h istor y of 37. Szikora I, Beren tei Z, Kulcsar Z, et al. Treat m en t of in t racran ial an eu r ysm s
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21. Passero SG, Rossi S. Nat ural h istor y of ver tebrobasilar dolichoect asia. 31:1139–1147
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22. Mangru m W I, Huston J III, Lin k MJ, et al. En larging ver tebrobasilar n on - vascular m anagem en t of dist al an terior in ferior cerebellar ar ter y an eu-
saccular in t racran ial an eu r ysm s: frequen cy, predictors, an d clinical out- r ysm s: Report of t w o cases and review of th e literat ure. Surg Neurol In t
com e of grow th . J Neurosurg 2005;102:72–79 2011;2:95
23. An son JA, Law ton MT, Spet zler RF. Ch aracterist ics an d surgical t reat m en t 39. Gon zalez LF, Alexan d er MJ, McDougall CG, Sp et zler RF. An teroin fer ior
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24. Coer t BA, Ch ang SD, Do HM, Marks MP, Stein berg GK. Surgical an d en do- 40. Peluso JP, van Rooij W J, Slu zew ski M, Beute GN. Superior cerebellar ar ter y
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an eur ysm s. J Neu rosurg 2007;106:855–865 dovascu lar t reat m en t . Neu roradiology 2007;49:747–751
25. Siddiqui AH, Abla AA, Kan P, et al. Pan acea or problem : flow diver ters in 41. Pierot L, Boulin A, Cast aings L, Rey A, Moret J. Select ive occlusion of basilar
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lizat ion device in t reat m en t of posterior circulat ion an eur ysm s. AJNR Am th e p osterior cerebral ar ter y: classificat ion an d en d ovascu lar t reat m en t .
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for com plex basilar and ver tebrobasilar jun ct ion an eur ysm s. Neurosu r- intracranial rupt ured an eur ysm s. Acta Neurochir (Wien ) 1990;103:27–29
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29. Sh apiro M, Becske T, Riin a HA, Raz E, Zum ofen D, Nelson PK. Non -saccular eur ysm s of posterior cerebral ar ter y: clin ical present at ion , angiograph ic
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316 coil-t reated basilar arter y bifurcat ion an eu r ysm s. J Neurosurg 2005; 48. Liu L, He H, Jiang C, Lv X, Li Y. Deliberate paren t ar ter y occlu sion for n on -
103:990–999 saccu lar posterior cerebral ar ter y aneur ysm s. In ter v Neu roradiol 2011;
32. Raym on d J, Guilber t F, Weill A, et al. Long-term angiograph ic recurren ces 17:159–168
after select ive en dovascu lar t reat m en t of an eu r ysm s w ith d et ach able 49. Chang SW, Abla AA, Kakarla UK, et al. Treatm ent of distal posterior cerebral
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33. Slu zew ski M, van Rooij W J, Slob MJ, Bescós JO, Slum p CH, Wijnalda D. Re- cerebral ar ter y bypass. Neurosurger y 2010;67:16–25, discussion 25–26
lat ion bet w een an eur ysm volum e, packing, an d com pact ion in 145 cere- 50. Nelson PK, Lylyk P, Szikora I, Wet zel SG, Wan ke I, Fiorella D. The pipelin e
bral an eur ysm s t reated w ith coils. Radiology 2004;231:653–658 em bolizat ion device for th e in t racran ial t reat m en t of an eur ysm s t rial.
34. Ch alouh i N, Jabbour P, Gon zalez LF, et al. Safet y an d efficacy of en dovas- AJNR Am J Neu roradiol 2011;32:34–40
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sten t assist an ce: a review of 235 cases. Neu rosu rger y 2012;71:785–794 pipelin e flow -divert ing sten t for an u nrupt ured A1 an eu r ysm . AJNR Am J
35. Fargen KM, Mocco J, Neal D, et al. A m u lt icen ter st udy of sten t-assisted Neuroradiol 2010;31:E43–E44
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73:466–472 com e of pipeline em bolization device—a prospective st udy in 143 patients
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lococh lear n er ve com plex. Neurosurger y 1980;6:483–507

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59 Infectious Intracranial Aneurysms
Jonathan J. Russin, W illiam J. Mack , and Steven L. Giannot ta

■ Relevant Anatomy M4: Surface of the Sylvian fissure over the cerebrum
Cerebrovascu lar su rgeon s’ fam iliarit y w ith th e circle of Willis is Cortical areas
w ell recogn ized. Th e t reat m en t of in fect ious in t racran ial an eu- • Orbitofrontal
r ysm s (IIAs), h ow ever, frequen tly requires surgeon s to operate • Prefrontal
outside of th e basal cistern s. A com preh en sive kn ow ledge of th e • Precentral
dist al bran ch es of both th e an terior an d posterior circu lat ion is • Central
crit ical for successfu l su rgical m an agem en t of IIAs. Given th at • Anterior parietal
h em atogen ous spread is th e m ost com m on et iology of IIAs, it fol- • Posterior parietal
low s th at territories w ith th e greatest flow are at th e h igh est risk. • Angular
In tot al, 56 to 79%of IIAs are located in th e m iddle cerebral ar ter y • Temporo-occipital
(MCA) ter r itor y, t w o-t h ird s of w h ich are in t h e d ist al vascu la- • Posterior temporal
t u re.1–3 Th e follow ing descript ion s an d n om en clat ure of th e MCA • Middle temporal
segm en t s are referen ced th rough ou t th is ch apter. • Anterior temporal
Adapted from Gibo H, Car ver CC, Rh oton AL, Len key C, Mitch ell RJ. Micro-
surgical an atom y of th e m iddle cerebral ar ter y. J Neurosurg 1981;54:
Middle Cerebral Artery 151–169.
Th e larger of th e term in al bran ch es of th e in tern al carot id ar ter y
(ICA), th e MCA ser ves th e greatest territor y of th e cerebral ves-
sels. It origin ates at th e sam e an atom ic locat ion as th e A1, below
th e an terior p erforated su bst an ce an d lateral to th e opt ic ch iasm .
Th e MCA th en cou rses laterally, p arallel to th e sp h en oid ridge, ■ Pathophysiology and Natural History
an d t urn s 90 degrees to exit th e sph en oidal com par t m en t . After
cou rsing over th e lim en in su la in to th e op ercu loin su lar com p ar t- of Disease
m en t , th e m ain bran ch es pass along th e in su la. Th e vessel m ain - In fect ious in t racran ial an eu r ysm s are m ost frequen tly th e result
tain s th is course un t il it t raverses th e fron topariet al an d tem po- of sept ic em boli in t h e set t ing of in fect iou s en d ocard it is (IE).5
ral op erculu m to reach th e surface of th e sylvian fissure. After How ever, ext ravascu lar sou rces of IIAs are w ell recogn ized .6–9
em erging from th e sylvian fissu re, cor t ical bran ch es t raverse th e Th e com m on alit y bet w een th e t w o et iologies is th e in t rodu ct ion
su rface of th e cerebral h em isph ere.4 MCA bran ch ing segm en ts of bacteria, fu ngu s, virus, or p arasite in to th e adven t it ia of in t ra-
are com plex an d custom arily referred to by th e territor y of cor- cran ial ar teries. On ce in th e adven t it ia, path ogen s in it iate an in -
tex th at th ey su pp ly (see text box). flam m ator y react ion th at perm eates th e in n er layers of th e arte-
rial w all, resu lt ing in focal w eaken ing.5 Hydrost at ic forces again st
a w eaken ed ar terial w all cause expan sion an d an eur ysm form a-
MCA Segments t ion . Th e in flam m ator y inju r y to th e vessel w all likely explain s
M1: ICA bifurcation to genu of the limen insula w hy m ost IIAs h ave circum feren t ial involvem en t of th e vessel, as
Branches opposed to m ore focal involvem en t seen in saccular an eur ysm s.
• Lenticulostriates (average num ber, 10) In it ial invest igat ion s repor ted th at th e path ogen ic in filt rat ion of
• Temporopolar th e vasa vasorum en abled bacteria to escape in to th e adven t it ial
M2: Genu of the limen insula to the circular sulcus layer of t h e vessel w all.10 How ever, t h e d ist al bran ch es of t h e
Branches cerebral circu lat ion rarely con t ain a vasa vasor u m . Su bsequ en t
• Insular branches ar t icles h ave post ulated that path ogen s could escape from sept ic
M3: Circular sulcus to the surface of the Sylvian fissure em boli an d en ter in to th e Virch ow -Robin space, th us in filt rat ing
Branches th e vessel adven t it ia.11 Ext ravascular path ogen s w ould h ave ac-
• Opercular branches cess to th e vessel advent it ia in sim ilar locat ion s. Com m on ch ar-
acterist ics of IIAs are presen ted in th e n ext text box.

689

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690 V Cerebral and Spinal Aneurysms

Characteristics of Infectious Table 59.1 Pathogens Associated w ith Infectious Intracranial


Intracranial Aneurysms Aneurysms

Gram -positive bacteria Viridans streptococci


Clinical
Staph. aureus
• Left-sided cardiac valvular disease
Strep. pneumonia
• Immunocompromised status
b-hemolytic Strep.
• Recent infection
Nocardia asteroids
• Younger age Peptostreptococcus
• Febrile presentation Rothia dentocariosa
Radiographic Gram -negative bacteria Pseudomonas aeruginosa
• Associated with distal branches Neisseria meningitides
• Multiple Salmonella
• Fusiform Klebsiella pneumonia
• Rapidly changing on repeat imaging Serratia marcescens
Laboratory Cardiobacterium hominis
• Elevated inflam matory markers Mycobacterium Tuberculosis
• Positive blood cultures Viruses VZV
HIV-1
Fungi Aspergillus
Candida albicans
Path ologic ch anges in IIAs h ave been invest igated in an im al Pseudallescheria boydii
m odels. Infiltration of polym orphonuclear leukocytes into the ad- Coccidioides immitis
ven t it ia follow ing sept ic em boli leads to p rogressive dest ruct ion Parasites Acanthamoeba
of t h e ar ter ial w all from t h e ou t sid e in . Ult im ately, d est r u ct ion Naegleria fowleri
of th e m uscularis m edia an d in tern al elast ic lam in a results in Toxoplasma gondii
w eaken ing of th e arterial w all (Fig. 59.1). An eu r ysm al dilat ion Abbreviations: Staph., Staphylococcus; Strep., Streptococcus; VZV, varicella zoster
can occu r as qu ickly as 24 h ou rs after sept ic em boli. Th e involved virus; HIV-1, hum an im munodeficiency virus 1.
arteries are com m on ly occlu ded dist ally, an d an eur ysm al dila- Source: Data adapted from Kannoth S, Thom as SV. Intracranial microbial
t ion is t ypically n oted at th e p roxim al en d of th e occlu sion .11 As aneurysm (infectious aneurysm): current options for diagnosis and management.
Neurocrit Care 2009;11:120–129, and Frazee JG, Cahan LD, Winter J. Bacterial
these arteries are distal in locat ion, and com m only occluded prior
intracranial aneurysm s. J Neurosurg 1980;53:633–641.
to t reat m en t , pat ien t s frequen tly do n ot sustain n ew n eurologic
deficit s follow ing en dovascu lar vessel sacrifice or su rgical t rap -
ping an d excision .10 tou s en cep h alit is, an d viral vascu lop at hy h ave been repor ted to
A variet y of path ogen s h ave been associated w ith IIAs. Th e cau se IIAs (Table 59.1).6–9,11
m ost com m on ly reported are bacterial in fect ion s w ith St repto- Th e n at u ral h istor y of IIAs is n ot w ell docu m en ted in th e lit-
coccu s v iridans an d Staphylococcus aureus. Th ese p ath ogen s are erat u re. Th e m ajorit y of pu blish ed dat a are based on sm all case
com m on ly associated w it h IE. Ext ravascu lar sou rces of in fec- series from single in st it u t ion s w ith lim ited follow -u p . How ever,
t ion , in clu ding m en ingit is, sin u s th rom bop h lebit is, gran u lom a- a few w ell-con st ructed review s provide th e best in form at ion to
date on th e n at u ral h istor y of t h ese rare an eu r ysm s. Ap proxi-
m ately 0.7 to 6.5% of all in t racran ial an eur ysm s are th e result of
an in fect ious et iology.5 Th e m edian age at presen tat ion of pa-
t ien ts w ith IIAs is 35.1 years, an d 65%of p at ien t s su ffer from IE.10
Am ong p at ien t s w ith IE, th e est im ated p revalen ce of IIAs is 0.8 to
12%. Th e ru pt ure rate of IIAs in IE pat ien ts h as been est im ated at
10%.12 Overall m ortalit y rates am ong patients harboring IIAs have
been repor ted at 10 to 18.7% in recen t case series, w ith som e-
w h at high er rates p resen ted in older repor t s (15–50%).12–14

■ Clinical Presentation
Th e clin ical p resen t at ion of p at ien t s w ith IIAs varies dep en ding
on et iology. Hem atogen ou s sp read from IE is presen t in 65% of
IIA cases. In t raven ous drug abuse (6.3%), bacterial m en ingit is
(5.2%), poor den tal hygien e (4.2%), an d cavern ous sin us th rom -
bosis (2.8%) are other com m on causes. Aneurysm al rupture is the
Fig. 59.1 Hem atoxylin and eosin stain of a cross-sectional slide from an presen tat ion in 72%of p at ien t s w ith IIAs. Oth er com m on presen -
excised infectious intracranial aneurysm (IIA) at low power. An intense in- tat ion s in clude fever, h eadach e, focal deficit , em esis, seizures,
flam m atory reaction is apparent in the vessel wall. cranial nerve palsies, and behavioral changes (Table 59.2).10 Many

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59 Infectious Intracranial Aneurysms 691

Table 59.2 Clinical Presentations of Infectious Intracranial paid to cutaneous m anifestations of IE, including Janew ay lesions,
Aneurysms Osler’s n odes, an d su bungual h em orrh ages. Fun du scopic exam i-
n at ion m ay reveal Roth spot s.
Clinical Sign/Symptom %*

Aneurysmal rupture 72
Headache 30 Laboratory
Fever 28 A com p lete blood cou n t an d basic m et abolic p an el sh ou ld be
Hem iparesis 15 obt ain ed if IIA is su sp ected . An elevated w h ite blood cell cou n t
Emesis 9
or th rom bocytosis can in dicate an in fect ious process. Elevated
Seizures 7
er yth rocyte sedim en t at ion rate or C-react ive p rotein levels also
Malaise 7
suggest in fect ion . Im m u n e com p lex deposit ion an d vascu lit is
Loss of consciousness 7
secon dar y to IE can m an ifest in glom er u lon ep h rit is an d resu l-
Aphasia 3
tan t in creases in serum creat in in e. Sept ic em boli to th e kidn eys
Ocular palsy 2
can p rodu ce h em at u ria, bu t rarely cau se ren al failu re.18
*Patients frequently present with m ore than one sign/symptom . Blood cu lt ures sh ould be obtain ed w h en an IIA is suspected.
Source: Data adapted from Ducruet AF, Hickman ZL, Zacharia BE, Narula R,
How ever, a recen t review suggested th at cu lt u res are p osit ive in
Grobelny BT, Gorski J, Connolly ES. Intracranial infections aneurysm s: a compre-
hensive review. Neurosurg Rev 2010;33:37–46. on ly 35.6% of affected p at ien t s.10 If an ext ravascu lar IIA sou rce
is su sp ected, a lu m bar p u n ct u re m ay be p erform ed to obt ain a
cerebrospin al fluid cu lt ure.
of th ese sym ptom s are at t ribut able to in t racran ial h em orrh age.
How ever, exp an sile IIAs h ave also been rep or ted to cau se sym p -
tom s secon dar y to m ass effect .15,16 In ad dit ion , sept ic em boli can
Diagnostic Imaging
prod u ce isch em ic sym ptom s th at resu lt in discover y of an in ci- Pat ien ts at risk for IIA, presen t ing w ith sp on tan eou s SAH, require
den t al IIA. Pat ien ts m ay also p resen t w ith sign s an d sym ptom s detailed evalu at ion of th e cerebral vascu lat u re. Com pu ted to-
related to th e u n derlying ext ravascular cau se. m ography angiography (CTA) h as been sh ow n to h ave excellen t
sen sit ivit y (99%) an d a 92.5% n egat ive predict ive valu e in SAH
p at ien t s.19 Pat ien t s h arbor ing IIA m ay be at greater r isk for a
false-n egat ive CTA given t h e frequ en t d ist al locat ion s of t h ese
■ Perioperative Evaluation an eu r ysm s. Det ailed p ost p rocessing of CTA im ages, w it h field s
History of view in clu ding th e dist al vascu lat u re, is crit ical for obt ain ing
h igh sen sitivit y. In a p at ien t at risk for a rupt u red IIA w h o pre-
Th e diagn osis of IIA sh ou ld be con sidered in p at ien t s w h o pres- sents w ith SAH, a negative CTA should be follow ed by digital sub-
en t w ith su barach n oid h em orrh age (SAH) an d con cu rren t fevers, t ract ion angiograp hy (DSA). CTA/DSA fin dings suggest ive of IIA
h istor y of cardiac valve disease or IE, recen t in fect ion s or n eu ro- in clude p erip h eral an eur ysm locat ion , fu siform an eu r ysm sh ap e,
su rgical p rocedu res, im m u n osu p p ression , h istor y of in t raven ou s an d th e presen ce of m ult iple an eur ysm s. In th e case of a n egat ive
drug u se, or recen t lu m bar p u n ct u re or sp in al/ep idu ral an esth e- DSA, m agnetic resonance im aging (MRI) of the brain m ay be w ar-
sia. Neu rologic com plicat ion s occu r in 10 to 40% of IE cases.17 ran ted to search for eviden ce of a th rom bosed an eur ysm .
Docu m en t at ion of a det ailed h istor y an d evalu at ion of t ran sien t Infect ious endocardit is pat ients presen ting w ithout neurologic
n eu rologic sym ptom s is crit ical in th is pat ien t popu lat ion . In on e sym ptom s are u n likely to ben efit from cath eter cerebral angiog-
cases series, eigh t of 13 (61.5%) p at ien t s exh ibited n eu rologic raphy.12 A risk-ben efit an alysis h as n ot been publish ed for CTA,
sym ptom s p rior to an eu r ysm al ru pt u re or d iagn osis of IIA.3 An - but given th e curren t recom m en dat ion s for DSA, it is likely n ot
teceden t n eu rologic m an ifestat ion s in clu ded h em iparesis, aph a- in dicated in th is populat ion . A com p uted tom ography (CT) scan
sia, facial w eakn ess, an d seizu re. Assessm en t of con st it u t ion al of th e h ead sh ould be perform ed in IE pat ien t s w h o presen t w ith
sym ptom s, in clu d ing an orexia, w eigh t loss, fat igu e, ch ills, an d n eu rologic sym ptom s. No diagn ost ic im aging guidelin es or rec-
n igh t sw eats, is also essen t ial. Congest ive h ear t failure develops om m en dat ion s exist for fur th er test ing in th e set t ing of a n ega-
in 30 to 40% of p at ien ts w ith IE.18 t ive h ead CT scan . Th e au th ors’ cu rren t p ract ice is to obt ain a CTA
Com m on ext ravascu lar cau ses of IIA in clu de m en ingit is, cav- at th e t im e of th e h ead CT scan in th ose p at ien ts w ith n eu rologic
ernous sinus throm bophlebitis, and orbitofacial infections. Sym p - sym ptom s. Care is taken to recon st ru ct th e distal cerebral vascu -
tom s su ch as p h otop h obia, h eadach e, visu al com plain t s, facial lat u re. In th e case of a n egat ive h ead CT scan an d CTA, an MRI
sw elling, local red n ess, otorrh ea, or n eck st iffn ess are suggest ive w ith diffusion-w eighted and gradient-echo im ages is obtained to
of poten t ial IIA sources. A careful h istor y of m edicat ion can iden - search for eviden ce of em bolic in farcts or bloom ing ar t ifact sug-
t ify poten t ial im m u n osu pp ressan t agen t s. gest ive of a th rom bosed an eu r ysm .

Physical Examination Treatment


Physical exam in at ion fin d ings t h at raise con cer n for r u pt u red Due to th e relat ively low in ciden ce rates of IIA, th ere are n o ran -
IIA in th e set t ing of SAH in clude fever an d sign s of IE. Sym ptom s dom ized con t rolled t rials in th e literat u re evalu at ing t reat m en t
con sisten t w ith congest ive h ear t failu re, su ch as h ear t m u rm u r, opt ion s. Th e m ajorit y of publicat ion s are in dividu al case series
jugu lar ven ou s d isten t ion , lu ng crackles, clu bbing, an d p it t ing or literat ure review s. Th erefore, t reat m en t recom m en dat ion s are
low er ext rem it y edem a, are also suggest ive. At ten t ion sh ould be based on class III dat a.

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692 V Cerebral and Spinal Aneurysms

Table 59.3 Timing of Cardiac Surgery for Infectious Endocarditis w ith Neurologic
Complications

Clinical Presentation Timing of Surgical Intervention Class of Evidence

CVA with GCS ≥ 9 and no ICH Immediate IIa level B


CVA with GCS < 9 or ICH Delay* IIa level B
TIA or silent em boli Immediate I level B
ICH Delay at least 1 month I level C
*Surgery should proceed if GCS improves with no ICH or after at least 1 m onth if ICH is present.
Abbreviations: CVA, cerebrovascular accident; GCS, Glasgow Com a Scale; ICH, intracranial hemorrhage; TIA,
transient ischemic at tack.
Source: Data adapted from Rossi M, Gallo A, De Silva RJ, Sayeed R. What is the optimal tim ing for surgery in infective
endocarditis with cerebrovascular complications? Interact Cardiovasc Thorac Surg 2012;14:72–80.

Gen eral t reat m en t con siderat ion s are con t ingen t upon th e in fect iou s an eur ysm s, m aking th e MCA territor y th e m ost com -
et iology of t h e IIA. Pat ien t s w it h IE frequ en t ly requ ire p eriop - m on site. In m ost cases a fron totem poroparietal cran iotom y pro-
erat ive and postoperat ive an t icoagu lat ion . Th e ch oice of a surgi- vid es ad equ ate access for su rgical in ter ven t ion . Fram eless ste-
cal versus en dovascu lar ap proach m ay dep en d on th e t reat m en t reotact ic n avigat ion can be valuable in localizing th e path ology
recom m en dat ion s of th e cardioth oracic su rger y team . A m ult i- an d lim it ing th e size of th e cran iotom y. Th e M1–M3 segm en ts
disciplin ar y ap p roach is n ecessar y for t h e su ccessfu l m an age- t ypically require a t ran ssylvian approach , w h ereas th e M4 seg-
m en t of th ese com plex pat ien ts. Recom m en dat ion s h ave been m en t is gen erally accessed at th e cerebral h em isph ere.
pu blish ed regarding th e opt im al t im ing for cardiac surger y after Dist al an ter ior cerebral ar ter y (ACA) an eu r ysm s frequ en t ly
n eu rologic com plicat ion s related to IE (Table 59.3).20 require an in terh em isph eric approach . An eu r ysm s of th e an te-
rior com m u n icat ing arter y (ACoA), A1, or th e proxim al A2 seg-
m en t s can gen erally be t reated w ith a pterion al cran iotom y via a
Unruptured
t ran ssylvian ap proach . Dist al A2 an eu r ysm s m ay requ ire a su p ra-
Sp ecific an t ibiot ic th erapy is in it iated follow ing th e diagn osis of orbit al cran iotom y w ith a subfron tal approach or an in terh em i-
IIA. As blood cult ures are positive in only approxim ately one-th ird sph eric approach , dep en ding on locat ion an d m orph ology.
of cases, em piric an t ibiot ics are recom m en ded after obtain ing An eur ysm s of th e P1 an d P2 segm en ts of th e posterior cere-
cult ures. Th e ch oice of an t ibiot ic is directed by th e presum ed bral ar ter y (PCA) an d s1 an d s2 segm en ts of th e superior cerebel-
sou rce of th e p ath ogen . In th e set t ing of IE, gu idelin es for em p iric lar arter y (SCA) can gen erally be accessed th rough th e sylvian
an t ibiot ic t h erapy are based on t h e m ater ial an d st r u ct u re of fissu re via an orbitozygom at ic cran iotom y. Th is can be m odified
t h e valve.21 Con su lt ing an in fect iou s disease sp ecialist is recom - in to a pretem p oral app roach by releasing th e tem poral pole. Pos-
m en ded w hen an IIA is diagn osed. terolateral retraction on the tem poral lobe then enhances visual-
Follow ing in st it u t ion of an t ibiot ic th erapy, IIAs sh ould be re- ization an d can be achieved w ith less retract ion and postoperat ive
im aged ever y 2 w eeks u n t il radiograp h ic resolu t ion . Th is para- edem a w h en com p ared w ith a su btem poral app roach .23 More
digm p rovides frequ en t sur veillan ce to iden t ify n ew an eur ysm s. periph erally located an eu r ysm s of th e P3 an d P4 segm en ts can
Th e u se of CTA as a su r veillan ce st u dy h as been sh ow n to be be approach ed via an occipit al in terh em isph eric approach. An -
reliable in sm all case series.22 On serial im aging, IIA sh ow sp on - eu r ysm s arising from th e s3 an d s4 segm en t s of th e SCA m ay be
taneous resolution in 30%of cases treated w ith antibiotics.2 If the approach ed from an occipit al t ran sten torial or an in fratentorial
IIA does n ot decrease in size or resolve on repeat im aging, th en supracerebellar app roach .24
su rgical or en dovascu lar in ter ven t ion sh ou ld be con sidered. Th e m ajorit y of dist al an terior in ferior cerebellar ar ter y (AICA)
an eur ysm s can be accessed th rough a ret rosigm oid or exten ded
ret rosigm oid app roach . An eu r ysm s arising from th e a1 or proxi-
Ruptured
m al a2 segm en ts m ay require im proved visualizat ion of th e an -
Th e diagn osis of a r u pt u red IIA requires st rong con siderat ion for terior brain stem , w h ich frequen tly m ean s u sing a t ran ssigm oid,
su rgical or en dovascu lar in ter ven t ion . Moribu n d p at ien t con di- presigm oid, or t ran slabyrin th in e approach .25
tion , cardiac failure, or an advanced directive m ay deter treat m ent. Proxim al p oster ior in fer ior cerebellar ar ter y (PICA) an eu -
However, given the relatively young age at presentat ion t ypical of r ysm s can be exposed via a far-lateral or ext rem e-lateral in ferior
th is pop u lat ion , an aggressive m an agem en t st rategy to exclu de transcon dylar-t ranst ubercular exposure (ELITE). More distal seg-
th e ru pt ured IIA from th e in t racran ial circulat ion is w arran ted. m en t s, such as th e distal p3 to p5, can u sually be accessed via a
suboccipit al cran iotom y.

■ Surgical and Endovascular Approaches Endovascular


En dovascu lar IIA app roach es avoid th e risks of perform ing op en
Surgical su rger y on an in fected or bacterem ic pat ien t an d do n ot requ ire
As the m ajorit y of IIAs result from hem atogen ous spread, cortical accessing a friable aneurysm through the cisternal or sulcal spaces.
territories w ith th e h igh est blood flow m ost frequen tly h arbor Furth er, en dovascular tech n iques en able th e t reat m en t of an eu-

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59 Infectious Intracranial Aneurysms 693

r ysm s at m ult iple an atom ic locat ion s in a single set t ing. Th ese len ce of sm all an eur ysm al size, sessile m orph ology, an d lesion al
procedu res m ay be perform ed u n der gen eral an esth esia or con - friabilit y often ren der vessel occlu sion th e p rim ar y opt ion . Pa-
sciou s sedat ion , d ep en d ing on op erator p referen ce an d clin ical t ien ts w ith distally located lesion s can frequ en tly tolerate vessel
circum stances. Antibiotics have generally been adm inistered prior sacrifice. Non eth eless, it is often h elp fu l to p erform fu n ct ion al
to th e procedure according to th e suspected path ogen an d in st i- assessm en t w ith sodium am ytal prior to vessel occlusion in elo-
t u t ion al protocols. qu en t cor t ical territories. Th is requ ires an aw ake p at ien t or elec-
Su p p or t for m icrocath eterizat ion is crit ical, as m ost IIAs are t rop hysiological m on itoring du ring th e crit ical por t ion s of th e
located in t h e d ist al cerebral vascu lat u re an d m ay requ ire n avi- procedu re. Vessels m ay be sacrificed w ith coils or liqu id em bolic
gat ion t h rough sm all, tor t u ou s ar ter ies. A gu id e cat h eter or agen t s, d epen ding on an atom ic con siderat ion s, vessel size, an d
sh u t tle sh eath is t ypically advan ced over a 0.035-in ch w ire in to operator preferen ce.
th e proxim al carot id or ver tebral ar ter y. Th ese deliver y system s In proper circum st an ces, IIAs are am en able to coil em boliza-
effect ively m ain t ain p osit ion an d can accom m odate m u lt ip le t ion an d paren t vessel preser vat ion . An eu r ysm al coil em boliza-
d evices if balloon rem odeling or dual cath eter tech n iques are re- t ion lessen s th e risk of n eu rologic deficits associated w ith paren t
quired for t reat m en t . In th e case of tor t u ou s vascu lar an atom y, vessel sacrifice. Lesion s w ith favorable an atom y m ay allow for
in term ediate dist al su p port cath eters can be effect ive. prim ar y or balloon -assisted coil em bolizat ion . As m ost su rgeon s
t r y to avoid sten t p lacem en t , balloon rem odeling is a tech n iqu e
frequently em ployed for aneur ysm s w ith less favorable neck anat-
om y an d does n ot require a perm an en t im plan t . As m en t ion ed
■ Surgical and Endovascular Technique above, the theoretical risk of placing platinum coils (foreign body)
in to a bacterem ic pat ien t is n ot recogn ized as a con t rain dicat ion
Con siderat ion s in th e m an agem en t of IIA differ from th ose of
to th is t reat m en t m odalit y.
oth er an eu r ysm s. Th e system ic bu rden of disease an d th e poten -
t ial n eed for p eriop erat ive an d postop erat ive an t icoagu lat ion (in
th e set t ing of IE) p resen t sp ecial ch allenges. En dovascu lar t reat-
m ent is generally preferred. Perform ance under m inim al sedation
or w ith cor t ical m on itoring en ables th e surgeon to test paren t
■ Illustrative Cases
vessel occlusion for poten t ial n eu rologic deficits prior to defin i- Case 1
t ive t reat m en t . Alth ough aw ake cran iotom y offers a sim ilar ad-
A 39-year-old m an w ith a h istor y of congen ital aor t ic sten osis
van t age, it presen ts a greater an esth esia ch allenge an d a greater
an d prior aor t ic valve (porcin e) an d proxim al aor ta replacem en t
r isk of an t icoagu lat ion p ostop erat ively.26 Con cer n s abou t h ard -
presented w ith fever, headache, interm it tent left-hand n um bn ess,
w are in fect ion in t h e set t in g of h em atogen ou s sp read h ave n ot
an d w ord fin ding difficult ies. Neurosu rger y w as con su lted, an d a
been su bst an t iated in th e literat ure.27
h ead CT an d CTA w ere perform ed (Fig. 59.2). A presum ed IIA
Su rgical in ter ven t ion is n ecessar y w h en en dovascu lar t reat-
w as iden t ified w ith ou t eviden ce of h em orrh age. Several hypo-
m en t is n ot possible or w h en vessel sacrifice is likely an d bypass
den sit ies w ere p resen t , con sisten t w ith em bolic in farcts. Em p iric
is plan n ed . A relat ively h igh frequ en cy of in t racerebral h em or-
rh age (ICH) can resu lt in elevated in t racran ial pressu re (ICP) or
n eurologic deficit , prom pt ing su rgical h em atom a evacuat ion in
m any p at ien t s.5 If feasible, op en su rgical t reat m en t of t h e IIA
sh ou ld be u n dert aken w h en cran iotom y is p erform ed for ICH.

Surgical
Th e frequ en t circu m feren t ial involvem en t of th e vessel w all an d
th e diam eter of th e an eu r ysm relat ive to th e paren t vessel often
m akes direct surgical clipping, w ith paren t vessel recon st ru c-
t ion , im possible. Th erefore, it is im por t an t to be prep ared to sac-
rifice th e p aren t vessel along w ith t h e an eu r ysm . In t raoperat ive
m on itor in g w it h m otor an d sen sor y evoked p oten t ials can be
evalu ated w ith tem porar y paren t vessel occlusion . In addit ion ,
in docyan in e green angiography can be u sed in t raop erat ively to
assess vascu lar dist ribut ion an d collateral flow. W h en t reat ing
IIAs in eloquen t an atom ic locat ion s, it is im por tan t to con sider
bypass opt ion s if vessel sacrifice is w arran ted. Preoperat ive plan -
n ing m ust in clude don or vessel h ar vest , an d th e n ecessar y in -
st r u m en ts an d sut u res sh ou ld be readily available.

Endovascular
En dovascu lar p aren t vessel occlu sion an d en dosaccu lar coil em - Fig. 59.2 Axial im age from a computed tom ography angiography (CTA)
bolizat ion are both poten t ial th erapeut ic opt ion s for IIAs. Preva- showing contrast filling a left inferior frontal aneurysm (arrow).

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694 V Cerebral and Spinal Aneurysms

Fig . 59.3 Gross photograph of an excised infectious intracranial aneu- Fig. 59.4 High-powered hem atoxylin and eosin stain showing branching
rysm (IIA). septated hyphae on the background of infiltrating inflam m atory cells.

van com ycin , gen t am icin , an d ceft riaxon e th erapy w as in st it uted,


an d in t raven ou s h eparin in it iated w ith th e an t icipat ion of urgen t
cardiac surger y. How ever, th e day after star t ing h ep arin th erapy,
th e p at ien t developed severe h eadach e an d acu te righ t-sided
w eakn ess. A CT scan of th e h ead revealed acute left ICH, rem ote
from th e IIA site. Th e h ep arin w as reversed an d th e pat ien t w as
taken em ergently to the operating room for evacuation of the ICH
an d excision of th e IIA (Fig. 59.3). Th e pat ien t tolerated th e n eu-
rosurgical p rocedure w ell. Path ological exam in at ion of th e IIA
dem on strated bran ch ing sept ated hyph ae (Fig. 59.4). An t ifu ngal
th erapy w as in st it u ted an d th e p at ien t ret u rn ed to th e op erat ing
room 1 m on th later for replacem en t of h is ascen ding aort a an d
aor t ic valve. Th e resected graft w as posit ive for Aspergillus. Th e
pat ien t con t in u ed du al an t ifu ngal t reat m en t w ith voricon azole
an d caspofungin for 6 w eeks. At 6-m on th follow -up, th e pat ien t
w as fu n ct ion ally in dep en den t .

Case 2
A 50-year-old m an w it h n o sign ifican t p ast m ed ical h istor y
p resen ted w ith acute on set of h eadach e, n ausea, an d vom it ing,
prom pt ing a CT scan of th e h ead (Fig. 59.5). On physical exam i-
n at ion , a h ear t m u r m u r w as n oted , an d ech ocard iograp hy re-
vealed severe m it ral valve regu rgit at ion w ith veget at ion s. A di-
agn ost ic angiogram w as sign ifican t for a left-sided P4 an eu r ysm
(Fig. 59.6). The cardiothoracic surgeon recom m ended m itral valve
replacem en t requiring an ticoagu lat ion postoperatively. Given th e Fig. 59.5 Axial noncontrast computed tom ography (CT) scan of the head
n eed for perioperat ive an t icoagulat ion , an en dovascular t reat- with a left occipital intracerebral hem orrhage (ICH) and a left subdural
m en t w as favored. Th e pat ien t w as taken for coil em bolizat ion of hem atom a.

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59 Infectious Intracranial Aneurysms 695

Fig. 59.7 Lateral digital subtraction angiogram of the posterior circula-


tion after coil em bolization of a P4 aneurysm and parent vessel sacrifice.
Fig. 59.6 Lateral view of a digital subtraction angiogram with a vertebral
artery injection showing a P4 aneurysm .

th e an eu r ysm w ith vessel occlu sion (Fig. 59.7). Blood cult ures talit y w as 30%. A series of 10 pat ien ts w h o un der w en t surger y
w ere posit ive for Rothia dentocariosa an d th e p at ien t w as t reated for IIAs w as publish ed by Ph uong et al14 in 2002. Th e im m ediate
w ith in t raven ous an t ibiot ics an d su bsequen tly un der w en t a suc- su rgical m orbid it y w as 20%. On e rep or ted p at ien t d evelop ed
cessful m it ral valve replacem en t. aph asia, an d on e pat ien t presen ted w ith n ew -on set in com plete
th ird n er ve p alsy postop erat ively. On follow -u p exam in at ion , th e
aph asic pat ien t h ad im proved but w as st ill disabled, an d th e
th ird n er ve palsy resolved, resu lt ing in 10%long-term m orbidit y.
■ Outcomes Ch u n et al13 also p u blish ed a series of 10 p at ien t s t reated su rgi-
Th e h eterogen eou s n at u re of th e p at ien t popu lat ion presen t ing cally for IIAs. No p ostoperat ive deficit s w ere iden t ified, an d n in e
w it h IIAs m akes gen eralizin g abou t ou tcom es ch allen ging. A of 10 h ad Glasgow Outcom e Scale scores of 5 at follow -up.
com p reh en sive review of t h e literat u re rep or ted t h at 36%of p a- Ch apot et al1 rep or ted a series of 18 IIAs in 14 pat ien t s m an -
t ien ts w ere t reated m edically, 45% w ere t reated surgically, an d aged en d ovascu larly. Of t h e 18 an eu r ysm s, five w ere located
17% w ere m an aged w ith en dovascu lar in ter ven t ion s. Outcom es proxim ally an d 13 w ere in th e dist al circu lat ion . Of th e five p rox-
for th e en t ire populat ion w ere an alyzed; 62% h ad posit ive out- im al an eu r ysm s, fou r w ere t reated w ith an eu r ysm al coiling an d
com es, w h ereas 20% declin ed n eu rologically. A 17% m or t alit y on e required vessel sacrifice (coil em bolizat ion ) of th e M1 seg-
rate w as n oted. Of th ose p at ien t s w h o died, 15% did so prior to m en t . In n in e of 13 dist al an eu r ysm cases, both th e an eu r ysm
in ter ven t ion an d 2% did so follow ing su rgical or en d ovascu lar an d th e paren t vessel w ere em bolized w ith cyan oacr ylate. Th e
t reat m en t .10 rem ain ing four an eur ysm s w ere t reated w ith paren t vessel oc-
To st rat ify outcom es am ong t reat m en t groups, it is n ecessar y clusion on ly. Im m ediate postoperat ive n eurologic d eficit s w ere
to exam in e in dividu al case series. In 2007, Kan n oth et al28 pub - iden t ified in t w o of 18 cases an d con sisted of a m ild h em iparesis
lish ed a series of 25 pat ien ts w ith IIAs. In it ially, 16 w ere t reated an d a qu adran tan opia, yielding a 12.5%m orbidit y. How ever, both
m edically, of w h om seven im proved, six required surger y, an d deficit s h ad resolved on follow -u p exam in at ion , yielding n o
three died. The surgical m ortalit y w as 9.1% and the m edical m or- long-term m orbidit y an d m or t alit y.1

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696 V Cerebral and Spinal Aneurysms

Fig. 59.8 Decision-making tree for the m anagem ent of ruptured versus unruptured IIAs. IIA, infectious intracranial aneurysm ; Rx, prescription.

■ Discussion ■ Conclusion
Th e diagn osis an d m an agem en t of IIAs largely dep en d s on th e In fect ious in t racran ial an eu r ysm s are a h eterogen eous group of
et iology of th e path ogen . Treat ing su rgeon s m ust con sider th e lesion s. W h en in ter ven t ion is in dicated, en dovascu lar t reat m en t
need for additional surger y, requirem ents for anticoagulation, and sh ou ld be favored, given th e frequ en t n eed for cardiac su rger y
th e dyn am ic n at u re of th ese lesion s. As in th e case of saccu lar an d an t icoagu lat ion . W h en eloqu en t cor tex is at r isk, effor t s
an eur ysm s, th e t reat m en t paradigm for IIAs depen ds on th e n a- sh ou ld be m ad e, en d ovascularly or surgically, to evalu ate th e p o-
t u re of p resen tat ion (Fig. 59.8). Un r u pt u red IIAs sh ou ld receive ten t ial deficits of vessel sacrifice. Revascularizat ion follow ed by
path ogen -specific or em p iric m edical th erapy follow ed by repeat su rgical or en dovascu lar exclu sion of th e an eu r ysm sh ou ld be
im aging of th e an eu r ysm 2 w eeks after diagn osis. Stable or in - con sidered w h en pre- or in t raop erat ive test ing predict s a post-
creasing size of th e an eur ysm is a st rong in dicat ion for in ter ven - operat ive deficit from vessel sacrifice. W h en in creased ICP re-
t ion . Con t in u ed su r veillan ce is in dicated w h en th e an eu r ysm is qu ires su rgical in ter ven t ion , th e preop erat ive prep arat ion sh ou ld
redu ced in size. Ru pt u red IIAs t ypically requ ire surgical or en do- in clude a plan for su rgical IIA t reat m en t if possible. Based on th e
vascu lar t reat m en t . h istorically h igh m orbidit y an d m or talit y associated w ith IIAs,
an aggressive m u lt idisciplin ar y approach is required.

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59 Infectious Intracranial Aneurysms 697

References
1. Ch apot R, Houdar t E, Sain t-Maurice JP, et al. En dovascular t reat m ent of 17. Fukuda W, Daitoku K, Min akaw a M, Fukui K, Suzuki Y, Fukuda I. In fect ive
cerebral m ycot ic an eur ysm s. Radiology 2002;222:389–396 en docardit is w ith cerebrovascular com plicat ions: t im ing of surgical in -
2. Corr P, Wrigh t M, Han dler LC. En docardit is-related cerebral an eur ysm s: ter ven t ion . In teract Cardiovasc Th orac Surg 2012;14:26–30
radiologic ch anges w ith t reat m en t . AJNR Am J Neuroradiol 1995;16:745– 18. Karch m er AW. In fect ive En docardit is. Prin ciples of In ternal Medicin e.
748 New York: McGraw -Hill; 2001:809–816
3. Frazee JG, Cah an LD, Win ter J. Bacterial in t racran ial an eur ysm s. J Neuro- 19. Prest igiacom o CJ, Sabit A, He W, Jeth w a P, Gan dh i C, Russin J. Th ree di-
surg 1980;53:633–641 m en sion al CT angiography versu s digit al subt ract ion angiography in th e
4. Gibo H, Car ver CC, Rh oton AL Jr, Len key C, Mitch ell RJ. Microsurgical an at- detect ion of in t racran ial an eu r ysm s in su barach n oid h em orrh age. J Neu -
om y of th e m iddle cerebral ar ter y. J Neurosurg 1981;54:151–169 roin ter v Surg 2010;2:385–389
5. Kan noth S, Th om as SV. In t racran ial m icrobial an eur ysm (in fect ious an eu- 20. Rossi M, Gallo A, De Silva RJ, Sayeed R. W h at is th e opt im al t im ing for
r ysm ): current opt ion s for diagn osis an d m an agem en t . Neurocrit Care surger y in in fect ive en docardit is w ith cerebrovascular com plicat ion s? In -
2009;11:120–129 teract Cardiovasc Th orac Surg 2012;14:72–80
6. Barrow DL, Prat s AR. In fect ious in t racran ial an eur ysm s: com parison of 21. Gou ld FK, Den n ing DW, Elliot t TS, et al; Working Par t y of t h e Br it ish
grou p s w ith an d w ith ou t en docardit is. Neu rosu rger y 1990;27:562–572, Societ y for An t im icrobial Ch em oth erapy. Guidelin es for th e diagn osis an d
discu ssion 572–573 an t ibiot ic t reat m en t of en docardit is in adult s: a repor t of th e Working
7. Bh ayan i N, Ran ade P, Clark NM, McGuin n M. Varicella-zoster vir us an d Par t y of th e Brit ish Societ y for An t im icrobial Ch em oth erapy. J An t im icrob
cerebral aneu r ysm : case repor t an d review of th e literat ure. Clin In fect Ch em oth er 2012;67:269–289
Dis 2008;47:e1–e3 22. Ahm adi J, Tung H, Giannot ta SL, Destian S. Monitoring of infectious intracra-
8. Mah adevan A, Tagore R, Siddappa NB, et al. Gian t serpen t ine aneu r ysm of nial aneurysm s by sequential com puted tom ographic/m agnetic resonance
ver tebrobasilar ar ter y m im icking dolich oect asia—an u n u su al com plica- im aging studies. Neurosurgery 1993;32:45–49, discussion 49–50
t ion of pediat ric AIDS. Report of a case w ith review of th e literat ure. Clin 23. Zador Z, Lu DC, Arn old CM, Law ton MT. Deep bypasses to th e dist al poste-
Neu ropath ol 2008;27:37–52 rior circu lat ion : an atom ical and clinical com parison of pretem poral an d
9. Mar tín ez AJ, Sotelo-Avila C, Alcalá H, Willaer t E. Gran ulom atous en ceph a- subtem poral approach es. Neurosurger y 2010;66:92–100, discussion 100–
lit is, in t racran ial ar ter it is, an d m ycot ic an eu r ysm d u e to a free-living 101
am eba. Act a Neuropath ol 1980;49:7–12 24. Rodríguez-Hern án dez A, Rh oton AL Jr, Law ton MT. Segm en tal an atom y
10. Du cr uet AF, Hickm an ZL, Zach aria BE, et al. In t racran ial in fect ious an eu- of cerebellar ar teries: a proposed n om en clat ure. Laborator y invest igat ion .
r ysm s: a com preh en sive review. Neurosurg Rev 2010;33:37–46 J Neurosurg 2011;115:387–397
11. Suw anw ela C, Suw anw ela N, Ch aruch inda S, Hongsaprabh as C. In t racra- 25. Gian n ot t a SL, Macer i DR. Ret rolabyrin t h in e t ran ssigm oid app roach to
nial m ycot ic an eur ysm s of ext ravascular origin . J Neurosurg 1972;36:552– basilar t r un k an d ver tebrobasilar ar ter y ju n ct ion an eu r ysm s. Tech n ical
559 n ote. J Neurosu rg 1988;69:461–466
12. van der Meulen JH, West st rate W, van Gijn J, Habbem a JD. Is cerebral an - 26. Lü ders JC, Stein m et z MP, Mayberg MR. Aw ake cran iotom y for m icrosurgi-
giography in dicated in in fective endocarditis? Stroke 1992;23:1662–1667 cal obliterat ion of m ycot ic an eur ysm s: tech nical repor t of th ree cases.
13. Ch un JY, Sm ith W, Halbach VV, Higash ida RT, Wilson CB, Law ton MT. Cu r- Neurosurger y 2005;56(1, Suppl):E201, discussion E201
ren t m ult im odalit y m an agem en t of in fect ious in t racran ial an eur ysm s. 27. Ray W Z, Dir inger MN, Moran CJ, Zip fel GJ. Early en d ovascu lar coiling
Neurosu rger y 2001;48:1203–1213, discu ssion 1213–1214 of p oster ior com m u n icat in g ar ter y saccu lar an eu r ysm in t h e set t in g of
14. Ph uong LK, Lin k M, Wijdicks E. Man agem en t of in t racran ial in fect ious an - St ap hylococcu s bacterem ia: case rep or t an d review of th e literat u re. Neu -
eu r ysm s: a series of 16 cases. Neurosurger y 2002;51:1145–1151, discus- rosurger y 2010;66:E847
sion 1151–1152 28. Kan n oth S, Iyer R, Th om as SV, et al. In t racran ial in fect iou s an eu r ysm : p re-
15. Br u st JC, Dickin son PC, Hugh es JE, Holt zm an RN. Th e diagn osis an d sen t at ion , m anagem en t an d outcom e. J Neu rol Sci 2007;256:3–9
t reat m en t of cerebral m ycot ic an eu r ysm s. An n Neu rol 1990;27:238–246
16. DiMaio S, Moh r G, Dufour JJ, Albrech t S. Dist al m ycot ic an eu r ysm of th e
AICA m im icking in t racan alicular acou st ic n eurom a. Can J Neurol Sci
2003;30:388–392

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60 Traumatic and Dissecting
Intracranial Aneurysms
Giuseppe Lanzino and Fredric B. Meyer

Th e w idesp read u se of n on invasive vascu lar im aging an d a bet ter Traum atic aneur ysm s have been reported in virt ually all m ajor
u n derst an ding of th e et iop ath ogen esis an d clin ical feat u res of in t racran ial arteries, but th e m ajorit y involve th e in tern al ca-
t rau m at ic an d d issect ing an eu r ysm s h ave led to th eir in creased rot id arter y (ICA) (46%), th e m iddle cerebral arter y (MCA) (25%),
recognition as an uncom m on but im portant source of intracranial and the anterior cerebral artery (ACA) (22%).8 The vessels affected
h em orrh age an d m orbidit y. Th is ch apter p rovides an over view are a fun ct ion of th e m ech an ism of injur y. For exam ple, given th e
of th e in ciden ce, clin ical presen tat ion , an d m an agem en t of in t ra- in t im ate relat ion sh ip of th e su praclin oid ICA an d basilar ar ter y
cran ial t raum at ic an d dissect ing an eur ysm s, as w ell as a discus- w ith th e base of th e skull, TAs of th ese vessels are often associ-
sion of th e blister-like an eu r ysm su bt ype. ated w ith t rau m at ic sku ll fract u res. On th e oth er h an d, TAs local-
ized on dist al bran ch es of th e ar teries form ing th e circle of Willis
are often caused by pen et rat ing injuries an d depressed skull
fract u res.2 Because of th eir superficial locat ion , scalp bran ch es of
■ Intracranial Traumatic Aneurysms th e extern al carot id ar ter y are often involved after even th e m ost
t rivial of blu n t inju ries.9
Incidence Involvem en t of t h e d ist al ACA is t h ough t to be related to
t rau m a secon dar y to d istor t ion of t h e falx from accelerat ion /
Th e exact in ciden ce of t rau m at ic an eu r ysm s (TAs) is u n kn ow n ,
d ecelerat ion forces in a closed h ead inju r y.6 Th e frequen t in -
an d est im ates var y w ith th e ch aracterist ics of th e pat ien t popu -
volvem en t of th e distal ACA an d th e posterior cerebral ar ter y
lat ion an alyzed . In gen eral, TAs occu r in less th an 1% of pat ien ts
(PCA) is probably a fun ct ion of th e an atom ic proxim it y of th ese
evalu ated for in t racran ial an eu r ysm s. Alt h ough rare in ad u lt s,
vessels to th e sh arp edge of th e falx an d th e ten torial in cisura,
TAs con st it u te th e secon d m ost com m on t ype of an eur ysm foun d
respect ively. Cor t ical TAs m ost often involve MCA bran ch es be-
in ch ildren an d adolescen ts.1 Male predom in an ce is con sisten t
cau se m ost of th e cor t ical m an tle adjacen t to th e convexit y is
across th e popu lat ion s st u died.2,3 With th e except ion of pat ien ts
supplied by th ese vessels.5
w ith m issile injuries,3 in w h om th e in ciden ce of m ult iple TAs can
be as h igh as 20%,4 m u lt iple TAs rarely occu r.
Natural History and Diagnosis
Alth ough it is w idely w rit ten th at TAs h ave a h igh risk of r upt ure,
Clinical Features n at ural h istor y dat a are lacking, an d th e t rue risk is un kn ow n .
Based on h istological fin dings, TAs h ave been t radit ion ally su b - Spon t an eous involu t ion of TAs w ith angiograph ic resolut ion can
divided in to t ru e, false, an d m ixed su bt yp es. Mixed an eu r ysm s also occur. For exam ple, Aarabi8 repor ted n o rebleeding in th ree
are t yp ically r upt u red berr y an eur ysm s w ith a false an eur ysm al of four pat ien t s available for follow -up at 13, 69, an d 113 m on th s
com p on en t , w h ich form s at th e site of ru pt u re, an d th u s sh ou ld w h o h ad suffered h em orrh age from a TAs bu t h ad refu sed t reat-
n ot be con sidered am ong th e subt ypes of TAs. Tr ue an d false TAs m en t . How ever, th ere is con sen sus th at on ce form ed, TAs h ave a
are differen t iated by th eir path ophysiological m ech an ism s an d relat ively h igh risk of ru pt u re if progressive en largem en t is dem -
th e com posit ion of th e TA sac. Tru e TAs can be cau sed by direct on st rated on serial im aging st udies. Mor talit y rates in pat ien ts
blun t t raum a or by in direct forces. Th ey represen t a “bulge” in m anaged conser vatively have been reported to be as high as 70%.8
th e vessel an d are com p osed of all th e differen t com p on en t s of How ever, select ion bias m ay be a factor in su ch rep or ts becau se
th e vessel w all. False TAs, on th e oth er h an d , are th e result of di- severely inju red pat ien ts w h o are n ot likely to su r vive th eir origi-
rect in terru pt ion of th e con t in u it y of a vessel w ith a perivascular n al inju r y are less likely to receive aggressive TA t reat m en t.
h em atom a. Th e w all of th e false an eur ysm is com posed on ly of Th e in ter val bet w een t rau m at ic injur y an d TA presen tat ion is
fibrin t issue surroun ding a par t ially organ ized h em atom a. Fibrin variable. Most adults an d ch ildren becom e sym ptom at ic bet w een
rem odeling an d h em odyn am ic excavat ion /recan alizat ion of th e 2 an d 8 w eeks post inju r y, w ith a peak obser ved bet w een 2 an d
h em atom a result in an eu r ysm form at ion .5,6 4 w eeks.5,6 Th ere are report s of except ion ally long in ter vals, as
Low -velocit y p en et rat ing inju r ies are m ore likely to be as- exem p lified by a p at ien t w h o bled 10 years after th e origin al
sociated w it h TAs t h an are h igh -velocit y p roject ile inju r ies.2 injur y.10
Iat rogen ic an eu r ysm s, a sp ecial categor y, h ave been obser ved A h igh in dex of suspicion for vascular injuries sh ould t rigger
after various surgical procedures, including transsphenoidal pro- vascu lar im agin g to test for TAs. Th is is p ar t icu larly im p or t an t
cedures, cran iotom y for t um ors an d vascular lesion s, an d th ird in pat ien t s w ith t rau m at ic h em atom a after a p en et rat ing inju r y
ven t riculostom y, an d h ave been reported even after placem en t an d in pat ien ts w ith a previou s t raum a w h o h ave a delayed su b -
of extern al ven t ricu lar drain s.7 arach n oid h em orrh age (SAH) or in t racran ial h em orrh age (ICH).

698

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Trau m at ic an eu r ysm s of th e m iddle m en ingeal ar ter y can be re- Treatment


spon sible for delayed expan sion of epidu ral h em atom as or even
in t raparen chym al h em orrh ages.11 Trau m at ic an eu r ysm s can be a th erap eu t ic ch allenge. Before th e
Th e p oin t of en t r y, pat tern , an d m ech an ics of pen et rat ing in - adven t of en dovascular tech n iques, th e m ain th erapeut ic opt ion
juries m ake a differen ce in th e poten t ial for developing a TA. For w as an open su rgical in ter ven t ion con sist ing of p aren t vessel
exam ple, th e in ciden ce of TAs h as been rep or ted to be esp ecially sacrifice w ith or w ith ou t byp ass. Becau se TAs often lack a t r u e
h igh in pat ien t s w ith pen et rat ing injuries an d in t racran ial h em a- w all, an d th e ou tlin ing is m ade u p of a sim ple fibrin layer, su rgi-
tom a an d w h en th e project ile en t r y is in th e facial/orbitopteri- cal m an ipu lat ion of TAs is associated w ith a h igh risk of in t raop -
on al area, exten ds across th e m idlin e or m ult iple in t racran ial erat ive r u pt u re. How ever, in som e cases, th e base of t h e TA can
com p ar t m en t s, or crosses areas of h igh vessel d en sit y, su ch as be “st rong” en ough to accept a surgical clip (Fig. 60.1).3 How ever,
t h e sylvian fissu re or t h e in terh em isp h er ic fissu re.8,12 Tran s- m any pat ien t s are crit ically ill or recovering from an un derlying
orbital injuries w ith in tracran ial pen et rat ion carr y a h igh risk of t rau m at ic con dit ion , in creasing th e likelih ood of su rgical com p li-
vascu lar inju r y, an d all su ch pat ien ts sh ould be tested for TA.5,13 cat ion . Th e brain is edem atou s an d friable, an d, if d ist al, TAs can
TAs in th e cavern ous sin u s an d pet rous ICA can exer t m ass effect be difficu lt to fin d .
an d p resen t w it h caver n ou s sin u s syn d rom e or can cau se ep i- With variou s en dovascu lar tech n iques available, th e m ajorit y
st a xis.5 A t r iad of sku ll base fract u re, u n ilateral blin d n ess, an d of TAs can be t reated safely even in th e acute ph ase, an d th e out-
ep ist a xis is st ron gly suggest ive of a carot id inju r y at t h e sku ll com e is often a fu n ct ion of t h e severit y of t h e origin al inju r y
base.5 rath er th an th e TA per se.3,12 En dovascu lar occlu sion of th e p ar-
As p hysician aw aren ess of th e poten t ial for TAs h as in creased, en t vessel in p at ien t s w ith ad equ ate collateral circu lat ion h as
th e m ajorit y of TAs are d iagn osed as par t of a prep lan n ed vascu - becom e a preferred an d less invasive altern at ive approach .14 Suc-
lar st u dy to look for th is possibilit y rath er th an after ru pt ure of cessful select ive obliterat ion of TAs, w h ile sparing th e paren t ar-
th e TA.8 A m in orit y of TAs are detected becau se of m ass effect s. ter y w ith coils or coil-assisted sten ting, also h as been reported.12,15
W it h t h e w id esp read availabilit y an d sop h ist icat ion of cu r- How ever, th is lat ter st rategy is ch aracterized by a h igh recu r-
ren t h elical com p u ted tom ograp hy (CT), CT angiograp hy (CTA) ren ce rate an d th e n eed for ret reat m en t du e to coil com pact ion ,
represen t s a valid screen ing m eth od for TAs. In cases in w h ich aneurysm regrow th, and coil m igration.12,15 Cohen et al12 reported
th ere is a h igh likelih ood of vascu lar inju ries based on th e m ech - th at of 13 pat ien ts w ith TAs t reated en d ovascularly, one pat ien t
an ism an d pat tern of injur y or th e clin ical/radiological pict ure, u n der w en t coiling w ith com plete obliterat ion an d n o recurren ce
cath eter angiograp hy sh ou ld be p u rsu ed even if th e CTA is n ega- at follow -u p . How ever, on e of th e th ree p at ien ts t reated w ith
t ive. Alth ough a repeat vascu lar st u dy m ay be in d icated after a sten t-assisted coiling w as fou n d to h ave an eu r ysm recan aliza-
n egat ive angiograp hy, th e yield is u su ally low. For exam ple, de- t ion at follow -u p. Th at p at ien t w as su bsequ en tly an d defin it ively
spite conduct ing a repeat angiograph ic st u dy 2 w eeks to 1 m on th t reated w ith en dovascu lar coil occlu sion of th e carot id an d su -
after an in it ial n egat ive st u dy, Coh en et al12 fou n d n o TAs in a perficial tem p oral ar ter y–MCA byp ass. As par t of a large st u dy
series of 15 p at ien t s w ith pen et rat ing h ead inju ries con sidered on w ar-t raum a h ead w ou n ds, Bell an d colleagu es 3 repor ted on a
at risk for TA. series of 14 intracran ial TAs treated w ith endovascular techn iques.

a b

Fig. 60.1a,b This young boy was adm it ted following a traum a resulting in the anterior com m unicating artery complex. The pseudoaneurysm was
anterior cranial fossa fracture. The original head computed tom ography separated from surrounding structures at surgery and clip ligated. (b) Post-
(CT) scan (not shown) dem onstrated an unusual am ount of subarachnoid operative angiogram shows complete occlusion of the pseudoaneurysm.
hem orrhage (SAH). (a) Angiogram showed a pseudoaneurysm involving

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700 V Cerebral and Spinal Aneurysms

Th ir teen w ere t reated w it h coilin g alon e, an d on e w it h sten t - factors cited for ext racran ial dissect ion s are n ot u sually im pli-
assisted coiling. Five of t h e 13 requ ired ad d it ion al t reat m en t cated in th e et iop ath ology of in t racran ial dissect ion s, alth ough
becau se of recu rren ce or regrow t h , an d th ree requ ired su rgical con gen it al con n ect ive t issu e d isord ers su ch as Eh lers-Dan los
clipp ing. syn drom e an d osteogen esis im p erfecta h ave been sp orad ically
Because of th e lim it at ion s of select ive sac em bolizat ion in pa- rep or ted in associat ion w it h in t racran ial dissect ion s.
t ien ts w ith TAs, several specialized tech n iqu es h ave been devel- Fibrom uscu lar dysp lasia an d cyst ic m edial n ecrosis are com -
oped to provide st ruct ural st rength to th e diseased segm en t an d m on fin dings on post m ortem exam in at ion s of pat ien ts w ith dis-
en d olu m in al recon st r u ct ion , w h ile p reser ving th e paten cy of th e sect ion s bu t ten d to be n on sp ecific an d associated w ith a variet y
paren t vessel. In th is resp ect , th e u t ilizat ion of flow diver ters for of system ic disorders. Th e putat ive role of rot ator y st ress in th e
th e t reat m en t of TAs involving large in t racran ial ar teries is an m ore frequ en t involvem en t of th e in t racran ial ver tebral arter y
appealing st rategy. How ever, it requ ires dou ble an t iplatelet th er- (VA) is sp ecu lat ive. It is t h ough t t h at th e p rim ar y p at h ological
apy, w h ich m ay be an issu e in th e set t ing of an acu te m u lt it rau m a m ech an ism of in t racran ial dissect ion s is th e sudden an d w ide-
or in t racran ial h em orrh age.16 spread disrupt ion of th e in tern al elast ic lam in a,18 w h ich even t u-
ally leads to th e form at ion of an in t ram ural h em atom a. Fur th er
progression an d th e t ype of dissect ion probably dep en d on th e
degree of involvem en t an d disr u pt ion of th e m edia layer. If th e
■ Intracranial Dissecting Aneurysms dissect ion exten ds across th e m edia, th en th e dissect ing plan e
bet w een t h e m ed ia an d t h e adven t it ia m ay lead to a su badven -
Clinical Features t it ial dissect ion w ith th e form at ion of a d issect ing an eu r ysm an d
In t racran ial dissect ing an eur ysm s are a poten t ial sou rce of SAH. su bsequ en t p ossible r u pt u re an d resu lt an t SAH. In ar ter ies in
Dissect ion s are in it iated by an in t im al tear th rough w h ich blood w h ich th ere is n o teth ering, such as th e MCA stem , th e pulsat ile
accum ulates bet w een th e differen t layers of th e vessel w all. Th e an d expan sile forces of a grow ing dissect ion can be dissipated by
arterial dilatations that follow are often term ed pseudoaneur ysm s elongation and developm ent of ectasia w ith gradual enlargem ent
or false an eur ysm s, but th ey sh ould be m ore properly called dis- of th e dissect ing segm en t , result ing in th e form at ion of a gian t or
sect ing an eu r ysm s becau se th ey st ill con t ain th e fu n dam en tal serpen t in e an eur ysm .
com p on en ts of th e n orm al vessel w all.17 Fusiform an eur ysm s h ave been con sidered a part icu lar form
Dissect ion s in th e ext racran ial por t ion s of th e ver tebral an d of dissect ing an eur ysm s. Mizut an i an d cow orkers 20 h ave pro-
carotid arteries occur m ostly in the m edia. Th e thicker vessel w all, posed a classification system based on pathological changes of the
relat ive to in t racran ial ar ter y w alls, an d th e su pp ort provided by in tern al elast ic m em bran e, w h ich u n ifies an eur ysm s (fu siform
su rrou n ding st ru ct u res an d p lan es p reven t bleeding. In t racran ial an d dissect ing) th at are n ot associated w ith bran ch ing poin t s.
ar teries lack an extern al elast ica layer, an d all of th e elast ic t issue
is concentrated in a thin internal elastic lam ina. The internal elas-
tic lam in a, com p osed m ostly of elast in an d collagen , p lays a cen -
Incidence and Location
t ral role in d eterm in ing ar terial w all st rength . Th e p rim ar y factor Th e in ciden ce of in t racran ial dissect ing an eu r ysm s rep or ted in
responsible for rem odeling, degeneration, and loss of the internal th e literat u re varies. In a 1988 st u dy con du cted in Japan , Yam -
elast ic m em bran e is h em odyn am ic st ress. Vessel w all vibrat ion aura 21 fou n d th e rate of dissect ing an eu r ysm s w as 28%in a series
from h em odyn am ic st ress is h eavily im plicated in th e tearing of of 94 ver tebral an eur ysm s, an d 10.4%in a series of 230 posterior
th e in tern al elast ic lam in a. In an au top sy st u dy of p at ien t s w ith circulat ion an eu r ysm s. In m ore con tem porar y large case series
intracranial dissecting aneurysm s, disruption of the internal elas- of both ru pt ured an d u n rupt ured an eur ysm s, dissect ing in t ra-
tic m em bran e w as fou n d in all n in e specim en s st u died.18 cran ial VA an eur ysm s con st it uted 1.6 to 1.9% of all an eur ysm s
Unlike ext racranial vessels, in tracranial vessels have a very th in t reated.22,23
m uscularis an d adven t it ial layers (t w o-th irds th in n er th an th eir Th ere ap p ears to be a m ale p redom in an ce for dissect ing an -
ext racran ial cou n terpar t s), w h ich m akes th em vu ln erable to t h e eu r ysm s, w h ich con t rast s w ith th e clear fem ale p redom in an ce
effect s of t raum a.19 In addit ion , th ey do n ot h ave extern al sup - observed in berr y aneur ysm s.24 Patients w ith intracranial dissec-
port as they pass th rough th e subarachnoid space. It has been sug- tion s presen ting w ith hem orrhagic sym ptom s ten d to be slightly
gested th at th ese factors m ake in t racran ial vessels m ore pron e to older th an th ose presen t ing w ith isch em ic or oth er n on h em or-
ar terial dilat at ion s an d pseu doan eur ysm form at ion on ce a dis- rh agic sym ptom s. In a th e n at ionw ide st udy con ducted in Japan
sect ion occu rs. In rupt u red dissect ing an eu r ysm s, th e w all adja- bet w een 1995 an d 1996, Yam aura et al25 foun d th e m ean age of
cen t to t h e site of r u pt u re is com p osed of adven t it ia or fibr in pat ien ts w ith in t racran ial dissect ion s presen t ing w ith SAH w as
associated w ith th rom bu s.18 53 years com pared w ith 48.9 years for pat ien ts presen t ing w ith
n on h em orrh agic sym ptom s.
Th e p osterior circu lat ion is m ore com m on ly involved th an th e
Etiology an terior circu lat ion . Posterior circu lat ion dissect ion is also m ore
Th e et iology of in t racran ial dissect ion is u n kn ow n , bu t is prob - com m on in adu lt s th an in ch ildren an d you ng adu lt s.26 Th e m ost
ably th e result of a m ult ifactorial process involving both gen et ic/ com m on site is th e V4 segm en t of th e VA at or n ear th e posterior
con gen it al an d acqu ired /environ m en t al factors. Th e effect of in ferior cerebellar ar ter y (PICA) origin . An terior circu lat ion dis-
m ech an ical st retch in g, w ell st u d ied in ext racran ial d issect ion , sections are m ore com m on in older adults than in ch ildren and
m ay n ot ap p ly to in t racran ial d issect ion s. Trau m a can lead to you n g ad u lt s.25 W h en fou n d in ad u lt s, t h e m ost com m on site is
in t racran ial dissect ing an eur ysm s in ch ildren , but in adults th ere t h e su p raclin oid ICA (Fig. 60.2) an d t h e M1/2 t r u n ks (Fig. 60.3).
is t ypically n o h istor y of t rau m a. In addit ion , th e com m on risk Dissect ing an eu r ysm s h ave been rep or ted in vir t u ally ever y in -

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60 Traumatic and Dissecting Intracranial Aneurysms 701

a b

c d

Fig. 60.2a–d This 19-year-old otherwise healthy m an presented with aneurysm involving the left internal carotid artery (ICA) extending from
sudden onset of headache and transient loss of consciousness. (a) Com - the supraclinoid potion to the bifurcation and the proxim al A1 segm ent.
puted tom ography (CT) scan of the head showed a large subarachnoid (d) The aneurysm was treated with parent artery sacrifice and coil occlu-
hem orrhage (SAH) with focal clot extension from the carotid cistern to the sion of the pseudoaneurysm al portion.
ipsilateral sylvian fissure. (b,c) Catheter angiography showed a dissecting

t racran ial vessel (Fig. 60.4). Th ere are several repor ted cases of w ill form w ith possible vessel rupture and hem orrh age.28 Indeed,
bilateral dissect ion s, occu rring sim u ltan eou sly or con secu t ively, in th e vast m ajorit y of p at ien t s w h o presen ted w ith h em orrh age
involving th e in t radu ral por t ion of th e VA.27 an d w ere st u died at au topsy, th e p lan e of dissect ion lay bet w een
th e m edia an d th e adven t it ia or w ith in th e m edia it self.18 In t ra-
cran ial d issect ion s p resen t ing bot h w ith isch em ia an d h em or-
Natural History and Clinical Presentation rh age are rare but h ave been repor ted.29
Risk of h em orrh age is related to th e pat tern of dissect ion . Dissec- There is a correlation bet w een the angiographic/m orphological
t ion s w ith an “en t r y on ly” p at tern in w h ich a tear form s in th e ap p earan ce an d t h e clin ical p resen t at ion of d issect ing an eu -
in t im a bu t th ere is n o reen t r y, h ave been fou n d to h ave a greater r ysm s. Kw ak an d colleagu es 30 st u d ied 133 p at ien t s w it h r u p -
ch an ce of ru pt u ring an d bleeding th an th ose th at h ave a reen t r y t u red an d u n r u pt u red in t racran ial d issect ion s ad m it ted over a
poin t .24 A long-h eld dogm a st ated th at if th e dissect ion is be- 7-year p eriod from 2000 to 2007. Pat ien t s w ere divid ed in to
t w een th e in t im a an d th e m edia, n arrow ing an d clot form at ion t h ree grou p s accord in g to t h eir an giograp h ic p at ter n : sten o -
w ill result in possible isch em ia. How ever, if th e dissect ion occu rs occlusive (46%), com bin ed sten o-occlusive an d an eu r ysm al (27%),
bet w een the m edia and the adventitia, a bulge (pseudoaneur ysm ) an d isolated an eur ysm al (22%). Th e sten o-occlu sive pat tern w as

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702 V Cerebral and Spinal Aneurysms

a b

c d

Fig. 60.3a–d This 21-year-old wom an presented with sudden onset of (b,c) Lateral and anteroposterior (respectively) right internal carotid artery
headache that occurred during intercourse. (a) A com puted tom ogram injection demonstrate the aneurysm. The aneurysm was treated with surgi-
showed a predom inantly right sylvian fissure subarachnoid hem orrhage cal trapping. She suffered a silent small infarct, but made a full and unevent-
(SAH) due to a dissecting dist al m iddle cerebral artery (MCA) aneurysm . ful recovery. (d) Angiography reveals the trapped segment of the vessel.

m ore frequen tly related to in farct ion th an w as th e isolated an eu- th e first w eek or t w o after p resen t at ion ), an d invasive t reat m en t
r ysm al p at ter n , w h ich w as m ore com m on ly associated w it h sh ould be con sidered. On th e oth er h an d, ch ron ic an d in ciden t al
h em orrhage. dissect ion s diagn osed after th e acu te p h ase ten d to h ave a ver y
Headach e w ith ou t associated h em orrh age is a frequ en t p ro- ben ign n at ural h istor y. In a long-term st u dy of 98 pat ien t s w ith
drom e of ru pt u re in p at ien t s w ith in t racran ial dissect ing an eu - in t racran ial u n rupt u red dissect ion s presen t ing w ith eith er isch -
r ysm s. In a series of 206 in t racran ial arterial dissect ion s, 78% of em ic sym ptom s or h eadach e, on ly on e p at ien t su ffered a SAH,
pat ien ts w ith dissect ing VA an eu r ysm s w h o even t u ally su ffered an d it occurred 11 days after th e on set of sym ptom s.24 Purely
a SAH h ad h ad preceding h eadach e, w h ich w as n on specific in in ciden tal dissect ion s w ere n ot in clu ded in th is series. Eigh teen
93%. In 96% of th ose w ith preceding h eadach e, SAH occurred percen t of pat ien ts w ith dissect ing an eu r ysm s sh ow ed com plete
w ith in 3 days. Th e longest in ter val bet w een on set of h eadach e h ealing at follow -up im aging, suggest ing th at m any un r upt ured
an d SAH w as 11 days.24 Sim ilarly, in a series of 21 pat ien ts w ith dissect ion s m ay be un diagn osed.24
VA dissect ing an eu r ysm s w h o in it ially p resen ted w ith ou t h em -
orrh age, Naito et al31 repor ted bleeding occu rred w ith in 1 day in
Treatment and Outcomes
t w o pat ien ts. In th e rem ain ing 19 pat ien t s, on ly on e ep isode of
bleeding occurred after 51 m on th s. Th ese obser vat ion s suggest In pat ien t s w h o presen t w ith h em orrh age, t reat m en t of th e dis-
that dissecting aneur ysm presenting w ith non hem orrhagic sym p - sect ing an eu r ysm is in dicated in th e acu te p h ase after m edical
tom s sh ou ld be regard ed w ith suspicion in th e acu te ph ase (e.g., an d n eu rologic stabilizat ion . As w ith berr y an eur ysm s, th e risk

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60 Traumatic and Dissecting Intracranial Aneurysms 703

a b

Fig. 60.4a–c A 44-year-old wom an presented with high-grade subarach-


noid hem orrhage (SAH). (a) Catheter angiography showed a dissecting
pseudoaneurysm of the left superior cerebellar artery, which was treated
with coil occlusion (b). The patient eventually m ade a good recovery.
(c) Follow-up catheter angiography 8 years later shows persistent occlusion
of the dissecting pseudoaneurysm with partial recanalization of the parent
c artery.

of rebleed ing in con ser vat ively t reated h em or rh agic p at ien t s is con st r uct ive en dovascular t rapping h as been foun d to be w ell
h igh .32 tolerated, especially if th e pat ien t h as adequate leptom en ingeal
Th ere are several su rgical an d en dovascu lar t reat m en t s for collaterals from th e ipsilateral an terior in ferior cerebellar arter y
dissect ing an eu r ysm s. Th e ch oice depen ds on th e locat ion , clin i- (AICA).22,23
cal p resen t at ion , collateral circu lat ion , an d involvem en t of crit i- In th e m ajorit y of pat ien ts, en dovascular t rapping of dissect-
cal side bran ches and perforating bran ch es. Despite an in creasing in g an eu r ysm s d ist al to t h e PICA can be p er for m ed w it h ou t u n -
n u m ber of “con st r u ct ive” tech n iqu es aim ed at p reser ving t h e tow ard con sequ en ces. How ever, d isast rou s con sequ en ces can
p aren t ar ter y, in ou r exp er ien ce t h e en d ovascu lar or su rgical occu r, depen ding on th e origin of th e an terior spin al ar ter y. Typi-
t rapp ing of VA dissect ing an eu r ysm s w ith or w ith ou t byp ass is cally, the an terior spinal arter y has a fairly sym m etric origin from
th e t reat m en t of ch oice. W h en con sidering th e t rap ping of a VA both distal VAs before un it ing to form a single m idlin e t run k. But
dissect ing an eu r ysm , it s locat ion relat ive to th e PICA—proxim al if it h as a u n ilateral or igin , ip silateral to t h e d issect ion , tet rap a-
to th e PICA origin , involving th e PICA, or dist al to it—is of para- resis can occur after en dovascular t rapping.33
m oun t im portan ce.23 An eu r ysm s p roxim al to PICA u su ally can As en dovascu lar tech n iqu es h ave becom e m ore sop h ist icated,
be t rapped en dovascularly w ith ou t com plicat ion , as long as th e th e u se of recon st r u ct ive tech n iqu es, su ch as sten t-assisted coil-
pat ien t h as a con t ralateral VA22 (Fig. 60.5). Th ose w ith PICA in - ing, sten t-w ith in -sten t tech n ique, or lately, flow diver ters, h as
volvem en t can be t reated w ith con st ruct ive en dovascular tech - in creased. Alth ough good result s h ave been reported w ith sten t-
n iqu es (telescoping sten t s or, m ore recen tly, flow diver ters). An - coiling an d sten t-w ith in -sten t , pat ien t s, esp ecially in th e acu te
oth er valid altern at ive, albeit m ore invasive, is surgical t rapp ing phase, are not com pletely protected from the risk of rebleeding.23
w ith occipital-to-PICA bypass or PICA-to-PICA bypass. Even de- In all cases, close follow -u p is n ecessar y becau se of t h e r isk of

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704 V Cerebral and Spinal Aneurysms

a b

c d

Fig . 60.5a– d A 36-year-old wom an experienced sudden headache. ing aneurysm is distal to posterior inferior cerebellar artery (PICA) origin.
(a) Head com puted tom ogram showed posterior fossa subarachnoid Given the large contralateral VA, the aneurysm was treated with endovas-
hem orrhage (SAH) with fourth ventricular hem orrhage. (b) Right vertebral cular trapping with preservation of the PICA. (c,d) VA angiography demon-
artery angiography showed retrograde filling of the contralateral vertebral strates VA occlusion and filling of the PICA.
artery (VA), which is involved by a dissecting pseudoaneurysm . The dissect-

fu r t h er p seu d oan eu r ysm grow t h 23 an d t h e p oten t ial n eed for tal clip ping w ith ou tflow occlu sion . Th is last st rategy, alth ough
ret reat m en t . Th e ap p licat ion of flow d iver ters to th e t reat m en t cou n ter in t u it ive, is based on t h e p r in cip le t h at occlu d in g t h e
of d issect ing pseu doan eu r ysm s in th e VA or oth er locat ion s is outflow results in decreased dist al dem an d an d even t ual th rom -
prom ising, bu t on ly a few isolated case repor t s are available th u s bosis of th e pseudoan eur ysm . Th is st rategy h as been origin ally
far, an d th e efficacy an d long-term success of th is approach is d escr ibed for t reat m en t of gian t ser p en t in e MCA an eu r ysm s 35
u n kn ow n .34 Of n ote, w h en flow d iver ters are u sed , du al an t i- an d PICA an eu r ysm s.36
platelet th erapy in th e set t ing of acu te SAH rem ain s an issu e. Th e ou tcom e of pat ien t s w ith r u pt u red in t racran ial dissect ing
Su rgical st rategies for th e t reat m en t of dissect ing an eu r ysm s an eur ysm s depen ds on th e clin ical presen tat ion at adm ission . In
in clu de clip /w rapp ing, t rap ping w ith or w ith ou t bypass, an d dis- a large series of 206 h em orrh agic in t racran ial dissect ion s from a

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60 Traumatic and Dissecting Intracranial Aneurysms 705

n at ionw ide Japan ese st u dy, 53% of p at ien ts exp erien ced a good those patien ts w ho present w ith nonhem orrhagic sym ptom s an d
recover y, an d th e m or talit y rate w as 27%.25 In p at ien ts p resen t- are evaluated w eeks or m on th s after th e on set of sym ptom s or in
ing w ith SAH th at is m an aged con ser vat ively, th e risk of rebleed- th ose w ith dissect ing an eur ysm s diagn osed in ciden t ally, con ser-
ing is h igh , alth ough in a series of n in e ru pt u red VA dissect ion s vat ive m an agem en t is a reason able opt ion (Fig. 60.6). Treat m en t
m anaged conser vatively, Mizutani24 reported spontaneous occlu- can be reser ved for th ose w h o sh ow pseu doan eu r ysm progres-
sion at follow -u p im aging w ith ou t rebleeding in five p at ien t s. In sion on follow -u p. In t racran ial dissect ion s h ave been rep or ted to

a b

Fig. 60.6a–c Incidental intracranial internal carotid artery (ICA) dissecting


aneurysm . This 28-year-old wom an with no significant prior history, under-
went imaging after falling off a bike. A calcified intracranial lesion was noted.
(a,b) Catheter angiography showed an incidental diffuse ICA dissecting pseu-
doaneurysm . (c) Computed tom ography (CT) angiography showed diffuse
calcifications, suggesting a chronic process. The pseudoaneurysm was felt
to be a purely incidental finding and no treatm ent was recom m ended. The
c patient is well 5 years later with no complaints.

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706 V Cerebral and Spinal Aneurysms

recu r in up to 9.5%of p at ien t s, often in differen t arteries th an th e The risk of rehem orrhage is ver y high in blister-like aneur ysm s
on e involved at on set .24 Th e m ajorit y occur w ith in 1 m on th of (Fig. 60.9), an d prom pt t reat m en t is recom m en ded. Differen t
th e origin al dissect ion , con firm ing an environ m en t al factor th at th erapeu t ic st rategies h ave been prop osed for th ese ch allenging
m ay in crease th e likelih ood of vessel in st abilit y. lesion s. Each h as lim it at ion s due to th e fragilit y of th e vessel w all
an d th e lack of a t r ue sac. Th e bulging por t ion of th e an eur ysm
occasion ally is am en able to p r im ar y clip p in g, bu t t h is st rategy
is often associated w ith in t raop erat ive com plicat ion s. Su t u ring
■ Intracranial Blister-Like Aneurysms of th e tear can be d on e in som e cases, bu t can in crease t h e size
Blister-like an eu r ysm s rep resen t a u n ique con dit ion . Th ere is a of th e tear because its edges are too friable to h old th e sut ure.
con t roversy over w h eth er blister an eu r ysm s rep resen t a form of “Con st ru ct ive” su rgical tech n iqu es in clu de p arallel clip p ing, cir-
d issect ing an eu r ysm s, a “sim p le” h ole in th e blood vessels, or cum feren t ial w rapping w ith fascia, Dacron , or periosteum .38 Th e
both . Th ey h ave been described as involving a segm en t along th e Su n dt clip graft can be a valid solu t ion to th is problem esp ecially
an terom edial w all of th e supraclin oid ICA. Th ey are n ot related to in sm aller blisters. It can also be u sed in th e presen ce of in t raop -
th e origin of eith er th e p osterior com m u n icat ing ar ter y (PCoA) erat ive rupt u re of th e ten u ou s pseu doan eur ysm al w all.39
or th e an terior ch oroidal ar ter y (ACh A). Th e path ogen esis of blis- It is advisable to expose th e cer vical ICA for proxim al con t rol
ter an eur ysm s is u n clear, but it appears th at h em odyn am ic st ress an d to con sider a balloon test occlusion before pu rsuing a surgi-
m ay n ot be a m ajor factor because th ey ten d to involve sites w ith cal ap p roach . Prep arat ion of t h e su p er ficial tem p oral ar ter y or
less im p inging blood flow. even t h e rad ial ar ter y for a p oten t ial byp ass is also advised .40
Diagn osis of blister-like an eu r ysm s is based on angiograph ic Paren t ar ter y occlu sion , w ith or w ith ou t su p p lem en t al byp ass,
feat ures, alth ough th ey can often be m issed on an in it ial angio- is th e surgical t reat m en t of ch oice because it excludes com pletely
gram . Th ey t yp ically app ear as an arterial “bu lge” w ith a broad th e w eak arterial segm en t from th e circu lat ion .40 How ever, com -
base (Fig. 60.7), or as irregular prot r usion s of th e dorsal w all of plete t rap ping is n ot alw ays possible becau se th e lesion m ay in -
th e ICA. Th ese lesion s lack an in tern al elast ic m em bran e as part volve th e origin of a large PCoA, or w orse, th e AChA.
of th eir w all, w h ich is m ade up of disten ded fragile adven t it ia Construct ive endovascular procedures w ith coiling alon e often
an d perilesion al th rom bus. Alth ough th ey rarely grow ver y large, fail due to progressive expansion and even rerupture of the pseu-
th e m ost com m on in dicat ion of th eir p resen ce is th eir in creasing d oan eu r ysm . In a review of 22 p at ien t s t reated w it h coiling
grow th on serial angiograp h ic st u dies (Fig. 60.8).37 alon e, 14 (64%) experien ced regrow th . It is possible th at coiling

a b

Fig. 60.7a,b A 37-year-old wom an presented with thunderclap headache on CT angiography, a catheter angiography was perform ed (b). This study
to an outside institution. (a) Head computed tom ography (CT) did not suggested an irregularit y involving the supraclinoid portion of the ICA
show subarachnoid hem orrhage (SAH). Because of the suspicious history (arrow). Given the lack of SAH, no treatm ent was recom mended at this
and the suggestion of an irregularit y of the internal carotid artery (ICA) point.

Neurosurgery Books Full


60 Traumatic and Dissecting Intracranial Aneurysms 707

a b

Fig. 60.8a–c The patient in Fig. 60.7 was readm it ted 1 m onth later with
sudden-onset headaches. (a) Head com puted tom ography (CT) showed a
diffuse subarachnoid hem orrhage (SAH). (b) She was transferred to our
institution, where a catheter angiography showed a blister-like aneurysm ,
which had developed at the site of the sm all broad-base bulge. (c) Three-
dimensional reconstruction of the catheter angiogram demonstrates a small
aneurysm arising from a non-branch point on the dorsal internal carotid
c artery (ICA).

alon e m ay “st abilize” th e lesion because repeat coiling is often sh ou ld be in terp reted w ith cau t ion becau se p at ien t s w ith p oor
associated w ith stabilit y at follow -up.37 Sten t-assisted coiling ou tcom e an d rebleed in g are less likely to be rep or ted in t h e
can be su ccessfu l becau se t h e sten t m ay p rovid e som e d egree literat u re th an th ose w ith good clin ical an d angiograph ic out-
of en d ovascu lar st ren gt h to t h e vessel w all. Sten t -w it h in -sten t com es. As is t r u e for dissect ing an eu r ysm s, th e n eed for dou ble
tech n iques w ith m ult iple telescoping stents h ave also been de- platelet th erapy in th e set t ing of an acu te SAH is a m ajor lim ita-
scribed.41 More recen tly, t reat m en t w ith flow -diver ters h as been t ion , bu t th e flow -diver ter ap p roach h olds som e p rom ise for an
rep or ted ,42,43 alt h ough t h e n u m bers are sm all. Th ese rep or t s obviou sly ch allenging con dit ion .

Neurosurgery Books Full


708 V Cerebral and Spinal Aneurysms

a b

Fig. 60.9a,b The sam e patient as in Figs. 60.7 and 60.8. The blister-like later shows stable residual. The patient is well without any deficits 3 years
aneurysm was treated with stent-assisted coiling. (a) Catheter angiography post treatm ent.
demonstrates the final coil mass. (b) Follow-up catheter angiography 1 month

dit ion s, en dovascu lar t reat m en t is often th e p rim ar y in ter ven -


■ Conclusion t ion . Su rger y is also a valid an d w ell-est ablish ed altern at ive in
With in creased aw aren ess an d bet ter im aging tech n iques, in t ra- cases w h ere an en dovascu lar ap proach is n ot ideal. Th e ou tcom e
cran ial t rau m at ic an d dissect ing an eu r ysm s are n ot in frequ en tly of pat ien ts w ith t raum at ic an d dissect ing an eu r ysm s is often
en cou n tered in clin ical pract ice. Trau m at ic an eu r ysm s are often d ict ated by t h e p r im ar y effect of t h e in it ial inju r y or t h e asso-
discovered before r u pt u re in p at ien t s w ith inju ries or m ech a- ciated h em orrh age, resp ect ively. W it h an in d ivid u alized t reat -
n ism of injur y suspiciou s for vascular im pairm en t . Dissect ing m en t , good resu lt s can be ach ieved in th e m ajorit y of p at ien t s.
an eur ysm s are a recogn ized cau se of subarach n oid h em orrh age Blister-like an eur ysm s represen t a separate en t it y an d con t in ue
an d are m ore frequen t in th e posterior circu lat ion th an in any to be a t h erap eu t ic ch allenge even w ith m od er n su rgical an d
other location. Given the challenges encountered w ith these con - en dovascu lar t reat m en ts.

References
1. Aeron G, Abru zzo TA, Jon es BV. Clin ical an d im aging feat ures of in t racra- 9. An dreoli A, Togn et t i F, Lan zin o G. Traum at ic an eur ysm of th e superficial
n ial ar terial an eur ysm s in th e pediat ric populat ion . Radiograph ics 2012; tem poral ar ter y from fist injur y. Br J Neurosurg 1990;4:353–354
32:667–681 10. Cour ville CB. Trau m at ic an eur ysm of an in t racran ial ar ter y. Descript ion of
2. Larson PS, Reisn er A, Morassut t i DJ, Abdulh adi B, Harpring JE. Traum at ic lesion in ciden t to a sh ot gun w oun d of th e skull an d brain . Bull Los Angel
int racranial an eur ysm s. Neurosurg Focus 2000;8:e4 Neu ro Soc 1960;25:48–54
3. Bell RS, Vo AH, Rober t s R, Wan ebo J, Arm on da RA. War t im e t raum at ic 11. Brun eau M, Gust in T, Zekh n in i K, Gilliard C. Traum at ic false an eu r ysm of
an eur ysm s: acute presen t at ion , diagn osis, an d m ult im odal t reat m en t of th e m idd le m en ingeal ar ter y cau sing an in t racerebral h em orrh age: case
64 cran iocer vical arterial injuries. Neurosurger y 2010;66:66–79, discus- report an d literat ure review. Surg Neurol 2002;57:174–178, discussion
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4. Haddad FS, Haddad GF, Tah a J. Trau m at ic in t racran ial an eur ysm s caused 12. Coh en JE, Gom ori JM, Segal R, et al. Result s of en dovascular t reat m en t of
by m issiles: th eir presen t at ion an d m an agem en t . Neurosurger y 1991;28: t raum at ic in t racran ial an eur ysm s. Neurosu rger y 2008;63:476–485, dis-
1–7 cu ssion 485–486
5. Sem ple PL. Aneu r ysm s. In : Le Rou x PD, Win n HR, New ell DW, eds. Man - 13. d u Trevou M, Bu llock R, Teasdale E, Qu in RO. False an eu r ysm s of t h e
agem en t of Cerebral An eur ysm s. Ph iladelph ia: Saun ders; 2003:397–407 carot id t ree due to un suspected pen et rat ing injur y of th e h ead an d n eck.
6. Kum ar M, Kitch en ND. In fect ive an d t rau m at ic an eur ysm s. Neurosurg Clin Inju r y 1991;22:237–239
N Am 1998;9:577–586 14. Jadhav AP, Pr yor JC, Nogueira RG. Onyx em bolizat ion for th e en dovascular
7. Kost y J, Pukenas B, Sm ith M, et al. Iat rogen ic vascular com plicat ion s as- t reat m en t of in fect ious an d t raum at ic an eu r ysm s involving th e cran ial
sociated w ith external ven t ricular drain placem ent: a repor t of 8 cases an d cerebral vascu lat u re. J Neu roin ter v Su rg 2013;5:562–565
and review of th e literat ure. Neu rosurger y 2013;72(2, Suppl Operat ive): 15. Fulkerson DH, Voorh ies JM, McCan n a SP, et al. En dovascu lar t reat m en t
on s208–ons213, discussion on s213 an d rad iograp h ic follow -u p of p roxim al t rau m at ic in t racran ial an eu r ysm s
8. Aarabi B. Man agem en t of t rau m at ic aneur ysm s caused by h igh -velocit y in adolescen t s: case series an d review of th e literat ure. Childs Ner v Syst
m issile h ead w oun ds. Neurosu rg Clin N Am 1995;6:775–797 2010;26:613–620

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16. Am en t a PS, St arke RM, Jabbour PM, et al. Successful t reat m en t of a t rau- 32. Yam ada M, Kit ah ara T, Kurat a A, Fujii K, Miyasaka Y. In t racran ial ver tebral
m at ic carot id pseudoan eur ysm w ith th e Pipelin e sten t: Case repor t and ar ter y dissect ion w ith su barach n oid h em orrh age: clin ical ch aracterist ics
review of th e literat ure. Surg Neurol In t 2012;3:160 an d ou tcom es in con ser vat ively t reated pat ien t s. J Neu rosu rg 2004;101:
17. Ch en M, Caplan LR. In t racran ial dissect ion s. In : Baum gar t n er RW, Bo- 25–30
gousslavsky J, Caso V, Paciaron i M, eds. Han dbook on Cerebral Ar ter y Dis- 33. Iw ai T, Naito I, Sh im agu ch i H, Su zu ki T, Tom izaw a S. Angiograp h ic fin d -
sect ion . Basel, Sw it zerlan d: Karger; 2005 in gs an d clin ical sign ifican ce of th e an terior an d posterior spin al ar teries
18. Mizut an i T, Kojim a H, Asam oto S, Miki Y. Path ological m ech an ism an d in th erapeut ic paren t arter y occlusion for ver tebral arter y an eur ysm s.
th ree-dim en sion al st ru ct u re of cerebral dissect ing an eu r ysm s. J Neu ro- In ter v Neuroradiol 2000;6:299–309
surg 2001;94:712–717 34. Narat a AP, Yilm az H, Sch aller K, Lovblad KO, Pereira VM. Flow -diver t ing
19. Yon as H, Dujovny M. “True” t raum at ic an eur ysm of th e in t racran ial in ter- sten t for r upt ured in t racran ial dissect ing an eur ysm of ver tebral ar ter y.
nal carot id arter y: case report . Neurosurger y 1980;7:499–502 Neurosurger y 2012;70:982–988, discu ssion 988–989
20. Mizut an i T, Miki Y, Kojim a H, Suzuki H. Proposed classificat ion of n on ath - 35. Horow it z MB, Yon as H, Ju ngreis C, Hung TK. Man agem en t of a gian t m id-
erosclerot ic cerebral fusiform an d dissect ing an eu r ysm s. Neurosurger y dle cerebral arter y fusiform serpen t in e an eur ysm w ith dist al clip applica-
1999;45:253–259, discussion 259–260 t ion an d ret rograde throm bosis: case repor t an d review of th e literat u re.
21. Yam aura A. Diagn osis an d t reat m en t of ver tebral an eur ysm s. J Neurosurg Surg Neurol 1994;41:221–225
1988;69:345–349 36. Nussbaum ES, Madison MT, Goddard JK, Lassig JP, Janjua TM, Nussbau m
22. Peluso JP, van Rooij W J, Sluzew ski M, Beute GN, Majoie CB. En dovascu lar LA. Rem ote dist al ou tflow occlu sion : a n ovel t reat m en t opt ion for com -
t reat m en t of sym ptom at ic in t radural vertebral dissect ing an eur ysm s. plex dissect ing an eu r ysm s of th e posterior in ferior cerebellar ar ter y. Re-
AJNR Am J Neuroradiol 2008;29:102–106 port of 3 cases. J Neurosurg 2009;111:78–83
23. Jin SC, Kw on DH, Ch oi CG, Ah n JS, Kw un BD. En dovascular st rategies for 37. Mat subara N, Miyach i S, Tsukam oto N, et al. En dovascular coil em boliza-
ver tebrobasilar dissect ing an eur ysm s. AJNR Am J Neu roradiol 2009;30: t ion for saccular-sh aped blood blister-like an eur ysm s of th e in tern al ca-
1518–1523 rot id ar ter y. Act a Neuroch ir (Wien) 2011;153:287–294
24. Mizut an i T. Nat ural course of in t racran ial arterial dissect ion s. J Neurosurg 38. Regelsberger J, Mat sch ke J, Grzyska U, et al. Blister-like an eur ysm s—a
2011;114:1037–1044 diagn ost ic and th erapeut ic ch allenge. Neurosurg Rev 2011;34:409–416
25. Yam au ra A, On o J, Hirai S. Clinical pict ure of in t racran ial n on -t raum at ic 39. Park PJ, Meyer FB. Th e Sun dt clip graft . Neu rosurger y 2010;66(6, Suppl
dissect ing an eur ysm . Neuropath ology 2000;20:85–90 Operat ive):300–305, discussion 305
26. Sch ievin k W I, Mokri B, Piepgras DG. Spon t an eous dissect ion s of cer vico- 40. Başkaya MK, Ah m ed AS, Ateş O, Niem an n D. Surgical t reat m en t of blood
ceph alic ar teries in ch ildh ood an d adolescen ce. Neurology 1994;44:1607– blister-like an eur ysm s of th e supraclin oid in tern al carot id ar ter y w ith
1612 ext racran ial-in t racran ial bypass an d t rapping. Neurosurg Focu s 2008;24:
27. Ot aw ara Y, Ogasaw ara K, Ogaw a A, Kogu re T. Dissect ing an eur ysm s of th e E13
bilateral vertebral arteries w ith subarachn oid hem orrh age: report of three 41. Gaugh en JR Jr, Hasan D, Dum on t AS, Jen sen ME, McKen zie J, Evans AJ. Th e
cases. Neu rosurger y 2002;50:1372–1374, discussion 1374–1375 efficacy of en dovascular sten t ing in th e t reat m en t of supraclin oid in ter-
28. Caplan LR. Dissect ion s of brain -supplying arteries. Nat Clin Pract Neurol n al carot id arter y blister an eur ysm s using a stent-in -sten t tech n ique.
2008;4:34–42 AJNR Am J Neuroradiol 2010;31:1132–1138
29. Alot aibi NM, Fugate JE, Kau fm an n TJ, Rabin stein AA, Wijdicks EF, Lan zin o 42. Mart in AR, Cr uz JP, Matouk CC, Spears J, Marot t a TR. Th e pipelin e flow -
G. Int racranial supraclin oid ICA dissect ion causing cerebral in farct ion an d diver t ing sten t for exclu sion of r u pt u red in t racran ial an eu r ysm s w ith dif-
subsequen t subarach n oid h em orrh age. Neu rocrit Care 2013;18:252–256 ficult m orph ologies. Neurosurger y 2012;70(1, Suppl Operat ive):21–28,
30. Kw ak JH, Ch oi JW, Park HJ, et al. Cerebral ar ter y d issect ion : sp ect r u m of discu ssion 28
clin ical presen t at ion s related to angiograph ic fin dings. Neuroin ter ven - 43. Con soli A, Nappini S, Ren ieri L, Lim bu cci N, Ricciardi F, Mangiafico S.
t ion 2011;6:78–83 Treat m en t of t w o blood blister-like an eur ysm s w ith flow diverter sten t-
31. Naito I, Iw ai T, Sasaki T. Man agem en t of in t racran ial ver tebral ar ter y dis- ing. J Neuroin ter v Surg 2012;4:e4
sect ion s in it ially presen t ing w ith out subarachn oid h em orrh age. Neuro-
surger y 2002;51:930–937, discu ssion 937–938

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61 Giant Aneurysms
M. Yashar S. Kalani and Robert F. Spetzler

Gian t an eu r ysm s are som e of th e rarest an d m ost form idable le- represented significant im provem ents on the existing sm all- series
sion s th at n eurosurgeon s en cou n ter. Defin ed by th e Cooperat ive rep or ts of t reat m en t of th is path ology. Despite Dan dy’s repor t of
St u dy of In t racran ial An eu r ysm s an d Su barach n oid Hem orrh age directly clip ping th e n ecks of an eu r ysm s u sing m od ified Cu sh ing
as lesion s w h ose largest diam eter is ≥ 2.5 cm , th ese lesion s con - silver clips, the t reatm ent of choice for gian t aneurysm s rem ained
st it u te 2 to 5%of all an eu r ysm s.1 Th e progn osis for pat ien ts w ith t h e h u n ter ian ligat ion of feed in g vessels, m ost com m on ly t h e
un t reated gian t an eu r ysm s is p oor,2,3 an d th e goal of t reat m en t carot id ar ter y.11
sh ou ld be safe an d com p lete obliteration of th e an eu r ysm . His- Th e n ext m ajor im provem en t in th e t reat m en t of t h ese le-
torically, gian t an eur ysm s h ave been treated su rgically. More re- sion s w as described in t w o series, on e by Drake 12 (174 an eu -
cen tly, en dovascu lar tech n iqu es h ave en abled clin ician s to m ake r ysm s, predom in an tly vertebrobasilar) an d th e other by Sun dt
great strides and im provem ents in the treatm ent of these difficult an d Piepgras 13 (80 an eu r ysm s, p redom in an tly carot id circu la-
cases, bu t th e long-term du rabilit y of th ese tech n iqu es rem ain s t ion ), in w h ich th ese su rgical gian ts d em on st rated su ccessfu l
a con cern . Th e use of flow -diver t ing sten ts is likely to fur th er t reat m en t w ith direct su rgical at tack. Desp ite im provem en ts in
im prove th e outcom e of pat ien t s w ith gian t an eu r ysm s, bu t dat a an eur ysm t reatm en t , th ese series dem on st rated th e differen t ial
on long-term ou tcom es for th ese devices are st ill pen ding, an d outcom e of an eu r ysm s in th e an terior an d posterior circulat ion ,
t h eir u se m ay n ot be t h e opt im al t reat m en t m odalit y in all w ith th e form er being m ore am en able to t reat m en t an d h aving
cases.4,5 Despite sign ifican t progress, th e best data an d repor ted bet ter ou tcom es. Th e exp erien ce of t h ese grou p s also d em on -
outcom es for th e safe an d com plete obliterat ion of gian t an eu- st rated t h at n ot all an eu r ysm s can be effect ively clip p ed , an d
r ysm s rem ain th ose from surgical series. Th is ch apter discusses oth er tech n iques su ch as flow reversal an d proxim al-vessel oc-
th e n at ural h istor y of gian t an eu r ysm s, th e t reat m en t st rategies clusion m ay be con sidered in un clipp able cases. More recen tly,
an d considerat ion s, an d th e outcom es of both surger y an d en do- several grou ps h ave rep or ted im proved p at ien t ou tcom es, w ith
vascu lar t reat m en t . Oth er ch apters in th is sect ion of th e book m ort alit y rates of 3 to 15%an d m orbidit y rates of 5 to 33%(Table
discu ss th e su rgical an d en dovascu lar t reat m en t of specific an - 61.1) for pat ients w ith th ese lesion s.
eu r ysm t yp es.

■ Pathology and Pathophysiology


■ History of Giant Aneurysm Treatment Saccu lar an eu r ysm s are th e m ost com m on su bt yp e of gian t an -
Hu tch in son 6 in 1875 w as th e first au t h or to rep or t th e case of a eu r ysm . Ap p roxim ately 60% of gian t an eu r ysm s occu r in t h e
pat ien t w ith a gian t an eu r ysm . He rep or ted on a 40-year-old an terior circulat ion , m ostly on th e proxim al in tern al carot id ar-
w om an w h o h ad presen ted w ith facial p ain , left ext raocu lar ter y (ICA), an d th e rem ain ing are foun d on bran ch es of th e verte-
m u scle paralysis, an d h eadach es. Hu tch in son diagn osed th e an - brobasilar system (Table 61.2). Gian t fusiform /serpen t in e 14 an d
eu r ysm based on an au dible br u it , an d sch edu led th e pat ien t for in fect ious an eu r ysm s 15 are rarer an d are post u lated to be caused
h un terian ligat ion of th e carot id ar ter y. At th e recom m en dat ion by dissect ion s an d in fect iou s et iology, respect ively.
of h is colleagues, h e did n ot perform th e procedure, an d th e pa- Th e p ath ological basis for th e m ajorit y of an eu r ysm s is poorly
t ien t su ccu m bed to th e com p licat ion s of a r u pt u red aor t ic an eu - u n derstood . Several lin es of eviden ce poin t to a t ran sm issible ge-
r ysm . At autopsy, a large calcified m ass th e size of a “h en’s egg” n et ic factor as th e pathophysiological basis of som e an eur ysm s.
w as identified protruding into the m iddle fossa. Given the lim ita- Pat ien t s w it h fam ilial p olycyst ic kid n ey d isease an d m u t at ion s
tions of diagnostic im aging of the tim e, m ost giant aneurysm s w ere in th e PKD gen es, as w ell as pat ien ts w ith fibrom uscular dyspla-
iden t ified p ost m or tem or as a resu lt of w orku p for “t u m ors.”7–9 sia an d oth er m u scu locutan eou s syn drom es, h ave dem on st rated
Over th e n ext 80 years, several in n ovat ion s, in clu ding cerebral an in creased risk for aneur ysm form at ion .16 More recen tly, sev-
angiography by Mon iz an d ven t riculography an d direct surgical eral oth er loci su ch as RBBP8, STARD13-KL, Sox17, an d CDKN2A-
clipping of an eur ysm s by Dan dy, resu lted in sign ifican t im prove- CDKN2B h ave been iden t ified as being associated w ith a h igh er
m en t s in th e outcom es of pat ien ts w ith an eur ysm s. In 1969, t w o risk of aneur ysm form ation.17,18 However, m ost aneur ysm s appear
large series on th e diagn osis an d m an agem en t of pat ien t s w ith to form de n ovo in patien ts w ithout a fam ily histor y of aneur ysm s
gian t an eur ysm s w ere publish ed.7,10 Alth ough th e descript ion s an d are likely to be caused by ch ron ic st ress on th e blood vessel
of gian t an eu r ysm s in t h ese early ser ies are based on p lain ra- w alls. Fu r th erm ore, scan n ing elect ron m icroscopy of th e bifurca-
d iography of th e skull, m ass effect as eviden ced by perivascular tion of intracranial vessels has revealed sign ificantly larger fen es-
disp lacem en t on angiography, an d surgeon s’ d escript ion s, th ey t rat ion s at th ese sites th an th ose n orm ally presen t th rough ou t

710

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Neurosurgery Books Full
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61

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Giant Aneurysms

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711
712 V Cerebral and Spinal Aneurysms

Table 61.2 Distribution of Giant Aneurysms in the Cerebral Circulation

Author No. of aneurysms ICA (%) MCA (%) ACA (%) VBA (%)

Sanai and Lawton 153 * 117 52 (44) 18 (15) 13 (11) 24 (21)


Lawton and Spet zler30 * 171 94 (55) 27 (16) 13 (8) 39 (23)
Sundt 154 * 323* 182 (56) 58 (18) 16 (5) 49 (15)
Peerless et al119 * 635 213 (34) 49 (8) 9 (3) 354 (56)
Hosobuchi121 * 84 56 (67) 4 (5) 9 (11) 15 (18)
Sym on and Vajda 155 * 55 26 (47) 10 (18) 7 (13) 12 (22)
Yaşargil156 * 31 14 (45) 4 (13) 1 (3) 12 (39)
Onum a and Suzuki157 * 32 15 (47) 3 (9) 10 (31) 4 (13)
*Som e patients had m ultiple giant aneurysm s.
Abbreviations: ICA, internal carotid artery; MCA, middle cerebral artery; ACA, anterior cerebral artery; VBA, vertebrobasilar
artery.
Source: From Sanai N, Lawton MT. Microsurgical managem ent of giant intracranial aneurysm s. In: Winn HR, ed. Youmans
Neurological Surgery, 6th ed. Philadelphia: Elsevier Saunders; 2011:3953–3971. Reprinted with permission from Elsevier.

th e system ic ar terial system .19 It is believed th at ch ron ic st ress pop u lat ion are gian t at p resen tat ion , suggest ing th at p ediat ric
cau sed by hyp er ten sion an d toxic m et abolic an d environ m en t al an eur ysm s m ay h ave a differen t biology from th at of th eir adult
factors (sm oking and stim ulant drugs) com bine to result in endo- cou n terp ar t s.25,29 Alt h ough an eu r ysm s overall occu r m ore fre-
thelial dam age and aneurysm form ation. The rarit y of an eur ysm s qu en tly in w om en , gian t an eu r ysm s in all region s oth er th an th e
in ch ildh ood argu es again st a congen it al origin as th e cause of proxim al ICA are m ore frequ en tly docu m en ted in m en . Th e over-
m ost an eu r ysm s in ad ults. all fem ale-to-m ale rat io ranges from 2:1 to 3:1, due to th e rela-
Th e an eu r ysm w all con sist s of viable t issu e th at h as u n der- t ive p rep on d eran ce of t h e m ore com m on p roxim al ICA lesion s
gon e ch ron ic dam age. Elim in ation of flow in to th e an eu r ysm al in w om en .30,31
segm en t en ables th e n orm alizat ion of blood flow w ith in th e ves- As is th e case w ith sm aller an eu r ysm s, som e gian t an eu r ysm s
sel an d p rovides a ch an ce for repair an d n eoen doth elializat ion . rem ain unchanged for years, w hereas others exhibit rapid grow th,
Treat m en t p lan n ing for sm all an d large an eu r ysm s dep en ds on becom e sym ptom at ic, an d r upt ure in on e-quarter to on e-th ird of
th e st rategy ch osen for flow exclu sion an d rein forcem en t of n a- cases.1,7,10,12,30,31 In rare cases, spon t an eous th rom bosis h as been
t ive blood vessel w all. Pu lsat ile an d irregu lar blood flow w ith in docu m en ted.32,33 Th e best st udies on th e outcom e of un t reated
th e an eu r ysm exer t s force on th e diseased vessel w all. Th is force gian t an eu r ysm s are t h ose p u blish ed by Drake’s grou p s.3 Th e
can cau se th e an eu r ysm sac to d isten d, th in ou t , an d grow.20 In experien ce from th is grou p suggest s th at th e n at u ral h istor y of
an at tem pt to h eal th e an eur ysm , th e body m ay in duce th rom bus an un t reated gian t an eur ysm (except th ose of th e cavern ous ca-
form at ion an d rem odeling of th e lum in al surface of th e en dothe- rot id arter y) is poor, w ith m orbidit y an d m ort alit y in excess of
lium .21,22 Unfortunately, ch ron ic, irregular, pulsatile flow does not 80% at 5 years associated w ith con ser vat ive t reat m en t. Peerless
provide th e body w ith th e op por t u n it y to h eal in an organ ized an d Drake 2 reported m ort alit y rates of 68% an d 85% at 2 an d 5
fash ion , an d disorgan ized collagen , ath erosclerot ic degen erat ion , years, resp ect ively, for u n t reated gian t an eur ysm s, an d even pa-
th rom bi of var ying age, an d dyst roph ic calcificat ion can resu lt . t ien ts w h o su r vived su ffered m arked n eu rologic dysfu n ct ion .
Con sequ en tly, gian t an eu r ysm s are dyn am ic lesion s w ith cyclical Kodam a an d Suzuki34 repor ted th at 75%of th eir un t reated h ospi-
cascades of th rom bu s form at ion an d resolu t ion . Not su rpris- talized pat ien t s died of subarach n oid h em orrh age (SAH). Nat ural
ingly, th ese lesion s can frequ en tly develop calcificat ion s. In addi- h istor y st udies suggest an an n ual rupt ure rate for gian t an eu-
t ion , a prom in en t sym ptom of gian t an eu r ysm s is th rom boem - rysm s of 6%, w hich is higher than the 0.5 to 3%rate seen in sm aller
bolic even ts,21,23,24 likely cau sed by th ese ep isodes of th rom bosis an eur ysm s.27
an d resolut ion . Th ese even ts m ay result in an eur ysm grow th an d
possibly ru pt u re, alth ough su barach n oid h em orrh age presen ta-
t ion is rare. Th e an eu r ysm sac m ay grow at th e n eck or fu n du s Clinical Presentation
an d m ay in corporate bran ch poin ts or perforat ing vessels, adding An terior circulat ion gian t an eur ysm s are located in th e cavern -
to th e t reat m en t challenge of th ese vascu lar an om alies. ous, paraclin oid, an d carot id bifu rcat ion region s of th e ICA, th e
proxim al m id dle cerebral ar ter y (MCA), an d th e an terior cerebral
ar ter y (ACA)/an terior com m un icat ing ar ter y (ACoA), in order of
Natural History m ost to least com m on presen tat ion . Gian t an eur ysm s of th e A1,
Pat ien t s w it h gian t an eu r ysm s u su ally p resen t in t h e fou r t h p er icallosal-callosom argin al ar ter y, an d t h e p oster ior com m u -
t h rough sixt h d ecad es of life, bu t t h ese lesion s h ave also been n icat ing ar ter y (PCoA) h ave been rep or ted bu t are exceed ingly
rep or ted in p ediat ric an d geriat ric pat ien t s.25–27 Th e p eak fre- rare.35–39 Posterior circulation aneur ysm s are located at the basilar
qu en cy of gian t an eu r ysm s is a decad e later th an sm aller an eu - ap ex, m idbasilar ar ter y, ver tebral arter y, ver tebrobasilar jun c-
r ysm s, an d th is st at ist ic h as been cited as eviden ce for th e grow th t ion , an d rarely on th e posterior in ferior cerebellar ar ter y (PICA)
of gian t an eur ysm s from sm aller coun terpar ts, alth ough rapid and anterior inferior cerebellar artery (AICA). Am ong patients w ith
grow t h of an eu r ysm s in sh or ter p er iod s h as been rep or ted .28 gian t an eur ysm s, 10 to 30% h ave oth er associated an eu r ysm (s),
Bet w een on e-qu ar ter an d on e-h alf of an eu r ysm s in th e p ediat ric and treatm ent m ust take into account hem odynam ic alterations

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61 Giant Aneurysms 713

Table 61.3 Aneurysm Location and Symptoms Caused by Mass also im proved th e visualizat ion of th rom bosed an d calcified an -
Effect eu r ysm con ten t s, an d con t rasted sequ en ces en able clin ician s
to d eter m in e flow ch aracter ist ics w it h in t h e an eu r ysm (Fig.
Aneurysm Location Presenting Mass-Effect Symptoms
61.1a,b). Xen on - CT en ables fu r th er evalu at ion of gian t an eu-
Anterior circulation Visual deficits r ysm s by sh ow ing collateral cerebral blood flow during tem po-
Cavernous ICA Retro-orbital headaches, diplopia, rar y carot id occlu sion an d is u sed in p rep arat ion for or an t ici-
or facial sensory loss; occasionally p at ion of revascu larizat ion . Th e an eu r ysm m orph ology relat ive
hypopituitarism; rarely epistaxis to th e sku ll base is w ell depicted on CT im aging. CT angiography
Ophthalm ic or paraclinoid ICA Ipsilateral retro-orbital headache
(Fig. 61.1c,d) is a n on invasive test , an d th u s it redu ces th e pos-
with decreased visual acuit y and
sible m orbidit y associated w ith angiography, especially in elderly
asymmetric visual field defects
pat ien ts, w h o are at h igh er risk for p rocedu ral com p licat ion s. We
Carotid bifurcation Visual field defects (homonymous
rou t in ely use CT angiography after an eur ysm clipping to en sure
hemianopsia), hem iparesis,
an eur ysm obliterat ion an d for follow -up .
seizures, dem entia, rarely
Noninvasive m agnetic resonance im aging (MRI) studies provide
hypopituitarism
ACA-ACoA Visual field defects (bitemporal th e best an atom ic in form at ion of gian t an eu r ysm s. MRI en ables
loss), decreased visual acuit y,
horm onal changes caused by
compression of the hypo-
thalamus, personalit y changes
Posterior circulation Posterior fossa symptoms, lower
cranial nerve deficits, gait
instabilit y
Abbreviations: ICA, internal carotid artery; ACA, anterior cerebral artery; ACoA,
anterior comm unicating artery

an d th eir effect on th ese oth er an eu r ysm s. Pat ien t s w ith gian t


an eur ysm s frequ en tly (60–80%) presen t w ith th rom boem bolic
even ts or w ith sym ptom s related to n eurovascu lar com pression
cau sed by m ass effect (esp ecially t r u e of p oster ior circu lat ion
an eu r ysm s t h at occu py t h e sm all sp ace of th e p oster ior
fossa).1,7,10,12,30,31 Pat ien t s p resen t ing w ith m ass effect gen erally
h ave a bet ter progn osis th an th ose w ith oth er sym ptom s.40
Sym ptom s of m ass effect depen d on an eu r ysm locat ion an d di-
rect ion of grow th (Table 61.3).
An eur ysm al r upt ure cau sing subarach n oid or in t raparen chy- a
m al h em orrh age is a less likely presen t at ion (20–30% of cases),
w it h a w orse ou tcom e t h an m ass effect .40 Pat ien t s w it h rap id
an eu r ysm al grow t h (frequ en t ly cau sed by acu te t h rom bosis)
can p resen t w ith severe h eadach es an d resem ble p at ien ts w ith
h em orrh age. Presen tat ion s th at occur m ore rarely in clude sei-
zures (usually caused by an MCA an eur ysm ), h em iparesis, an d
h em iplegia.

■ Treatment Strategies and


Considerations
Diagnostic Tests and Data Acquisition
Historically, p lain sku ll rad iograp hy w as u sed to diagn ose gian t
an eur ysm s. Gian t an eur ysm s are frequen tly calcified (20% of
cases),7 an d th e calcificat ion can be iden t ified by radiograp hy.
Addit ionally, giant aneur ysm s m ay rem odel th e skull base and the b
sella (40% of cases 7,41 ), an d th ese ch anges can also be iden t ified
Fig . 61.1a–f Com puted tom ography (CT) for aneurysm diagnosis.
on plain radiography. Th e oth er im aging m odalit y h istorically
(a) Sagit tal CT depicts a giant aneurysm of the anterior com m unicating
used in th e diagn osis of an eu r ysm s w as cerebral angiography. artery complex after subarachnoid hem orrhage. (b) Axial CT dem onstrates
Th e adven t of com p u ted tom ograp hy (CT) h as im p roved t h e a giant fusiform vertebrobasilar artery aneurysm compressing the brain-
m easu rem en t of an eur ysm size an d p aren t vessel caliber. It h as stem . (continued on page 714)

Neurosurgery Books Full


714 V Cerebral and Spinal Aneurysms

c d

e f

Fig. 61.1a–f (continued ) (c) Three-dim ensional (3D) reconstruction coro- trunk. Lateral (e) and anteroposterior (f) angiogram s dem onstrate dim inu-
nal CT angiography (CTA) shows the aneurysm al dilatation of the anterior tive posterior com m unicating arteries and no filling of the posterior circula-
com m unicating artery com plex in a patient with a giant aneurysm . (d) 3D tion in a patient with a dolichoectatic vertebrobasilar artery aneurysm . This
reconstruction coronal CTA dem onstrates a dolichoectatic vertebrobasilar patient failed an Allcock test. (Courtesy of Barrow Neurological Institute.)
artery aneurysm that includes brainstem perforators located on the basilar

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61 Giant Aneurysms 715

th e visu alizat ion of th e th rom bu s, often w ith it s ch aracterist ic Table 61.4 Selection of Surgical Approach Based on Location of the
on ion -r ing ap p earan ce of lam in ated , in ter ven ing layers of h e- Giant Aneurysm
m osid erin an d m eth em oglobin .42 Flu id-at ten u ated inversion re-
Site of Aneurysm Skull Base Approach
cover y (FLAIR) sequ en ces dem on st rate p erilesion al edem a th at
can be associated w ith rap id an eu r ysm al en largem en t or acu te Proximal internal carotid artery Pterional, orbitozygom atic
t h rom bosis. Magn et ic reson an ce an giograp hy (MRA) can d em - Bifurcation of the internal carotid Pterional, orbitozygomatic
on st rate t h e in t racran ial circu lat ion , bu t at ou r in st it u t ion th is artery
st u dy is seld om ord ered as w e rely on a com bin at ion of CT im - Proximal anterior cerebral artery Pterional, orbitozygomatic
Distal anterior cerebral artery Pterional, orbitozygomatic,
aging an d diagn ost ic angiography in m ost cases. MRA can be
interhemispheric
used to follow pat ien t s w ith coiled an eu r ysm s, bu t it h as lim ited
Middle cerebral artery Pterional, orbitozygomatic
u t ilit y in cases of su rgical clip p in g d u e to t h e sign ifican t clip
Vertebral artery Far lateral
ar t ifact .
Vertebrobasilar junction Far lateral
Conven t ion al angiograp hy is th e gold stan dard for obt ain ing
Midbasilar artery Petrosal, far lateral,
an atom ic in for m at ion , in clu d ing p aren t vessel an atom y, an eu -
orbitozygom atic
r ysm m or p h ology, locat ion of p er forat in g vessels, feasibilit y of High basilar artery Orbitozygomatic
vessel occlu sion , evalu at ion of byp ass opt ion s, an d bot h in t ra- Posterior inferior cerebellar artery Far lateral, suboccipital
cran ial–in t racran ial an d ext racranial–in t racran ial collaterals (Fig. Anterior inferior cerebellar artery Petrosal, far lateral,
61.1e,f). Angiography can be used to assess vascu lar reser ve by orbitozygom atic
p er for m in g balloon -test occlu sion an d Allcock’s test .43–47 As a Superior cerebellar artery Orbitozygomatic
t reat m en t m odalit y, d iscu ssed elsew h ere, angiograp hy can be
Source: From Lem ole GM, Henn J, Spet zler RF, Riina HA. Surgical m anagem ent
used to coil em bolize an an eur ysm or to p lace flow diverters to of giant aneurysms. Oper Tech Neurosurg 2000, 3:239–254. Reprinted with
obliterate an eur ysm s. A caveat w ith t radit ion al angiography is permission from Elsevier.
th at it m ay fail to disclose th e an eu r ysm ’s t ru e size w h en a sig-
n ifican t port ion of th e an eur ysm is filled w ith th rom bus. In ch il-
dren , angiograp hy sh ou ld be p erform ed w ith great cau t ion given possible em bolic sou rce, w h ile p reser ving th e pat ien t’s baselin e
th e con cern abou t rad iat ion exp osu re an d ch ild ren’s in abilit y to n eu rologic st at u s.
tolerate large volum es of con t rast agen t . Th e su ccessfu l m icrosu rgical t reat m en t of gian t an eu r ysm s
dep en ds on a solid u n derstan ding of sku ll base p rocedu res an d
facilit y w ith th e m icrosurgical t reat m en t of an eur ysm s in clud-
Treatment Considerations
ing variou s byp ass opt ion s. In t reat ing gian t an eur ysm s, skull
Given th e poor n at u ral h istor y of gian t an eu r ysm s, w e recom - base approach es (Table 61.4) en able bon e rem oval an d exp osu re
m en d th at th ese lesion s be t reated aggressively. Un t il recen tly at of th e an atom y, w h ich are n ecessar y steps in order to t reat an eu-
our in st it ut ion , all gian t an eu r ysm s w ere in it ially evaluated for r ysm s w ith out u n due com pression of brain an d cran ial n er ves.
su rgical t reat m en t an d m ost w ere t reated su rgically u n less m ed- Th e ten et s of an eu r ysm su rger y in clu de a safe an d at rau m at ic
ical or ot h er con dit ion s p reclu ded m icrosu rgical t reat m en t . With approach , su barach n oid dissect ion , vascular con t rol, an d exclu -
th e adven t of th e flow -diver t ing sten t s, su ch as th e Pipelin e Em - sion of th e an eu r ysm from th e circu lat ion , w h ile p reser ving in -
bolizat ion Device (Covidien /ev3, Redw ood Cit y, CA), m ore gian t flow , ou t flow , an d p aren t an d p er forat in g vessels. An eu r ysm
an eur ysm s of th e ICA are being referred for en dolum in al recon - su rger y h as ben efited greatly from im proved n euroan esth esia
st r u ct ion . Not able except ion s in clu de gian t an eu r ysm s w ith sig- an d th e use of barbit urates, m ild hypoth erm ia, an d circu lator y
n ifican t clot bu rden s an d m ass effect , cases in w h ich perforat ing arrest in rare cases.48 Th ese tech n iqu es allow for m ore aggressive
vessels arising from th e an eu r ysm sac preclude th e deploym en t m an ipu lat ion of th e dom e an d sac w ith ou t fear of r u pt u re, an d
of flow diver ters, an d cases of SAH w h ere sten ts an d an t iplatelet provide th e t im e n ecessar y to perform a byp ass or recon st ru c-
agen t s are con t rain d icated . Alt h ough su rgical clip p ing of t h e t ion proced ure in cases w h ere on e is n ecessar y.
an eur ysm n eck an d clip recon st r uct ion are th e m ost desirable Pat ien t s w ith gian t an eur ysm s w h o p resen t w ith m ass effect
procedures, techn ical or struct ural lim itations such as dysplastic/ or t ran sien t isch em ic at t acks due to em bolic even t s sh ould n ot
fu siform m orph ology or calcified n ecks m ay dict ate a less defin i- u n dergo em ergen t surgical in ter ven t ion . In stead, th ese p at ien t s
t ive t reat m en t , su ch as proxim al or distal vessel occlu sion , an eu - should undergo routine preoperative clearance and m anagem ent .
rysm trapping, or excision w ith or w ithout revascularization w ith We advocate th orough diagn ost ic evalu at ion of an eu r ysm s in -
th e goal of obliterat ing th e an eur ysm . clu ding CT im aging, MRI, an d form al angiograp hy before in it iat-
Th e follow ing discu ssion is based on th e exp erien ce of t h e se- ing t reat m en t .
n ior auth or (R.F.S.) w ith t reat ing m ore th an 6,000 pat ien t s w ith In th e rare in stan ce w h en th e pat ien t presen ts w ith an SAH,
an eur ysm s an d m ore th an 400 pat ien ts w ith gian t an eur ysm s th e goal is to con du ct an early su rger y to exclu de th e an eu r ysm
over the past 30 years. Each patient w ith a giant aneur ysm should an d th en assist th e pat ien t th rough th e post-SAH period. Pat ien t s
be evaluated by an in terdisciplin ar y n eurovascular team , an d all presen t ing w ith SAH requ ire cardioresp irator y an d basic n eu ro-
opt ion s in cluding clipping, t rapping, excision , revascu larizat ion , logic su pp or t ive care, early ven t ricu lostom y w ith cerebrosp in al
an d en d ovascu lar t reat m en t sh ou ld be en ter t ain ed . Th is is es- flu id (CSF) drain age in th ose w ith poor Hun t-Hess scores (grades
p ecially t r ue w ith th e in t roduct ion of flow diver ters an d th e pos- IV an d V), an d vasospasm p rophylaxis.
sibilit y of en dolu m in al recon st ru ct ion . Th e goals of an eu r ysm Acu te t h rom bosis of gian t an eu r ysm s m ay lead to rap id d e-
t reat m en t in clu de obliterat ion of th e lesion , decom p ression of ter iorat ion of a p at ien t ’s n eu rologic st at u s. Th is d eter iorat ion
m ass effect associated w ith th e lesion , an d obliterat ion of th e h as been at t ributed to th rom boem bolic even ts as w ell as a rapid

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716 V Cerebral and Spinal Aneurysms

in crease in th e size of clot w ith in th e an eur ysm , w h ich causes adh eren t perforators to be dissected an d th e an eu r ysm n eck to
in creased m ass effect . In th ese cases it m ay be n ecessar y to oblit- be m an ipu lated for p lacem en t of clips.
erate th e an eu r ysm or decom p ress th e an eu r ysm con ten t s. In At Barrow Neu rological In st it u te, hyp ot h er m ic ar rest s h ave
pat ien ts w h o are t reated w ith byp ass an d proxim al or distal ves- been u sed 105 t im es in 103 p at ien t s w it h an eu r ysm s, 97 of
sel sacrifice, a sh or t cou rse of h ep arin an t icoagu lat ion m ay be w h ich w ere p oster ior circu lat ion an eu r ysm s.4 8 Th ese p oster ior
n ecessar y to preven t rapid th rom bosis an d possible clot t ing of circulat ion an eu r ysm s in cluded 60 basilar apex, 21 m idbasilar,
essen t ial perforators. 11 ver tebrobasilar, an d four superior cerebellar ar ter y (SCA) an -
eur ysm s, as w ell as one posterior cerebral artery (PCA) aneur ysm .
Hypoth erm ic circulator y arrest is a com plex but h igh ly effect ive
Vascular Control and Hypothermic Cardiac Standstill
procedu re; it requ ires an organ ized team effort an d sh ou ld be
Obt ain in g vascu lar con t rol is on e of t h e cen t ral ten et s of an eu - u sed ju diciou sly in appropriate p at ien ts on ly. In th e past 5 years,
r ysm su rger y. Doin g so en ables t h e su rgeon to con t rol in t raop - w e h ave p er for m ed few er t h an 10 of t h ese p roced u res. Th e
erat ive r u pt u re of t h e an eu r ysm , an d p lacin g tem p orar y clip s greater use of aden osin e an d im proved en dovascular tech n iques
en ables t h e robu st h an d lin g of an eu r ysm s d u r in g t h e fin al clip h as greatly lim ited th e use of th is procedure.49,50
placem en t . Obtain ing vascu lar con t rol also en ables th e su rgeon Th e su ccess of hyp oth erm ic cardiac arrest as a tool du ring th e
to op en an d decom p ress an eu r ysm s, a tech n ique th at is par t icu- clipping of com p lex an eu r ysm s is determ in ed by five key vari-
larly u sefu l in t reat ing p at ien ts w ith gian t an eu r ysm s w ith a sig- ables: depth of hypoth erm ia, durat ion of circu lator y arrest , bar-
n ifican t clot bu rden . bit urate use, h em ostasis, an d rate of rew arm ing after an eur ysm
Vascular con t rol in th e an terior circulat ion can be ach ieved by clipping.51 In ou r experien ce of 103 pat ien ts as n oted above,48
accessing th e carot id ar ter y in th e n eck or at th e skull base by th e m ean brain tem perat u re du ring st an dst ill h as been 17.2°C
drilling th e p et rou s bon e at Glasscock’s t riangle. Som e cen ters (range 12–20°C) an d th e m ean du rat ion of stan d st ill w as 21.8
rout in ely expose th e cer vical carot id arter y in all pat ien t s un der- m in utes (range 2–72 m in utes). Th e absolute m axim um period of
going surger y for gian t an terior circu lat ion an eur ysm s. Because cerebral isch em ia th at can be safely tolerated is sign ifican tly in -
it m ay be difficu lt to gain proxim al vascu lar con t rol at th e carot id creased by th e use of profoun d hypoth erm ia an d th e adm in ist ra-
ar ter y exit from t h e caver n ou s sin u s, exp osing t h e cer vical ca- t ion of in t raven ou s barbit u rates before cooling to ach ieve bu rst
rot id ar ter y can be p ar t icu larly ben eficial in t h ese sit u at ion s. suppression of elect roen ceph alogram (EEG) act ivit y. Th e period
In cases of op h th alm ic an d p araclin oid ICA an eu r ysm s, in t racra- of circulator y arrest sh ould be lim ited to fin al an eur ysm dissec-
n ial proxim al con t rol can be ach ieved by rem oving th e clin oid t ion an d clip ap plicat ion . Met icu lou s at ten t ion to in t raoperat ive
process. h em ost asis, m in im al u se of brain ret ract ion , an d close obser va-
Obt ain ing vascu lar con t rol in th e p osterior circu lat ion is m ore t ion of t h e p at ien t’s clot t in g factors are th e keys to m in im izin g
ch allenging. Desp ite th e m ost aggressive su rgical exp osu res, vas- t h e m ost frequ en t ly seen com p licat ion of th is p roced u re—p ost -
cular con t rol in th e posterior circulat ion , w ith it s n eurovascular operat ive h em atom a (seen in 16 pat ien ts).
labyr in t h , is lim ited d u e to sm all an atom ic cor r id ors. Vascu lar Oth er com plicat ion s of hypoth erm ic arrest in our experien ce
con t rol in th is region is fu r th er lim ited by th e presen ce of rich in clude 16 perforator st rokes, seven oth er cerebrovascu lar acci-
perforat ing vessels, esp ecially at th e basilar apex–P1 com plex dents (th ree PCA, three MCA, one SCA), one stern otom y for a heart
an d at th e m idbasilar region feeding th e brain stem . How ever, n ot star t ing after arrest , an d m ult iple an esth esia-related com pli-
som e degree of vascu lar con t rol can be ach ieved w ith select ex- cat ion s. Th e overall p eriop erat ive m or t alit y rate w as 14%. An ad-
posu res. Using th e far-lateral app roach , tem porar y clip s can be dit ion al 18% of pat ien ts exp erien ced severe com plicat ion s for a
p laced on t h e bilateral ver tebral ar ter ies. Th e orbitozygom at ic com bin ed m orbidit y an d m or t alit y of 32% for th is p rocedu re. At
ap p roach can t h eoret ically p rovid e tot al vascu lar con t rol w h en a m ean of 9.7 years, 63% of th e pat ien ts w ere bet ter or th e sam e,
d ealing w it h an eu r ysm s of t h e basilar ap ex, bu t p lacem en t of 10% w ere w orse, an d 9% w ere dead; 18% w ere lost to follow -up.
m ultiple tem porar y clips can com plicate fin al clip placem en t by At last follow -up, th e an n ual h em orrh age rate after an eur ysm al
lim it ing th e access corridors. clip ping u n der hyp oth erm ic arrest w as 0.5%p er year. Th ese dat a
Th e im por t an ce of obt ain ing p roxim al an d dist al con t rol of led u s to con clude th at alth ough th e procedure is h igh ly effec-
an eur ysm blood flow can n ot be overst ressed. Alth ough in m ost t ive, it s u se sh ou ld be ju diciou s, given th e sign ifican t p oten t ial
instances adequate vascular control can be obtained by using tem - for com plicat ion s, an d rest ricted to pat ien t s w ith gian t posterior
porar y clips or add it ion al bon e rem oval (th e an terior an d poste- circulat ion an eur ysm s w h ere th e surgeon h as n o oth er opt ion
rior clin oid p rocess, for exam ple), in cer t ain sit u at ion s th e size for obtain ing vascular con t rol. Th e risks of in t raoperat ive ru p -
of th e an eur ysm precludes adequate visualizat ion of th e paren t t ure an d perforator st rokes du ring clipping of com plex posterior
vessel an d perforators. In an eur ysm s in th e posterior fossa th at circulat ion an eur ysm s are th e m ost im por t an t factors just ifying
are n ot am en able to en dovascular t reat m en t , w e advocate th e th e u se of th is tech n iqu e given cu rren t in n ovat ion s in en dovas-
select ive u se of hypoth erm ic circu lator y arrest to obt ain vascu lar cu lar tech n ique.
con t rol of t h e an eu r ysm . Given cu r ren t advan ces in en d ovascu -
lar tech n iques, w e n ow lim it th e use of cardiac st an dst ill to pa-
t ien ts w ith com p lex an d gian t basilar apex an eu r ysm s, especially
those w ith significant throm bus or calcification , a posteriorly pro-
ject ing an eur ysm dom e, or previou sly t reated an eur ysm s. W h en
■ Surgical Approaches
st an dst ill is u sed, barbit u rate cerebral protect ion an d protect ive Alth ough h istorically su rgeon s favored large an d, at t im es, de-
hypoth erm ia are in duced, th en cardiac arrest is in duced an d th e st r u ct ive su rgical ap proach es to t reat ing gian t an eu r ysm s, m ore
an eur ysm sac collapsed. Th e collapse of th e an eur ysm en ables recen tly th e pen dulu m h as sw ung tow ard th e use of sm aller cra-

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61 Giant Aneurysms 717
Fig. 61.2 Schem atic drawing showing a selec-
tion of surgical approaches to posterior circula-
tion giant aneurysm s. Aneurysms of the upper
third of the basilar artery (purple) are t ypically
exposed via an extended orbitozygom atic ap-
proach, aneurysms of the middle third (dark blue)
via one of several transpetrosal approaches, and
aneurysm s of the lower third (teal) of the basilar
artery and intradural vertebral arteries via a far-
lateral approach. (Courtesy of Barrow Neurologi-
cal Institute.)

n iotom ies th at expose th e n ecessar y an atom y w ith ou t dest roy- Orbitozygomatic-Pterional Approach
ing th e sku ll base. Properly p laced cran iotom ies provide m axi-
The pterional transsylvian approach is one of the m ost com m only
m al exposure w ith m in im al brain ret ract ion , w h ich h elps protect
u sed approach es to an terior circulat ion an eu r ysm s. Alth ough
th e pat ien t from inju r y. At ou r in st it ut ion , w e rarely use brain
th is app roach p rovides access to th e circle of Willis, visu alizat ion
ret ractors an d d ep en d in stead on dyn am ic ret ract ion to gain ac-
can be im p roved by th e add it ion of orbit al an d zygom at ic oste-
cess to th e depth s of th e subarach n oid space.52 With adequate
otom ies.59,68 We advocate th e use of OZ osteotom ies in t reat ing
visualizat ion of th e an atom y, dyn am ic ret ract ion, an d con t rolled
giant aneur ysm s, because the osteotom ies im prove working space
applicat ion of an an eur ysm clip of appropriate length an d sh ape,
at a sh allow er d epth an d low er t rajector y to th e sku ll base, w h ile
th e an eu r ysm n eck can be obliterated an d th e paren t vessels an d
m in im izing brain ret ract ion (Fig. 61.3).58 We rout in ely use th e
all perforators preser ved.
OZ approach in t reat ing an eur ysm s of th e an terior circulat ion ,
Yaşargil et al53 ch am pion ed th e pterion al ap p roach for an eu -
basilar apex, PCA, an d SCA.57 In cases w h ere a deep bypass su ch
r ysm s of th e an terior circu lat ion an d basilar bifurcat ion . Drake 54
as su p er ficial tem p oral ar ter y (STA)-to-SCA or STA-to-PCA is
used a subtem poral-transtentorial approach for aneurysm s of the
p lan n ed , t h e su btem p oral var iat ion of t h e OZ cran iotom y is es-
p oster ior circu lat ion . Ot h ers h ave u sed su boccip it al, t ran soral,
sen t ial for adequ ate exp osu re.58 Th e exp osu re provided by th e
an d t ran sm a xillar y-t ran sclival ap p roach es for p oster ior circu -
OZ approach can be im proved by drilling th e an terior clin oid
lat ion an eur ysm s.55,56 Alth ough each of th e aforem en t ion ed ap -
process. Th e OZ ap p roach is also u sefu l w ith h igh -riding gian t
proach es h as it s lim itat ion s, th ey are u sefu l in select cases. At ou r
an eur ysm s of th e basilar ar ter y becau se it exposes th e upper in -
in st it ut ion , pat ien ts w ith an terior circu lat ion an eur ysm s are
terpedun cular space.
t reated u sing th e orbitozygom at ic (OZ) or th e in terh em isph eric
approach . As for an eur ysm s of th e posterior circulat ion , w e di-
vide our app roach to th e basilar ar ter y in to th ree dom ain s (Fig. Patient Positioning
61.2). For an eu r ysm s at th e top th ird of th e basilar ar ter y, w e Th e pat ien t is posit ion ed su p in e on th e su rgical t able. Th e pa-
advocate th e OZ approach .57 Both th e t w o-piece an d th e on e- t ien t’s h ead is rotated 30 to 90 degrees to th e con t ralateral side
piece app roach es w ith t ran szygom at ic m odificat ion s of th e OZ w ith th e n eck exten ded to p lace th e m alar em in en ce at th e apex
approach (w ith fur th er extension provided by drilling of th e cli- of th e surgical field. Th is allow s th e fron tal lobe to fall back from
vus) adequ ately exp ose th is area of th e basilar arter y, an d th e th e sku ll base. Th e p at ien t’s h ead is p laced in a Mayfield clam p
approach can also be used for an eur ysm s of th e PCA an d SCA an d fixed to th e su rgical table.
(Fig. 61.3).58,59 Th e m idd le th ird of th e basilar ar ter y is reach ed
using on e of several t ran spet rou s app roach es (Figs. 61.4, 61.5,
Skin Incision
61.6, 61.7).60–64 Th e low er th ird of th e basilar ar ter y is accessed
using su boccipital, ret rosigm oid (Fig. 61.8), or far-lateral cran i- Th e skin in cision u sed is sim ilar to th e pterion al in cision . It be-
otom ies (Fig. 61.9) an d m odificat ion s th ereof (Fig. 61.10).65–67 gin s 1 cm an terior to th e t ragus at th e root of th e zygom at ic arch .
Su rgical ap proach es u sed at ou r in st it u t ion are described in de- Th e in cision is exten ded p ast t h e m idlin e to th e con t ralateral
tail in th e follow ing su bsect ion s. m idpupillar y lin e. During th e scalp in cision , th e posterior bran ch
(text cont inues on page 726)

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a b

c d

Fig. 61.3a–e Schem atic drawings showing orbitozygom atic approaches.


(a) The t wo-piece orbitozygom atic approach uses a pterional craniotomy
and rem oves the orbitozygomatic unit as a single piece. Osteotom ies nec-
essary to perform this approach include those across the root of zygom a,
across the m alar eminence to the inferior orbital fissure, through the orbital
roof lateral to the supraorbital nerve, across the posterior orbit and pterion,
and down to the inferior orbital fissure. (b) The view of the m idbasilar ar-
tery is obstructed by the anterior and posterior clinoid processes and the
dorsum sellae (pink and orange highlights); these structures can be drilled
away to provide a view down to the m idbasilar artery (c). (d) Additional
inferior exposure of the basilar artery enables the aneurysm al neck to be
dissected and defined (arrow), working along the artery axis; this also en-
ables an additional site of vascular control. (e) View from an orbitozygo-
m atic approach upon opening of the carotid, lam ina term inalis, and sylvian
cisterns. This approach allows three routes of access to the basilar apex.
The opticocarotid triangle (green arrow) is used when the carotid artery is
separated from the optic nerve. The orange arrow designates the opening
bet ween the optic tract and A1-M1 interval. The blue arrow designates the
carotid-oculom otor triangle. ACA, anterior cerebral artery; CN, cranial
e nerve; ICA, internal carotid artery; MCA, m iddle cerebral artery; PCA, pos-
terior cerebral artery; PCoA, posterior com m unicating artery; SCA, supe-
rior cerebellar artery. (Courtesy of Barrow Neurological Institute.)

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61 Giant Aneurysms 719
Fig. 61.4 The three t ypes of presigm oid transpetrosal
approaches are highlighted. The retrolabyrinthine ap-
proach (dark blue area) preserves the sem icircular canals
and cochlea but provides limited exposure anteriorly where
the neck of a m idbasilar aneurysm is located, frequently
rendering this approach ineffective. Alternatively, a trans-
labyrinthine (light blue area) or a transcochlear (green area)
approach is indicated despite the sacrifice of hearing and
the risk to facial nerve function. (Courtesy of Barrow Neu-
rological Institute.)

a b

Fig. 61.5a,b Schem atic drawings dem onstrating exposure obtained via a This provides a lim ited working space bet ween the sinus and the otic cap-
retrolabyrinthine approach. (a) The initial procedure involves an extended sule. CN V, trigeminal nerve; CN IX, glossopharyngeal nerve; CN X, vagus
m astoidectomy, skeletonizing the facial nerve (CN VII), sem icircular ca- nerve. (a, modified from Zubay G, Porter RW, Spet zler RF. Transpetrosal
nals, and the sigm oid sinus. (b) Next, the dura is opened in the presig- approaches. Operative Tech 2001;4:24–29. Used with perm ission from El-
m oid space, exposing the vestibulocochlear (CN VIII) and facial nerves. sevier. b, courtesy of Barrow Neurological Institute.)

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720 V Cerebral and Spinal Aneurysms

a b

Fig. 61.6a–c Schem atic drawings dem onstrating exposure obtained via a
translabyrinthine approach. (a) Upon reaching the sem icircular canals, the
internal auditory canal is skeletonized and the facial nerve is traced out to
its genu (b). (c) Opening of the dura allows visualization of the subarach-
noid space and intracanalicular and vertical portions of the facial nerve.
AICA, anterior inferior cerebellar artery; CN V, trigeminal nerve; CN VII, facial
nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; L, left. (Modified
from Zubay G, Porter RW, Spet zler RF. Transpetrosal approaches. Operative
c Tech 2001;4:24–29, 2001. Used with perm ission from Elsevier.)

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61 Giant Aneurysms 721
Fig. 61.7 Schem atic drawing dem onstrating exposure obtained via a
transcochlear approach after skeletonization of the facial nerve (CN VII).
The facial nerve can be transposed once the superficial petrosal and
chorda t ympani nerves are sectioned. ICA, internal carotid artery.
(Courtesy of Barrow Neurological Institute.)

Fig. 61.8 Schematic drawing dem onstrating the retro-


sigm oid craniotomy with exposure of the sigm oid sinus.
The placem ent of the craniotomy close to the sinus en-
ables retraction of the sinus, providing a greater degree
of exposure into the cerebellopontine angle. (Courtesy of
Barrow Neurological Institute.)

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Fig. 61.9a–g Schematic drawings of the far-lateral exposure. (a) The
vertebral artery (VA) is depicted at its horizontal portion as it pierces
the dura. Bet ween C1 and C2 the VA is under the root of C2. During
surgery, this landm ark can be used to localize the artery. (b) Once
the posterior arch of C1 is rem oved, the VA is exposed. Alternatively
the foram en transversarium of C1 can be drilled with a diam ond bit
to provide m ore room . The VA is mobilized to provide access to the
occipito–C1 joint. (c) In the far-lateral retrocondylar approach, the VA
is exposed from the occipital condyle to the point of piercing the
dura. (d) The VA is protected while the condylar drilling is taking place.
The drilling of the condyle exposes the cortical bone first, the cancel-
lous bone next, and finally the cortical bone again as one approaches
the hypoglossal canal.

c d

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61 Giant Aneurysms 723

Fig. 61.9a–g (continued ) (e) Extensive drilling of


the occipital condyle leads to the extradural expo-
sure of the jugular tubercle. (f) The surgical expo-
sure once the dura is opened. (g ) Magnified view
of part f dem onstrates that the posterior inferior
cerebellar artery (PICA) can be followed as it emerges
from the VA to its tonsillar segm ent. Note the prox-
imit y of the spinal accessory nerve (CN XI) to the
dura m at ter. CN XII, hypoglossal nerve; CN IX, glos-
sopharyngeal nerve; CN X, vagus nerve; PCEV, pos-
terior condylar emissary vein. (Modified from Baldwin
HZ, Miller CG, van Loveren HR, Keler JT, Daspit CP,
Spet zler RF. The far lateral/combined supra- and in-
fratentorial approach: a human cadaveric prosection
model for routes of access to the petroclival region
and ventral brain stem. J Neurosurg 1994;81:60–68.
Used with permission from the American Association
g of Neurological Surgeons.)

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724 V Cerebral and Spinal Aneurysms

Fig. 61.10a–h Schem atic drawings of the com bined approaches to the
posterior fossa. (a) The skin incision extends from the pinna to below the
foram en m agnum . This enables both a subtemporal exposure and a far-
lateral exposure. (b) Careful param edian m uscle-split ting dissection pro-
vides exposure of the far-lateral component without risking injury to the
vertebral artery. (c) A subtemporal craniotomy (dashed line) can be per-
form ed as a part of this procedure or as a stand-alone exposure. The dura
over the exposed transverse and sigm oid sinuses m ay be opened in one of
several ways.

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61 Giant Aneurysms 725
Fig. 61.10a–h (continued ) (d) Opening over the presigm oid dura (dashed
line) allows visualization of the anatomy with m inim al retraction of the cer-
ebellar hem isphere. (e) Simultaneous cuts in the retrosigmoid dura can be
perform ed to expose down to the foram en m agnum . (f) The sigm oid sinus
can be divided (extended dashed line) to provide greater exposure. (g) The
exposure of the contents of the posterior fossa obtained after a com bined
exposure. Movem ent of the operating m icroscope and retraction of the
sinus (g) posteriorly or (h) anteriorly provides a wide surgical exposure for
perform ing the operation. AICA, anterior inferior cerebellar artery; CN III,
oculom otor nerve; CN IV, trochlear nerve; CN V, trigem inal nerve; CN VII,
facial nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XI, spi-
nal accessory nerve; CN XII, hypoglossal nerve; PICA, posterior inferior cer-
ebellar artery; SCA, superior cerebellar artery. (a–c,g,h, courtesy of Barrow
Neurological Institute. d-f, modified from Baldwin HZ, Miller CG, van Lov-
eren HR, Keler JT, Daspit CP, Spet zler RF. The far lateral/com bined supra-
and infratentorial approach: a human cadaveric prosection model for routes
of access to the petroclival region and ventral brain stem . J Neurosurg
1994;81:60–68. Used with perm ission from the Am erican Association of
Neurological Surgeons.)

e f

g h

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726 V Cerebral and Spinal Aneurysms

of th e superficial tem poral ar ter y sh ould be preser ved in case a praorbital osteotom y, the m alar em inence and zygom atic root are
bypass is n eeded. Th e scalp flap is elevated an teriorly from th e n ot exposed. Th e dissect ion sh ould be don e using a “cold” tech -
su p erficial tem p oralis fascia. Exten sive exp osu re of th e su bgaleal n iqu e an d sh arp dissect ion , because elect rocauter y can lead to
fat pad in th e pterion al region sh ould be avoided to preven t in - at rophy of th e tem p oralis m u scle du e to dam age to it s in n er va-
jur y to th e fron talis bran ch of th e facial n er ve. Both su bfascial or t ion . Next , th e fron tozygom at ic su t u re is exposed an d th e perior-
m yofascial dissections can be perform ed to preserve the nerve.69,70 bita is freed along th e supralateral orbit . If a m ore m edial orbi-
totom y is n eeded, th e supraorbital n er ve can be m obilized from
its foram in al n otch an d ret racted w ith th e scalp. Th e periorbit a
Craniotomy and Opening
is dissected using a blu n t probe, su ch as a Pen field No. 1, sw eep -
Du ring th e cran iotom y, care m u st be taken to avoid th e fron tal ing from th e in ferior orbit al fissu re laterally to th e supraorbit al
sin u s, an d , if t h e sin u s is violated , it m u st be rep aired . Th e su b - n otch m edially. How ever, rough m an ipu lat ion of th e periorbita
galeal fat pad is exposed an d the tem poralis m uscle, its fascia, and can lead to in creased sw elling an d h igh er risk of en oph th alm os.
its p eriosteal flaps are elevated togeth er w ith th e scalp. A fascial Th e su p raorbit al m od ified OZ cran iotom y (Figs. 61.3 an d
cuff can be left for reapproxim at ion of th e tem poralis m u scle.71 61.11) can be perform ed using a one- or t w o-piece m ethod; both
In th e m odified OZ ap proach con sist ing p red om in an tly of a su- h ave been applied to obt ain th e full exp osu re.58,59

a b

Fig. 61.11a–c A 47-year-old wom an with a history of a coiled basilar apex


aneurysm was noted to have a recurrence on follow-up imaging. (a) Antero-
posterior vertebral artery angiogram dem onstrates a giant basilar apex an-
eurysm . The patient was taken to the operating room for possible clipping
versus basilar occlusion and superficial temporal artery (STA)-to-superior
cerebellar artery (SCA) bypass. The lesion was approached via a one-piece
orbitozygom atic craniotomy. (b) Intraoperative photograph dem onstrates
the coils within the aneurysm dom e. The aneurysm was prim arily clipped.
(c) Anteroposterior postoperative angiogram dem onstrates obliteration of
the aneurysm without evidence of a residual. (Courtesy of Barrow Neuro-
c logical Institute.)

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61 Giant Aneurysms 727

Tw o -Piece Method lateral to th e fron tozygom at ic su t u re, back tow ard th e bur h ole
at th e an atom ic keyh ole. An osteotom e can be u sed to com p lete
A pterion al cran iotom y is perform ed in th e u sual fash ion . Th e
th e cran iotom y as n eeded.
size of th e pterion al cran iotom y is dep en den t on th e n eed for
Th e flap m ust be elevated from th e dura in a m ed ial to lateral
exp osu re. Next , th e du ra is freed from th e floor of th e an terior
direct ion to preven t driving th e orbital roof in to th e fron tal lobe.
fossa an d th e sph en oid ridge. Malleable ret ractors can be used to
W h en com bin ed w ith resect ion of th e an ter ior an d p oster ior
protect th e brain an d orbital con ten ts du ring th e osteotom ies.
clin oid p rocesses an d clival resect ion , th e fu ll orbitozygom at ic
Th ese osteotom ies are perform ed w ith th ree cu t s. Th e first cu t
approach can expose lesion s dow n to th e m iddle of th e basilar
begin s lateral to th e sup raorbit al n otch at th e m edial edge of th e
ar ter y.
pterion al cran iotom y, exten d ing p erpen dicu lar from th e orbital
rim to th e orbit al roof. Th e secon d cu t begin s from th e p osterior
asp ect of t h e first cu t , p er p en d icu lar tow ard t h e su p er ior or- Closure
bit al fissu re. Th e orbitotom y can be com p leted w ith rongeu rs.
Th e last cut is m ade from th e orbital rim , ju st lateral to th e fron - If th e sin us w as en tered, th en it sh ould be repaired. Th e du ra
tozygom at ic su t ure, tow ard th e superior orbit al fissu re, again in m ust be closed in a w atert igh t fash ion to preven t CSF leaks. Th e
a perpen dicular fash ion . A h an d-h eld osteotom e can be used to cran iotom y can be repaired using plates. Th e m yofascial tem po-
com p lete th e cu t s. Next , th e du ra is op en ed w ith an in feriorly ralis flap is reapproxim ated to th e cuff th at w as left adh eren t to
based flap . Du ral su t u res are p laced m ore deep ly over t h e m e- th e bon e, an d th e scalp is closed in layers.
d ial surface of th e flap to gen tly ret ract th e periorbital con ten ts Risks associated w ith th e exten sive bony rem oval of th e OZ
in fer iorly an d laterally, p rovid ing an ad d it ion al cen t im eter of ap p roach in clu d e p er iorbit al sw elling an d br u isin g, p u lsat ile
exp osu re. en op h th alm os, orbit al en t rap m en t , blin dn ess, inju r y to th e facial
n er ve, diplopia, tem poral w ast ing, difficult y w ith ch ew ing, an d
oth er cosm et ic defect s. Th e ben efit s gain ed from th is exposure,
One -Piece Method h ow ever, w arran t it s use, especially in t reat ing com plex lesion s
Th e on e-p iece m eth od is rarely u sed . Th is cran iotom y com bin es such as gian t an eur ysm s.
th e pterion al cran iotom y an d orbitotom y in to a single flap . Th e
pterion al cran iotom y is p erform ed in th e u su al fash ion , an d
drilling stop s at th e orbital rim ju st lateral to th e su praorbital
Interhemispheric Approach
n otch an d again at th e pterion from below. Th is m an euver leaves Alth ough proxim al ACA an d ACoA an eur ysm s can be effect ively
a sm all r idge of bon e bet w een th e su p ralateral orbit al r im an d t reated u sing an OZ ap p roach , access to th e distal ACA territor y is
t h e pter ion al bon e flap . Th e orbitotom y cu t s are m ad e from enhanced by using an interhem ispheric approach (Fig. 61.12).72–74
w ith in th e orbit using a reciprocat ing saw. Th e t w o cut s n eeded A bifron t al in terh em isp h eric ap proach can be cou pled w ith an
to com plete th e cran iotom y in clu de a cu t th rough th e orbital rim OZ craniotom y as needed to provide proxim al control from below
just lateral to th e su praorbital n otch con n ect ing to th e pterion al an d good visualizat ion of dist al ACA lesion s from above, th us en -
cran iotom y. Th e secon d cu t proceeds over th e orbital rim , ju st abling clipping of distal lesion s.

a b

Fig. 61.12a,b (a) Schem atic diagram of the skin incision and craniotomy for an interhem ispheric approach. (b) Dissection in the interhem ispheric fissure
leads the surgeon to the bilateral anterior cerebral arteries. (Courtesy of Barrow Neurological Institute.)

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728 V Cerebral and Spinal Aneurysms

Patient Positioning m aking it n ecessar y to open th e callosal cistern to gain access to


th e dist al ACA.
Th e p at ien t is p laced su p in e on th e su rgical t able. Th e p at ien t’s
h ead is secured in a Mayfield th ree-pin h ead h older an d at tach ed
to th e bed. Th e h ead can be sligh tly flexed. Closure
Th e du ra is closed u sing a 4-0 su t u re, an d th e cran iotom y is re-
Skin Incision paired in th e u su al fash ion . Th e skin is closed in a m u lt ilayered
fash ion .
A bifron t al or “t rapdoor” skin in cision is used to expose th e skull.
In cases w h ere a possible pterion al or OZ approach m ay be com -
bin ed w ith th e in terh em isph eric approach , th e OZ skin in cision Subtemporal Approach
is exten ded to th e con t ralateral m idpu p illar y lin e.
Drake ch am pion ed th e use of th e subtem poral cran iotom y for
access to th e basilar ar ter y. Variat ion s of th is approach , in cluding
Craniotomy and Opening com bin at ion s w ith t h e t ran ssylvian pterion al ap p roach , called
Th e cran iotom y is p lan n ed to cross t h e su p erior sagit t al sin u s. the tem poropolar, half-and-half, or on e-and-a-half approach, and
We prefer to p lace th e bu r h ole over th e sin u s. Using th is tech - th e an terior t ran sp et rosal ap proach h ave been described . Th e
n ique, th e sin us can be st ripped off of th e skull an d th e cran iot- su btem poral ap p roach can be select ively u sed to gain access to
om y can be p er for m ed, kn ow in g t h at t h e sin u s is p rotected by u pper basilar or basilar bifu rcat ion an eu r ysm s th at project pos-
t h e foot p late. Next t h e d u ra is op en ed an d u sed to ret ract t h e teriorly (Fig. 61.14). Th e su btem p oral ap p roach can be com bin ed
sin u s. Th is p rovides an add it ion al layer of p rotect ion of th e sin u s w ith any of th e t ran spet rosal approach es to gain access to th e
in case an in st ru m en t in adverten tly slips, w h ich w ould injure en t ire length of th e basilar ar ter y. How ever, w e h ave aban don ed
th e sin u s. the use of th is approach for giant aneur ysm s due to the possibilit y
of injur y to th e vein of Labbé during th e approach an d ret ract ion
of th e tem poral lobe.
Intradural Exposure
Usin g t h e su rgical m icroscop e for gu idan ce, t h e in terh em i-
Transpetrosal Approaches
sp h eric fissure is open ed an d dissect ion is con t in ued bet w een
th e falx an d th e fron t al lobe. Dissect ion is con t in u ed u n t il th e Th e an terior brain stem an d clivu s can be accessed by graded re-
ACA is iden t ified an d th e path ology is visualized (Fig. 61.13). At m oval of th e pet rou s bon e (Fig. 61.4). Th ree m ain t ran spet rous
th e level of th e cingu late, sign ifican t adh esion s m ay be p resen t , ap proach es (w ith variable bony rem oval an d m orbidit y profiles)

a b

Fig. 61.13a–e A 38-year-old woman with a fusiform right anterior cere- hem ispheric craniotomy. The inflow artery to the fusiform aneurysm was
bral artery aneurysm. (a) Sagit tal computed tomographic angiography (CTA) clipped proximally and a side-to-side A3–A3 bypass was perform ed to re-
and (b) coronal three-dim ensional (3D) reconstruction depicts the fusi- vascularize the distal territory.
form nature of the aneurysm . The aneurysm was approached via an inter-

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61 Giant Aneurysms 729

Fig . 61.13a– e (continued ) (c) A sagit t al CTA depict s the placem ent of
the clip proxim al to the fusiform segm ent of the aneurysm . (d) Anterior-
posterior and (e) lateral postoperative angiograms demonstrate obliteration
of the aneurysm and back-filling of the distal anterior cerebral artery via the
A3–A3 bypass from the left side. (Courtesy of Barrow Neurological Institute.) e

Fig. 61.14 Schematic drawing of the subtemporal ap-


proach and the exposure offered. The temporal lobe is
retracted exposing the basilar artery and the perforators
arising from the P1. a, artery; n, nerve. (Courtesy of Barrow
Neurological Institute.)

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730 V Cerebral and Spinal Aneurysms

can be u sed to gain access to t h e m id d le an d low er t h ird of t h e sible, if th e surgeon requires a w ider exp osu re of th e in ferior as-
basilar ar ter y: (1) Th e exten d ed ret rolabyrin t h in e tech n iqu e pect of th e clivu s. Th e p osterior extern al au ditor y can al an d th e
involves lim ited pet rous bon e resect ion w ith preser vat ion of bon e overlying th e m astoid segm en t of th e facial n er ve sh ould be
h earing. (2) Th e t ran slabyrin th in e tech n iqu e involves aggressive th in n ed to m in im ize th is obst ru ct ion to visu alizing th e clivu s.
p et rou s bon e resect ion an d sacr ifice of h ear ing. (3) Th e t ran s- Th e dist al en d of th e su perior vest ibu lar n er ve in th e vest ibu le is
coch lear tech n iqu e involves m a xim u m p et rou s bon e resect ion , u sed as a referen ce for easy iden t ificat ion of th e facial n er ve, be-
sacrifice of h earing, an d t ran sp osit ion of th e facial n er ve. Moving cau se it exit s th e in tern al au ditor y can al. Th e bon e overlying th e
th rough th ese th ree variat ion s of su rgical exposu re p rovides a labyrin th in e segm en t of th e facial n er ve is also th in n ed w ith care
gradu ated in crease in th e am ou n t of pet rou s bon e resect ion . As u sing a d iam on d bit an d con t in u ou s in t raoperat ive m on itoring
exp osu re of th e brain stem an d clivu s in creases, th e likelih ood of facial n er ve fun ct ion .
an d p oten t ial for m orbidit y also in creases; p oten t ial m orbidit ies
include loss of hearing, injury to the facial nerve, and an increased Transcochlear Technique
in ciden ce of CSF leaks.
For m axim um exposure of the clivus, the anterior brainstem , and
th e m idbasilar region , th e t ran scoch lear tech n iqu e is u sed (Figs.
Patient Positioning
61.7 an d 61.15).75,76 How ever, th is vast exposure is provided at
Th e pat ien t is p osit ion ed su p in e on th e operat ing t able, w ith th e th e exp en se of h earing an d w ith an in creased risk of facial n er ve
h ead parallel to th e floor an d fixed to th e operat ing table in a paresis or paralysis. Th e extern al au ditor y can al is t ran sected
Mayfield th ree-pin h ead h older. A soft roll is p laced u n d er th e an d oversew n in t w o layers. After th e t ran slabyrin th in e expo-
ipsilateral shoulder to provide appropriate elevation and support. su re, th e greater su perficial p et rosal n er ve is sect ion ed, an d th e
facial n er ve is t ran sposed p osteriorly, u sing th e du ra of th e in ter-
Skin Incision and Petrosal Drilling n al auditor y can al to protect par t of th e n er ve. Th e en t ire t ym -
p an ic p or t ion of t h e tem p oral bon e is rem oved w it h exp osu re
The skin incision begins 3 cm posterior to the pinna and continues of th e periosteum of th e tem porom an dibular join t . Th e in tern al
in a gen tle cur ving fash ion aroun d th e ear to th e in ferior border auditor y can al an d coch lea are th en rem oved. Exposure of th e
of th e m astoid. Th is represen ts th e posterior par t of th e in cision jugular bulb is accom plish ed by rem oving th e bon e th at sepa-
u sed for t h e com bin ed ap proach . Th e ear is ret racted in feriorly rates it from th e ICA at th e skull base. Th e close relat ion sh ip of
w ith fish h ooks th at are at tach ed to a Leyla bar. Th is m an euver cran ial n er ves IX, X, an d XI m u st be con sidered, an d injur y to
exp oses par t of th e tem poral squam a, extern al au ditor y m eat u s, th ese n eu ral st ru ct ures m u st be avoid ed . Th e bon e su rrou n ding
an d m astoid region . Th e n eu ro-otologist perform s th is approach th e ICA is rem oved u p to th e sip h on . If direct exp osu re of th e ICA
th rough th e tem poral (pet rou s) bon e an d exp oses t h e sigm oid is u n n ecessar y, a th in rim of bon e can be left to en case th e vessel.
sin u s an d du ra, exten ding 1 to 2 cm p osterior to th e sin u s; th e Bon e is also rem oved from th e floor of th e plate of th e m iddle
n eu rosurgeon th en perform s th e in t radural par t of th e proce- fossa dow n to th e h orizon t al segm en t of th e ICA.
dure. The m astoidectom y portion of the tem poral bone procedure
is com pleted w ith a h igh -speed drill. Suct ion irrigat ion is u sed
Intradural Exposure
con t in uou sly du ring drilling of th e tem poral bon e.
Th e du ra m ater is in cised ju st in ferior an d p arallel to th e su p e-
Extended Retrolabyrinthine Technique rior p et rosal sin u s an d ju st su p erior to th e jugu lar bu lb. Th ese
t w o d u ral in cision s m eet at t h e sin od u ral angle an d t h e p et rou s
Th e exten ded ret rolabyrin th in e app roach p reser ves h earing. Th e acu st icu s. Th e du ra m ater of t h e in ter n al au d itor y can al is
posterior an d su perior sem icircu lar can als are skeleton ized both open ed an d th e cerebellopon t in e angle is exposed for subarach -
above an d below th e ot ic capsule, to expose as m uch dura as pos- n oid dissect ion .
sible. Th e bon e overlying th e su p erior p et rosal sin u s is rem oved
w ith the drill, and the endolym phatic sac and duct are preserved.
Closure
Th e ret rolabyrin t h in e ap proach p rovid es access to th e cere-
bellopon t in e angle, but does n ot en able sign ifican t an terior visu - Closure of th e su rgical field is accom plish ed in an atom ic layers
alizat ion of th e brain stem (Fig. 61.5). It th erefore h as a lim ited w h en possible. Th e dura is reapproxim ated w ith 4-0 braided
role in th e m an agem en t of an eur ysm s of th e vertebrobasilar nylon sut ure w h ere possible. Abdom in al adipose t issue, tem po-
t ru n k w h en u sed in isolat ion , bu t it does p rovide a lateral view to ralis m uscle, fascia lat a, an d fibrin glue are used to obliterate th e
th e basilar ap ex. eu st ach ian t u be (in th e t ran slabyrin th in e an d t ran scoch lear ap -
proach es) an d th e void created by tem p oral bon e resect ion . In
th e lat ter sit u at ion , th e fat is carefu lly packed in th e du ral ren t
Translabyrinthine Technique
th at rem ain s to t am pon ade th e defect an d to preven t CSF leak-
If greater exposure is required, th e t ran slabyrin th in e approach age. We favor lu m bar sp in al drain age of CSF (over 1–5 days) to
can be u sed. Th e t ran slabyrin th in e ap proach sacrifices h earing, aid in t issue h ealing an d preven t CSF leaks.
but th e addit ion al space gain ed by rem oval of th e sem icircular
can als an d skeleton izat ion of th e p osterior h alf of th e in tern al
auditor y can al provides a larger view of th e an terior brain stem
Combined Approaches
an d cerebellopon t in e angle, w h ich is n ecessar y to access gian t Th e exp osu re of th e ver tebrobasilar ar ter y p rovided by th e t ran s-
m idbasilar arter y an eur ysm s (Fig. 61.6). Rem oval of all of th e petrosal approaches can be dram atically enhanced w hen com bined
bon e overlying th e sigm oid sin u s an d th e jugular bulb is pos- w ith a supraten torial approach such as th e OZ or sub tem poral

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61 Giant Aneurysms 731

a b

Fig. 61.15a–c Transpetrosal approaches to giant aneurysm s. Transpetro-


sal approaches are rarely needed but when used they provide improved
access to the anterior m idbasilar zone with m inim al need for brain retrac-
tion. This 51-year-old m an presented with diplopia and headache. (a) Lat-
eral vertebral artery angiogram and (b) three-dim ensional reconstruction
of the vertebral artery angiogram dem onstrate a giant midbasilar aneu-
rysm . The patient underwent a transcochlear approach for direct clipping
of the aneurysm . (c) Postoperative lateral angiogram dem onstrates oblit-
eration of the aneurysm and the result was durable at the 3-year follow-up.
c (Courtesy of Barrow Neurological Institute.)

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732 V Cerebral and Spinal Aneurysms

craniotom y (Fig. 61.10).76,77 The use of these com bined techniques m ust be elevated w ith great care to protect th e vein of Labbé,
is n ow rarely in dicated, bu t th ese approach es can be select ively w h ich is in directly teth ered to th e skull base via th e sigm oid
used to access lesion s exten ding from th e sph en oid ridge an d sin u s. Th e vein of Labbé can be m obilized by dissect ing it from
cavern ou s sin u s to th e foram en m agn u m an d an terior cer vical th e cor t ical su rface to m in im ize ten sion on th e vessel. Th ese fin al
spin al cord. An im por tan t variable in th e com bin ed approach is m an euvers expose th e ipsilateral pet rous region , clivus, brain -
th e im p or t an ce an d fate of both th e du ral sin u ses (su p erior p e- stem , cran ial n er ves, an d th e m ajor ar terial vessels of th e brain -
t rosal, sigm oid, or t ran sverse sin us) an d th e vein of Labbé. Som e stem . With m icroscop ic su rgical tech n iqu es, an eu r ysm s in th e
auth ors advocate preser vat ion of th e m ajor dural sin us, w h ereas posterior circu lat ion can th en be readily addressed.
oth ers, in th e set t ing of paten t con t ralateral ven ou s circulat ion ,
advocate sacrifice of the sigm oid or transverse sinus to gain added
Closure
exp osu re.
Closure of th e su rgical field is accom plish ed in an atom ic layers
w h en possible. Th e tem poral an d occipit al dura is reapproxi-
Patient Positioning
m ated w ith 4-0 braided nylon su t u re. Abdom in al adipose t issu e,
Th e p at ien t is p osit ion ed su p in e, w it h t h e h ead p osit ion ed p ar- tem poralis m uscle, fascia lata, an d fibrin glue are used to obliter-
allel to th e floor an d fixed to th e operat ing t able in a Mayfield ate th e eu stach ian t u be (in th e t ran slabyrin th in e app roach ) an d
th ree-p in h ead h older. A soft roll is p laced u n der th e ip silateral th e void created by tem p oral bon e resect ion . In th e lat ter sit u a-
sh ou lder to p rovide app ropriate sup port . t ion , th e fat is carefu lly packed in th e du ral ren t th at frequ en tly
rem ain s to t am pon ade th e defect an d to p reven t CSF leakage. We
advocate th e use of a lum bar drain age system for 1 to 5 days to
Incision
en able t issue h ealing an d reduce th e risk of CSF leakage.
Th e skin in cision begin s at th e level of t h e zygom a, 1 cm an terior Th e com bin ed su p ra- an d in fraten torial ap proach , w ith it s
to th e ear, an d con t in u es in a gen tle cur ving fash ion posteriorly differen t variat ion s, p erm it s exqu isite su rgical exposu re w h en
aroun d th e ear to en d just below th e m astoid t ip. To obt ain in - dealing w ith m ost aneur ysm s involving the vertebrobasilar trunk.
creased exposure, th e posterior par t of th e in cision m ay be ex- Th ese ap p roach es p erm it th e su rgeon to deal w ith th ese lesion s
ten ded fu r th er posteriorly. To obtain m axim u m exposure th at safely an d ad equ ately, w it h m in im al brain ret ract ion , m akin g
in clu des th e foram en m agn u m , th e com bin ed app roach can be t h ese tech n iqu es p ar t icu larly su it able for t reat in g gian t an eu -
fu r th er com bin ed w ith th e far-lateral su boccipit al ap proach . Th e r ysm s in th is region .
scalp flap is ret racted in feriorly w ith fish h ooks at t ach ed to a
Leyla bar. Th is m an euver exposes th e lateral aspect of th e skull:
zygom a, lateral tem poral bon e, extern al auditor y m eat us, an d
Far-Lateral Approach
m astoid region . Th e far-lateral ap p roach (Fig. 61.9) to t h e in fer ior clivu s an d
u p p er cer vical region is a tech n ical m od ificat ion of t h e su boc-
cipital approach . Th e far-lateral approach en h an ces exposure to
Craniotomy and Dural Opening
th e in ferior brain stem an d u p p er sp in e, p roviding su rgical access
After the neuro-otologist has fin ish ed the petrous bone resection, to lesion s involving th e low er basilar ar ter y, th e ver tebrobasilar
th e n eu rosu rgeon p roceeds w ith a su btem p oral-su boccip it al system , an d th e cran iover tebral jun ct ion .
cran iotom y th at crosses th e t ran sverse sin us an d th ereby ex- Th e en h an ced exposu re p rovided by th e far-lateral ap p roach
poses th e rem ain der of th e sigm oid sin u s. Th is exposes a large is accom plish ed via a lateral su boccipit al cran iotom y coupled
du ral su rface. Th e an terior p ar t of th e du ral in cision is m ad e over w ith th e rem oval of th e m edial h alf of th e occipital con dyle an d
th e tem p oral lobe an d exten ds p osteriorly at least 1 cm below th e p osterolateral arch of C1 (dow n to t h e su lcu s ar teriosu s of
w h ere th e superior petrosal sin us enters the sigm oid sinus. Rarely, th e ver tebral arter y). Occasion ally, a m ore exten sive lateral ex-
a low -lying vein of Labbé is foun d adh eren t to th e tem poral dura posu re of th e clivu s is requ ired to deal w ith gian t an eu r ysm s in -
or ten torium an d m ust be preser ved. If th e sigm oid sin us is to be volving th e m idbasilar or low er basilar ar ter y. Th is exposu re can
preser ved, th e du ral in cision crosses th e su perior pet rosal sin u s be ach ieved by com bin ing th e far-lateral approach w ith eith er an
to join w ith a du ral in cision in fron t of th e sigm oid sin us. Alter- isolated t ran spet rosal or th e com bin ed su pra- an d in fraten torial
n at ively, th is sin us can be sacrificed w h en th e con t ralateral sin u s approach . Th is “com bin ed–com bin ed” approach can provide a
is paten t . Th e su perior p et rosal sin u s can u su ally be cau terized w ide, flat route to th e en t ire length of th e clivus, bu t it is ver y
or clip p ed an d su bsequ en t ly d ivid ed . An ot h er in cision can be rarely in dicated.
m ad e beh in d t h e sigm oid sin u s to p rovid e access, if n ecessar y,
in fron t of an d beh in d th e sigm oid sin us.
Patient Positioning
Th e p at ien t is p laced in th e p ark-ben ch posit ion . Th e h ead is
Intradural Exposure
placed in a Mayfield th ree-pin h ead h older an d p osit ion ed later-
After the dural incision s have been com pleted, the superior petro- ally on th e op erat ing table, w ith th e su rgical side facing upw ard.
sal sin u s divided, an d th e fate of th e sigm oid sin u s determ in ed, Th e su rgical t able is exten ded by p lacing a ¾-in ch plast ic board
th e du ral in cision is exten ded dow n th rough th e ten toriu m (p os- u n d er t h e m at t ress an d p u llin g t h e m at t ress an d board 15 to
terior to th e four th cran ial n er ve) to th e ten torial h iat us, th ereby 20 cm ou t p ast t h e t able’s en d . Th e p at ien t ’s d ep en d en t arm is
con n ect ing th e su p ra- an d in fraten torial com par t m en t s. If th e t h en allow ed to d rop off of t h e exten d ed en d of t h e op erat in g
sigm oid sin u s h as been preser ved, th e p osterior tem p oral lobe table (to im prove ven ous ret urn , m axim ize cran ial rotat ion an d

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61 Giant Aneurysms 733

flexion , an d m in im ize brach ial plexus injur y) an d is carefully th rough th e hyp oglossal can al du ring t h is drilling. In select cases,
cradled in foam un dern eath th e edge of th e t able, w ith in th e gap w e h ave exten ded th e bon e rem oval by drilling th e m astoid pro-
bet w een t h e Mayfield h ead h old er an d t h e h ead -h older t able cess an d occipitoatlan t al ar t icular facet , but th is is reser ved for
at t ach m en t . A foam roll is placed in th e axillar y region just at th e cases in w h ich an exqu isite an terior view is n ecessar y. Th us, th is
edge of th e t able’s en d. Th e h ead is posit ion ed to p lace th e in fe- tech n ique is rarely u sed.
rior clivu s p erpen dicu lar to th e floor an d obt ain m axim al open -
in g of th e p oster ior cer vical-to-occip it al an gle, t h ereby en -
abling greater m ovem en t of t h e op erat ing m icroscop e arou n d
Intradural Procedure
t h e su rgical field . Th e position of th e h ead star t s w ith th e m id- During an in t radural procedure, th e du ra m ater is open ed in a
lin e p arallel to th e floor. First , th e h ead an d n eck are flexed in th e cu r vilin ear fash ion an d , w it h it s base, h in ged laterally. Usin g
an teroposterior plan e un t il th e ch in is on e fingerbreadth from arach n oidal m icrodissect ion an d m in im al elevat ion of th e cere-
th e stern u m ; secon d, rot ated 45 degrees dow nw ard (to th e con - bellar ton sil, th e pon tom edullar y jun ct ion is exposed. In t reat ing
t ralateral side, aw ay from th e lesion ); an d th ird, laterally flexed giant vertebrobasilar aneur ysm s, this approach enables proxim al
30 degrees dow nw ard tow ard th e opposite sh oulder. With th e con t rol of th e bilateral ver tebral ar teries an d th eir bran ch es. Dis-
pat ien t in th is posit ion , th e ip silateral m astoid p rocess is th e sect ion can be p erform ed bet w een th e n er ves an d vessels of th e
h igh est poin t in th e surgical field. Th e upper sh ou lder is pulled posterior fossa to expose lesion s of in terest (Fig. 61.16).
dow n tow ard th e feet an d taped, fu r th er in creasing th e w orking
space for th e surgeon . Th e kn ees an d arm are w ell padded, an d
th e en t ire body is secu red w ith t ap e to allow fu ll rot at ion of th e Closure
operat ing t able. Closure of th e surgical field is accom plish ed in an atom ic layers.
Th e cer vical an d occip it al d u ra are reap p roxim ated w it h 4-0
Incision braided nylon sut ure. Th e cer vical h em ilam in ectom y an d cran i-
otom y are repaired using a st an dard plat ing system . During th e
Alth ough differen t cen ters use differen t in cision s, w e prefer an closu re, w e m ay loosen th e Mayfield h eadset from th e t able to
inverted hockey-stick incision starting at the m astoid prom inence, exten d t h e n eck an d allow bet ter reapp roxim at ion of th e fascia
u n der t h e superior n u ch al lin e to th e m idlin e, dow n to th e spi- an d m uscle. Th e rem ain ing layers are approxim ated in th e usu al
n ous process of C4. A 1-cm edge cuff of m uscle an d fascia is left fash ion w ith th e app ropriate su t ure of th e su rgeon’s preferen ce.
at th e u p per in cision to en able reap proxim at ion . Th e parasp in al
m uscles are split along th e m idlin e ligam en t , an d subperiosteal
dissect ion is p erform ed to expose th e spin ou s p rocess of th e Treatment Paradigms
u pp er cer vical ver tebrae.
Direct Clipping and Clip Reconstruction
With im provem ents in skull base approaches, m icrosurgical tech-
Bone Removal
n iques, an d n euroan esth esia, 50 to 70% of gian t an eur ysm s can
Using a h igh -speed drill an d Kerrison rongeurs, th e lateral m ass be directly clipped or clip recon st r ucted (Fig. 61.17).31,51,78 Table
of C1 an d t h e ver tebral ar ter y are exp osed . A r ich ven ou s bu n - 61.1 list s th e p ublish ed t reat m en t resu lt s for pat ien ts w ith gian t
d le su r rou n d s t h e lateral m ass of t h e u p p er cer vical ver tebrae. an eur ysm s. In deed, direct clipping of th e an eu r ysm n eck or its
Bleeding from th is plexu s can be con t rolled by com pression , bi- recon st ru ct ion u sing a t an dem -clip ping tech n iqu e is th e t reat-
polar coagu lat ion , an d th e u se of h em ostat ic m aterial. Next , th e m en t of ch oice. At Bar row Neu rological In st it u te, w e p roceed
Midas Rex drill w ith a B1 at t ach m en t an d foot p late (Midas Rex w it h an eu r ysm t reat m en t w it h t h e goal of d efin it ive clip p in g
Instit ute, Fort Worth, TX) is used to perform a C1–2 hem ilam inec- bu t prepare for altern at ive st rategies (i.e., bypass an d vessel sac-
tom y, w hich m ay be repaired at th e com pletion of the procedure. rifice) in th ose rare cases th at can n ot be direct ly clipp ed. Nat u -
To en h an ce th e u pw ard t rajector y afforded by th is procedu re, rally, cer tain an eur ysm s are best t reated w ith bypass an d vessel
a lateral suboccipital-ret rosigm oid cran iotom y is perform ed, be- sacrifice (cavern ou s carot id ar ter y an eu r ysm s, for exam ple),79
gin n ing at th e foram en m agn um , exten ding rost rally to th e an d in th ese cases w e proceed w ith th is st rategy an d do n ot sub -
t ran sverse sin u s, an d back cau dally to th e foram en m agn u m at ject th e pat ien t to dissect ion s w ith in th e cavern ous sin us th at
th e poin t of en t r y of th e ver tebral ar ter y. Th e cran iotom y can be m ay inju re crit ical n er ves. Th e u lt im ate t reat m en t decision is
tailored depen ding on th e rost ral exten sion of th e lesion being m ade during intraoperative evaluation of the aneur ysm m orphol-
t reated. ogy, paren t vessel caliber, perforator locat ion , presen ce of th rom -
Next , t h e rem ain ing rim of th e foram en m agn u m an d th e m e- bus an d calcificat ion s, fragilit y of vascular t issues, an d sku ll base
dial h alf of th e occip it al con dyle are rem oved w ith a com bin at ion an atom y th at m ay rest rict access to th e an eur ysm n eck. In th e
of a h igh -speed drill an d rongeu rs. Th e ext radu ral ver tebral ar- paraclin oid region , th e an terior clin oid p rocess an d th e p roxim al
ter y sh ould be protected during con dylar drilling. Drilling of th e an d distal dural rings m ay n eed to be rem oved to gain access to
con dyle is th ough t to be su fficien t on ce t h e con dylar vein s are th e an eu r ysm , w h ereas in t racavern ou s dissect ion m ay be n eces-
en cou n tered . Th is occu rs ~ 1 cm an terior (d eep ) to t h e p oin t of sar y in th e case of a cavern ou s ICA an eu r ysm s in th e rare in -
th e ver tebral ar ter y en t r y in to th e du ra. Con dylar drilling is es- st an ce w h en cavern ous ICA exposure is perform ed.
sen t ial for gain ing im p roved visu alizat ion of th e an terior brain - Evaluat ing w h eth er gian t an eu r ysm s can be clipped depen ds
stem . How ever, d r illin g of t h e con dyle beyon d t h e m ed ial h alf on soften ing of th e an eur ysm sac. Soften ing of th e sac can be
can dest abilize th e cran iover tebral ju n ct ion an d requ ire fixat ion perform ed by an eu r ysm t rap p ing, p roxim al occlu sion , dist al oc-
an d fusion . Th ere is lit tle risk to cran ial n er ve XII as it courses clu sion , t h e u se of card iac st an d st ill (rarely u sed for p oster ior

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734 V Cerebral and Spinal Aneurysms

a b

c d

Fig. 61.16a–h A 65-year-old wom an presented with Fisher grade IV sub- reveals a giant right posterior inferior cerebellar artery aneurysm. The patient
arachnoid hem orrhage. (a) Sagit tal, (b) coronal, (c) axial, and (d) three- was taken to the surgical theater for a right-sided far-lateral craniotomy and
dimensional (3D) reconstruction computed tomography angiography (CTA) clipping of the aneurysm .

circu lat ion an eu r ysm s), or t h e m ore recen t u se of ad en osin e. sion in th e cer vical ICA can be u sed to accom p lish th e sam e goal.
An eu r ysm t rap p ing h as been advocated as a good opt ion be- In cases w h ere th e an eur ysm con tain s a sign ifican t por t ion of
cau se it soften s th e an eu r ysm sac w h ile p reven t ing em bolizat ion throm bus, it m ay be necessary to open the aneurysm and decom -
of th rom bu s from th e sac, on ce th e an eur ysm sac is collapsed, press th e an eu r ysm before at tem pt ing to place a clip (Fig. 61.18).
an d th e fin al clip can be placed. In rare cases, an eur ysm t rapping In th ese sit uat ion s, th e an eu r ysm otom y m ust be properly placed
is in ad equ ate to p rovid e t h e rela xat ion n ecessar y to t reat t h e to preven t tearing th e an eur ysm at th e n eck an d to provide ade-
an eur ysm . In th ese cases, it m ay be n ecessar y to aspirate th e an - qu ate t issu e for clip p lacem en t . We advocate th e p reparat ion of
eu r ysm con ten t s u sing direct pu n ct u re or u sing th e “Dallas m a- th e cer vical ICA for all cases of gian t proxim al ICA an eu r ysm , bu t
n euver” by accessing th e cer vical carot id ar ter y.80 Balloon occlu - w e do n ot rou t in ely expose th e carot id ar ter y.

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61 Giant Aneurysms 735

e f

g h

Fig. 61.16a–h (continued ) (e –h) Postoperative CTA reveals obliteration of the aneurysm : (e) sagit tal, (f) coronal, (g ) axial, and (h) 3D reconstruction.
(Courtesy of Barrow Neurological Institute.)

Although direct clipping of the aneurysm neck is the treatm ent m ay allow m ore vigorous m an ipulat ion of th e rest of th e an eu-
of ch oice for m ost an eu r ysm s, at t im es placem en t of m u lt iple r ysm as ideal clip posit ion s are iden t ified. A furth er con st rain t is
clips, u sing Drake’s 12 an d Sugita et al’s 81 tan dem clipping tech - the fact that giant aneurysm s t ypically contain significant clot and
n ique, m ay be n ecessar y to obliterate th e an eur ysm . An eur ysm calcification. Because clips m ay not provide adequate closure force
clip s h ave th eir w eakest force at th e clip t ips; in som e cases, it to secu re th ese an eur ysm s, som e auth ors h ave recom m en ded
m ay be n ecessar y to stack m ult iple clips to provide ext ra support th e u se of cru sh ing in st r u m en t s to p rep are th e an eu r ysm for
for por t ion s of th e an eu r ysm th at are inadequately covered by fin al clipping.82 Special care m ust be paid w h en using crush ing
t h e in it ial clip . Tem p orar y clip s on t h e an eu r ysm n eck can be forceps as th ey can cause an eur ysm tearing. In cases w h ere th e
u sed to p lace an d opt im ize fin al clip s. Th e an eu r ysm n eck can an eur ysm clip does n ot provide adequate obliterat ion of th e
be fragile and prone to tearing, and placem ent of a tem porar y clip n eck, residu al flow w ith in th e an eur ysm m ay cause a on e-w ay

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736 V Cerebral and Spinal Aneurysms

force to preven t flow of blood in to th e an eur ysm sac. In placing


an eur ysm clips, care m ust be t aken to avoid scissoring th e blades,
as th is too can in adequately obliterate th e an eur ysm an d cause
tears. Placem ent of clip blades too close to the n ative vessel lum en
can in du ce vessel sten osis, w h ereas placem en t too far aw ay m ay
produ ce a “dog ear” th at m ay requ ire placem en t of booster clip s.
At Barrow Neurological Instit ute, w e use indocyanine green
(ICG) angiography in ever y an eur ysm case.84 ICG en ables visu al-
izat ion of flow in th e proxim al, distal, an d p erforat ing vessels,
w h ile exclusion of flow in th e an eur ysm is con firm ed. In select
cases, w e con t in u e to u se in t raoperat ive angiography, but w ith
th e in t rodu ct ion of ICG th is in dicat ion is redu ced . If th ese m o-
dalit ies are n ot available, direct visu alizat ion or Dop pler u lt ra-
son ography can be u sed to assess th e p aten cy of th e vessels after
clip placem en t.

Revascularization and Aneurysm Surgery


Fig. 61.17 Schem atic drawing of tandem clip placem ent. All aneurysm s
should be inspected for direct clipping of the aneurysm neck. Creative In cases w h ere th e an eur ysm n eck can n ot be directly clipped, it
application of aneurysm clips m ay be necessary for clip reconstruction of m ay be n ecessar y to use oth er tech n iques to exclude th e an eu -
giant aneurysm s. When necessary, tandem clips m ay be applied to rein- r ysm from th e circulat ion . On e st rategy for t reat m en t of un clip -
force one another. (Modified from Spet zler RF, Koos WT, Richling B, Lang J, pable an eu r ysm s is to in du ce flow reversal by sacrificing th e
eds. Color Atlas of Microneurosurgery, vol 2, 2nd ed. New York: Thiem e; diseased vessel eith er p roxim al or distal to th e an eu r ysm , w h ile
1997:314. Used with permission from Thiem e Publishers.)
providing a byp ass to revascu larize th e dist al territor y (Figs.
61.19 an d 61.20).23,24
Proxim al vessel occlu sion en ables reversal of blood flow an d
valve sit uat ion during systole th at m ay lead to a delayed an eu- in duct ion of th rom bosis w ith in th e an eu r ysm dom e du e to blood
r ysm ru pt ure. Altern at ively, fen est rat ion t ubes can be gen erated st agn at ion . Dist al vessel occlu sion sim ilarly in du ces st agn at ion
u sing m u lt iple clip s.83 of flow an d a st an ding fluid colu m n w ith in th e an eur ysm , w h ich
Ideal clip placem en t en ables th e en t ire surface of th e an eu- m ay resu lt in th rom bosis of th e an eu r ysm . Sim ilarly, a diseased
r ysm n eck to be covered by th e clip blade w ith adequate closing segm en t of a vessel can be t rapp ed. Proxim al ligat ion an d sim p le

a b

Fig. 61.18a–f Schem atic drawings showing rem oval of the intralum inal tebral artery is noted to be compressing the brainstem and cranial nerves.
thrombus and the re-creation of a vascular lum en of a dolichoectatic aneu- (b) The aneurysm is opened.
rysm of the vertebral artery. (a) The dolichoect atic aneurysm of the ver-

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61 Giant Aneurysms 737

c d

Fig. 61.18a–f (continued ) (c) The throm bus is rem oved with an ultrasonic
aspirator. (d) Once the lum en of the aneurysm is encountered, (e) Surgicel
(Johnson & Johnson, Arlington, TX) is used to control the bleeding (f) and
the vessel walls are brought together for reconstruction. (Courtesy of Bar-
row Neurological Institute.) f

t rapp ing w ith ou t byp ass can be u sed in rare cases w h ere ade- to occlude a cerebral vessel. How ever, th e BTO it self is n ot w ith -
qu ate collaterals exist .85 Th is tech n iqu e h as been u sed select ively out risks,86 an d predict ive result s are less th an perfect . Several
for cavern ou s ICA or un rupt ured proxim al carot id ICA an eu - st u dies of ICA occlu sion follow ing BTO h ave docu m en ted st roke
r ysm s. Proxim al ligat ion or t rapping m an euvers w ith out bypass m orbidit y rates of 1.5 to 4.8%w ith ongoing isch em ia in 10 to 12%
can rarely be perform ed safely in th e MCA; w e do n ot advocate of p at ien t s 44,87–89 an d delayed isch em ia rates of 1.4% p er year.90
th e u se of th is st rategy. In ad d it ion to ongoing isch em ic r isks, t h e sacr ifice of a m ajor
In h istorical series, surgical occlusion of th e ICA w ith out by- cerebral vessel in creases th e risk of flow -related an eur ysm s in
pass for th e m an agem en t of in t racran ial an eu r ysm s w as associ- collateral bran ch es, an d th is risk can be as h igh as 10%.91 Given
ated w ith infarction in up to 40%of cases.11 Balloon-test occlusion these challenges, w e h ave a st rategy of revascularizing in any case
(BTO) has been used in an attem pt to determ ine w hether it is safe w h ere a m ajor vessel sacrifice is p lan n ed.

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738 V Cerebral and Spinal Aneurysms

d
e

Fig. 19b

Fig. 19a
Fig. 19

Fig. 19d

Fig. 19c Fig. 19e

Fig. 61.19a–e Schem atic drawings of techniques for revascularization of barrel STA–MCA bypass. Alternatively, an anterior temporal artery-to-MCA
the anterior circulation. (a) Internal carotid artery (ICA) aneurysm s at the in situ bypass m ay be used for select aneurysm s. (e) Anterior cerebral ar-
cranial base can be trapped and revascularized with a cervical-to-petrous tery aneurysm s can be trapped and revascularized with an A2–A2 in situ
carotid bypass using a saphenous vein graft. (b) Cavernous ICA aneurysm s bypass. ACA, anterior cerebral artery; ACoA, anterior communicating artery;
can be trapped with a petrous-to-supraclinoid (C3–C5) carotid bypass using Ant. temp. A., anterior temporal artery; ECA, external carotid artery; MCA,
a saphenous vein graft or, alternatively, a cervical-to-supraclinoid carotid m iddle cerebral artery; Ophth. A., ophthalm ic artery; PCoA, posterior
bypass. (c) Supraclinoid ICA aneurysm s can be trapped with a superficial com m unicating artery; Rec. A. of Heubner, recurrent artery of Heubner;
temporal artery-to-middle cerebral artery (STA–MCA) bypass. An alternative Saph., saphenous; Supraclin., supraclinoid. (Courtesy of Barrow Neurologi-
strategy is to use an STA–MCA bypass with a saphenous vein interposition cal Institute.)
graft. (d) MCA aneurysms can be trapped and revascularized with a double-

Bypasses can be classified based on th e degree of blood flow opt ion w h ere sign ifican t flow is n eeded.91,93 Th e STAs provide a
th ey provid e. A h igh -flow byp ass (su ch as th e ICA–MCA byp ass reliable bypass in cases in w h ich flow m ust be directed to a sin -
w ith a saph en ou s vein in terposit ion graft) can be u sed to aug- gle bran ch ,94 bu t su ch grafts are n ot capable of acu tely replacing
m en t flow in cases w h ere large vessels such as th e ICA or MCA th e flow dem an ds of th e carot id ar ter y or t h e MCA. In cer t ain
are sacr ificed p roxim ally.92 Mediu m -flow byp ass (su ch as th e cases, a d ou ble-barrel STA bypass can be p erform ed . In selected
ICA to MCA w ith a radial arter y in terposit ion graft) is an oth er cases, th e STA–MCA graft h as been com bin ed w ith a gradu al, d e-

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61 Giant Aneurysms 739

Fig. 20 Fig. 20a

Fig. 61.20a,b Schem atic drawings of techniques for revascularization of


the posterior circulation. (a) The m idbasilar artery can be occluded proxi-
m ally or distally to the aneurysm and revascularized with a superficial tem -
poral artery (STA)-to-posterior cerebral artery (PCA) bypass or an STA-to-
superior cerebellar artery (SCA) bypass. We prefer to occlude the basilar
artery in the perforator-free zone below the SCAs. In select cases a double-
barrel bypass using the STA as a donor to PCA and SCA m ay be used to re-
vascularize the brainstem . (b) Vertebral artery aneurysm s can be trapped
by placing clips on the proxim al vertebral artery and at the origin of the
posterior inferior cerebellar artery (PICA). Endovascular coils can be placed
distally in the vertebral artery. A PICA–PICA in-situ bypass is used for revas-
cularization of the distal territories. Alternatively, an occipital artery-to-PICA
Fig. 20b bypass can be performed. (Courtesy of Barrow Neurological Institute.)

layed p roxim al occlu sion of th e ICA or MCA, w ith gen erally good tion of th e aneur ysm .23,96,97 Flow reversal can be perform ed using
results.23,24 Delayed proxim al occlusion follow ing distal STA–MCA en d ovascu lar tech n iqu es or by direct su rgical clipp ing. Occlu sion
bypass h as been repor ted to cause com plicat ion s because th e of th e in flow vessel can be perform ed at th e basilar ar ter y below
flow reversal provided by the bypass is adequate to induce throm - th e SCAs or on th e ver tebral ar teries distal to th e PICA t akeoff.
bosis of th e an eur ysm in som e cases, but in oth ers it can in duce Hu n terian ligat ion of th e basilar ar ter y is n ot w ith ou t risks,
an eur ysm al ru pt ure.95 We advocate im m ediate proxim al or dis- an d brain stem st rokes caused by flow m ism atch h ave been re-
tal occlusion after augm en tat ion of flow w ith a bypass. In th ese por ted. On e m eth od of augm en t ing flow to th e basilar apex an d
rare cases, delayed occlu sion can be perform ed surgically or by brainstem is by perform ing an extracranial-to-intracranial (EC–IC)
using en dovascular tech n iqu es. bypass procedure.98 In th e posterior circulat ion , t w o possible by-
Flow reversal an d byp ass can also be u sed in th e posterior cir- p ass opt ion s are t h e STA–SCA98 an d t h e STA–PCA byp asses 91
culat ion . Wide-based, large, com plex an eur ysm s of th e basilar (Fig. 61.20). In d ivid u ally t h ese byp asses m ay n ot su p p ly ad e-
apex pose a m ajor t reatm en t ch allenge as th ey are frequ en tly n ot qu ate blood to t h e brain stem . In cases w h ere a sin gle byp ass
am en able to direct m icrosurgical clipping or conven t ion al en do- m ay n ot sufficien tly revascularize th e brain stem , a double-barrel
vascular th erapies. Th e occlusion of th e basilar ar ter y m ay redi- STA–SCA an d STA–PCA byp ass m ay be perform ed to augm en t
rect flow from the basilar trunk and cause throm bosis and resolu- blood flow to th e basilar apex.99

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740 V Cerebral and Spinal Aneurysms

In Situ Bypass
In select cases, cerebral revascularization m ay be perform ed w ith-
out th e n eed to redirect flow from th e ext racran ial circulat ion .
Using in situ bypasses, flow can be redirected to distal territories,
an d th e an eur ysm can be t rapped or excised. We h ave repor ted
our experien ce w ith in sit u tem poral ar ter y-to-M2 bypasses for
t reat m en t of proxim al gian t MCA an eu r ysm s 100 (Fig. 61.19). In
th ese cases, th e tem p oral ar ter y is u sed to revascu larize th e d is-
tal MCA territor y, w h ereas th e MCA is occlu ded proxim al to th e
diseased por t ion of th e vessel. Oth er opt ion s for in sit u bypasses
in clu de th e p aired ACA an d PICA.101 In th ese sit u at ion s, blood
flow dist al to th e an eur ysm can be augm en ted w ith a side-to- a
side an astom osis.

Excision and Direct Vessel Reconstruction


Excision alon e is rarely possible or in dicated, esp ecially in cases
involving gian t an eu r ysm s w h ere a sign ifican t port ion of th e
vessel m ay be involved, but can be used w h en vessel redun dan cy
allow s it (Fig. 61.21).

Aneurysmal Wrapping
Alt h ough an eu r ysm al w rap p ing can be u sed to t reat sm aller
an eur ysm s,102 w rapp ing or coat ing gian t an eur ysm s w ith gau ze,
m uslin , cot ton, or acr ylic glue is rarely effect ive in preven t ing
grow th or elim in at ing fu t u re risk of h em orrh age.100,103 We do
n ot advocate th e use of th is tech n ique for th e t reat m en t of gian t
an eur ysm s.

Endovascular Techniques
b
Th e en dovascu lar t reat m en t of an eu r ysm s is con st an tly evolv-
ing, an d th is topic is w idely covered in th is book. Alth ough , h is-
torically, proxim al balloon occlu sion of th e in flow vessel (a form
of h u n terian ligat ion ) w as th e m eth od of ch oice for t reat ing gian t
an eu r ysm s, m ore recen t ly coils, sten t s, liqu id em bolics (e.g.,
Onyx-HD, Micro Th erap eu t ics, Ir vin e, CA), an d flow d iver ters
h ave revolu t ion ized an eu r ysm t reat m en t .
Although initially favored, in tra-aneurysm al balloon occlusion
is n ow associated w ith h igh rates of an eur ysm can alizat ion , de-
layed grow th , an d an eu r ysm ru pt u re. Th e in t rodu ct ion of Gug-
lielm i coils en abled th e dep osit ion of th rom bogen ic coils in to th e
an eur ysm sac.104 Un for t u n ately, coil com p act ion h as resu lted in
a gen erally poor ou tcom e as assessed by an eur ysm obliterat ion ,
recu rren ce, an d need for ret reat m en t , especially for gian t an eu -
r ysm s.31,34,66,85,92,105–136 Recu r ren ce rates as h igh as 40% h ave
been cited using variou s coils (Table 61.1). Th is is esp ecially t r u e c
for an eu r ysm s at th e basilar apex w h ere h em odyn am ic factors Fig. 61.21a–c Schem atic drawings of aneurysm excision and direct re-
predispose th ese an eu r ysm s to recu rren ce an d recan alizat ion anastom osis. (a) This giant m iddle cerebral artery (MCA) aneurysm is
after coiling.26,137 More recen tly, com p lex sten t ing tech n iqu es am enable to resection with prim ary reanastom osis. (b) After obtaining
proxim al and distal control, (c) the aneurysm is resected and the ends of
h ave provided som e im provem en t for a subset of an eu r ysm s,138
the parent artery are reanastom osed. (Courtesy of Barrow Neurological
but overall th e result s after sten t ing rem ain dism al. An eur ysm s Institute.)
th at are ideal for coil em bolizat ion are th ose w ith sm all n ecks
an d saccu lar m orp h ology. Th ese an eu r ysm s are also ideal for
su rgical clipp ing. In cases of w ide n ecks or a dysp last ic an eu r ysm cially in th e case of SAH.139 With th e con t in ual im provem en t of
w all, coils can n ot be ret ain ed w ith in th e an eu r ysm . Th e u se of en dovascu lar tech n ology, coiling resu lts for gian t an eur ysm s are
sten t ing tech n ology h as greatly im p roved coiling for w ide-n eck boun d to im prove. How ever, today en dovascular tech n iqu es are
an eur ysm s 138 (Fig. 61.22), bu t th e n eed to p lace th e p at ien t on n ot w ith ou t risks an d com plicat ion s. Access-related inju r y, con -
an t iplatelet regim en s m akes th is an un at t ract ive opt ion , espe- t rast toxicit y, radiat ion injur y, an d isch em ic an d h em orrh agic

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61 Giant Aneurysms 741

a b

Fig . 61.22a,b Schem atic drawings of endovascular treatm ent of giant coiling is one option for obtaining high packing densit y while preventing
aneurysms. (a) Giant aneurysm s can be treated with deposition of throm - coil extrusion from aneurysm s. The stent is used to but tress the coils within
bogenic coils. Despite initial excitement, the results of coiling for giant aneu- the aneurysm lumen. The results of stent-assisted coiling are bet ter than
rysm s have been dism al, with high rates of recurrence. (b) Stent-assisted those for coiling alone. (Courtesy of Barrow Neurological Institute.)

com p licat ion s of en dovascu lar procedu res are rare bu t real risks. Flow -diver t ing sten t s h ave recen tly gain ed Food an d Drug Ad-
Part ially t reated an eur ysm s are ch allenging lesion s for surgical m inist rat ion (FDA) approval an d are curren tly u sed for th e t reat -
rep air. Alth ough coiling can resu lt in resolu t ion of m ass effect , in m en t of proxim al ICA an eur ysm s.4,112,144 Flow -diver t ing sten ts,
m ost cases this is not the case. Coil em bolization of the aneurysm su ch as th e Pipelin e Em bolizat ion Device an d th e Silk (Balt Ex-
m ay reduce th e h em odyn am ic pulsat ion on su rrou n ding n eural t ru sion , Mon t m oren cy, Fran ce), are h igh - porosit y, h igh -coverage
st r u ct u res, bu t w orsen ing of m ass effect can be obser ved. stents that enable diversion of blood flow out of the aneur ysm and
Onyx-HD, a h igh -viscosit y form of Onyx polym er, h as been in to th e n at ive direct ion of blood flow (Fig. 61.23). Exclu sion of
advocated for th e em bolizat ion of an eur ysm s. Th e results of sev- flow from th e an eur ysm en ables th e stagn at ion n ecessar y to in -
eral t rials u sing Onyx w ith an d w ith ou t sten t s h ave been prom is- duce throm bosis of the aneur ysm (Fig. 61.24). Once throm bosis is
ing, bu t long-term ou tcom es are n ot available at th is t im e.140–143 accom plish ed, gradual clot resorpt ion an d n eoen doth elializat ion

a b

Fig . 61.23a,b (a) A flow-diverting device placed across a giant aneurysm neck can be used to redirect flow, allowing for the aneurysm wall to heal.
(b) Flow diverters can be com bined with coils to provide m ore im m ediate throm bosis of aneurysm s. (Courtesy of Barrow Neurological Institute.)

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742 V Cerebral and Spinal Aneurysms

a b

c d

e f

Fig. 61.24a–f Endovascular treatment of a giant aneurysm. Endovascular giogram s dem onstrate the aneurysm. (c) Anteroposterior and (d) lateral
techniques have expanded greatly over the past decade. For select aneu- post–coil/pipeline angiogram s demonstrate complete obliteration of the
rysm s, the use of a flow diverter can provide robust results. This 36-year- aneurysm . At 6 m onths post treatm ent, (e) anteroposterior and (f) lateral
old m an with an incidentally identified giant internal carotid artery (ICA) angiogram s dem onstrate a durable treatm ent without evidence of recur-
aneurysm was treated using a com bination of a flow-diverting stent and rence or residual. (Courtesy of Barrow Neurological Institute.)
coil em bolization. (a) Anteroposterior and (b) lateral preoperative ICA an-

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61 Giant Aneurysms 743

en able th e h ealing of disease vessels. Flow diver ters h ave been


sh ow n to en able p reser vat ion of flow to covered p er forators,
■ Conclusion
bu t com p licat ion s in clu d ing late t h rom boses h ave been re- Gian t an eu r ysm s are ch allenging, u n com m on lesion s. Given th e
por ted.145–147 Th e results of th e Pipelin e for In t racran ial Treat- poor nat ural histor y of these aneur ysm s, patients require treat-
m en t of An eur ysm s (PITA) an d Pipelin e for Un coilable or Failed m ent to m inim ize m orbidit y and m ortalit y. Although the m ajorit y
An eu r ysm s (PUFS) t rials for th e u se of th ese devices in th e proxi- of gian t an eur ysm s can be directly clipped or clip recon st ru cted,
m al an terior circulat ion h ave been prom ising.4 Th e resu lt s of th e a sm all por t ion requ ire th e use of com plex revascu larizat ion an d
use of flow diverters in th e p osterior circu lat ion h as been less flow -reversal tech n iqu es. With th e con t in ual im provem en t in
prom ising,5 alth ough in dividu al su ccesses h ave been reported.148 en d ovascu lar tech n iqu es, it is p ossible t h at m ore of th ese lesion s
An eu r ysm s w ith sign ifican t clot m ay n ot allow th e p rop er su r- w ill be t reated using th ese approach es in th e fut ure. For n ow,
face area con t act n ecessar y to fully exclude flow, w h ich preven ts h ow ever, w ith lim ited dat a on en dolum in al recon st ru ct ion an d
an eur ysm h ealing. At our in st it ut ion , w e advocate th e use of poor ou tcom es w ith th e u se of flow diver ters in th e p osterior
flow diverters in proxim al ICA gian t an eur ysm s. We select ively circulat ion , su rgical t reat m en t rem ain s th e m ain stay for pat ien t s
use th ese devices in difficult p osterior circulat ion an eu r ysm s, w ith th ese com plex lesion s. Surgical t reat m en t of pat ien ts w ith
but results on th e use of th is class of devices are pen ding long- gian t an eur ysm s requ ires adh eren ce to th e ten et s of sku ll base
term follow -up.149 Th e added n ecessit y to u se du al an t ip latelet s an d an eur ysm surger y: (1) resect bon e an d do n ot ret ract brain
w it h flow d iver ters m akes t h e d iver ters less t h an id eal in t h e to expose n eeded an atom y; (2) obtain early vascular con t rol; an d
set t ing of SAH, but su ccessful use h as been repor ted w ith th is (3) obliterate an eu r ysm s w h ile p reser ving t h e in flow , p aren t ,
device, alth ough w ith sign ifican t poten t ial risk, in th e set t ing of outflow, an d p erforat ing vessels.
h em orrh age.139

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19:E8 98. Ogaw a A, Kam eyam a M, Mu raish i K, Yosh im oto T, Ito M, Saku rai Y. Cere-
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79. Barn et t DW, Barrow DL, Joseph GJ. Com bin ed ext racran ial-in t racran ial J Neu rosurg 1992;76:955–960
bypass an d in t raoperat ive balloon occlusion for th e t reat m en t of in t racav- 99. Kalan i MY, Hu YC, Sp et zler RF. A d ou ble-bar rel su p er ficial tem p oral
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92–97, discussion 97–98 rebral arter y (STA-PCA) bypass for revascularizat ion of th e basilar apex.
80. Batjer HH, Sam son DS. Ret rograde suct ion decom pression of gian t para- J Clin Neurosci 2013;20:887–889
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81. Sugit a K, Kobayash i S, Kyosh im a K, Nakagaw a F. Fen est rated clip s for to a secon dar y t r u n k of t h e m id d le cerebral ar ter y for t reat m en t of a
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86. Math is JM, Barr JD, Ju ngreis CA, et al. Tem porar y balloon test occlu sion of 105. Bavin zski G, Killer M, Gru ber A, Reinprech t A, Gross CE, Rich ling B. Treat-
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diol 1995;16:749–754 able coils: a 6-year exp erien ce. J Neu rosu rg 1999;90:843–852
87. Sw earingen B, Heros RC. Com m on carot id occlusion for un clippable ca- 106. Eskr idge JM, Son g JK. En dovascu lar em bolizat ion of 150 basilar t ip
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cussion 30 cran ial an eu r ysm s: a 7-year, single-cen ter exp er ien ce. Neu rosu rger y
89. Sudh akar KV, Saw lan i V, Ph adke RV, Kum ar S, Ah m ed S, Gujral RB. Tem po - 1999;45:793–803, discussion 803–804
rar y balloon occlusion of in tern al carot id arter y : a sim ple an d reliable 108. Gobin YP, Viñ uela F, Gurian JH, et al. Treat m en t of large an d gian t fusi-
clin ical test . Neurol In dia 2000;48:140–143 form in t racran ial an eur ysm s w ith Guglielm i det achable coils. J Neuro-
90. Roski RA, Sp et zler RF, Nu lsen FE. Late com p licat ion s of carot id ligat ion surg 1996;84:55–62
in t h e t reat m en t of in t racran ial an eu r ysm s. J Neu rosu rg 1981;54:583– 109. Hauck EF, Woh lfeld B, Welch BG, W h ite JA, Sam son D. Clipping of ver y
587 large or gian t un ru pt u red in t racran ial aneu r ysm s in th e anterior circula-
91. Law ton MT, Ham ilton MG, Morcos JJ, Spet zler RF. Revascularizat ion an d t ion : an outcom e st udy. J Neurosurg 2008;109:1012–1018
an eu r ysm su rger y: cu rren t tech n iqu es, in dicat ion s, an d ou tcom e. Neu ro- 110. Hen kes H, Fisch er S, Weber W, et al. En dovascular coil occlusion of 1811
surger y 1996;38:83–92, discussion 92–94 in t racran ial an eur ysm s: early angiograph ic an d clin ical result s. Neuro-
92. Jafar JJ, Russell SM, Woo HH. Treat m en t of gian t in t racran ial an eur ysm s surger y 2004;54:268–280, discussion 280–285
w ith saph en ous vein ext racran ial-to-in t racran ial bypass graft ing: in dica- 111. Jah rom i BS, Mocco J, Bang JA, et al. Clin ical an d angiograph ic outcom e
t ion s, operat ive tech n ique, an d result s in 29 pat ien t s. Neurosurger y after en d ovascu lar m an agem en t of gian t in t racran ial an eu r ysm s. Neu ro-
2002;51:138–144, discussion 144–146 surger y 2008;63:662–674, discu ssion 674–675
93. Kam ijo K, Mat sui T. Acute ext racran ial-int racranial bypass using a radial 112. Lylyk P, Miran da C, Cerat to R, et al. Curat ive en dovascular recon st r uct ion
ar ter y graft along w ith t rap ping of a r u pt u red blood blister–like an eu- of cerebral an eu r ysm s w ith th e pipelin e em bolizat ion device: th e Bue-
r ysm of th e in tern al carot id ar ter y. Clin ical ar t icle. J Neurosu rg 2010;113: n os Aires experien ce. Neurosu rger y 2009;64:632–642, discussion 642–
781–785 643, qu iz N6

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746 V Cerebral and Spinal Aneurysms

113. Higash ida RT, Halback VV, Dorm an dy B, Bell JD, Hiesh im a GB. En d o- 134. Hacein -Bey L, Con n olly ES Jr, Mayer SA, Young W L, Pile-Sp ellm an J, Solo-
vascular t reat m en t of int racran ial an eur ysm s w ith a n ew silicon e m icro- m on RA. Com p lex in t racran ial an eu r ysm s: com bin ed op erat ive an d
balloon device: tech n ical con siderat ion s an d in dicat ion s for th erapy. en dovascular approach es. Neurosurger y 1998;43:1304–1312, discus-
Radiology 1990;174(3 Pt 1):687–691 sion 1312–1313
114. Hallacq P, Piot in M, Moret J. En d ovascu lar occlu sion of t h e p osterior 135. Arn autović KI, Al-Meft y O, Angt uaco E. A com bin ed m icrosurgical skull-
cerebral ar ter y for th e t reat m en t of p 2 segm en t an eu r ysm s: ret rosp ec- base an d en dovascular approach to gian t an d large paraclin oid an eu-
t ive review of a 10-year series. AJNR Am J Neuroradiol 2002;23:1128– r ysm s. Surg Neurol 1998;50:504–518, discussion 518–520
1136 136. Pon ce FA, Albu qu erqu e FC, McDougall CG, Han PP, Zabram ski JM, Sp et z-
115. Slu zew ski M, Men ovsky T, van Rooij W J, Wijn alda D. Coiling of ver y large ler RF. Com bined endovascular and m icrosurgical m anagem ent of giant and
or gian t cerebral an eur ysm s: long-term clin ical an d serial angiograph ic com plex unruptured aneurysm s. Neurosurg Focus 2004;17:E11
result s. AJNR Am J Neuroradiol 2003;24:257–262 137. Henkes H, Fisch er S, Mariu sh i W, et al. Angiograph ic an d clin ical result s
116. Kolasa PP, Kaurzel Z, Lew in ski A. Treat m en t of gian t paraclin oid an eu - in 316 coil-t reated basilar ar ter y bifurcat ion an eur ysm s. J Neu rosu rg
rysm s. Ow n experience. Neuroendocrinol Let t 2004;25:287–291 2005;103:990–999
117. Murayam a Y, Viñ uela F, Ish ii A, et al. In it ial clinical experien ce w ith m a- 138. Fargen KM, Mocco J, Neal D, et al. A m u lt icen ter st u dy of sten t-assisted
t rix det ach able coils for th e t reat m en t of in t racran ial an eur ysm s. J Neu- coilin g of cerebral an eu r ysm s w it h a Y con figu rat ion . Neu rosu rger y
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118. Sh i ZS, Ziegler J, Duckw iler GR, et al. Man agem en t of gian t m iddle cere- 139. Mar t in AR, Cru z JP, Matou k CC, Spears J, Marot t a TR. Th e p ipelin e flow -
bral arter y an eur ysm s w ith in corporated bran ch es: part ial en dovascu lar diver t ing sten t for exclu sion of ru pt u red in t racran ial an eu r ysm s w ith
coiling or com bin ed ext racran ial-in t racran ial bypass—a team approach. difficult m orphologies. Neurosurger y 2012;70(1, Suppl Operative):21–28,
Neurosu rger y 2009;65(6, Suppl):121–129, discussion 129–131 discu ssion 28
119. Peerless SJ, Wallace MC, Drake CG. Gian t in t racran ial an eur ysm s. In : 140. Cekirge HS, Saatci I, Geyik S, Yavu z K, Ozt ü rk H, Pam u k G. In t rasaccu lar
Youm ans JR, ed. Neurological Surgery: A Com prehensive Reference Guide com bin at ion of m et allic coils an d onyx liqu id em bolic agen t for th e en -
to th e Diagn osis an d Man agem en t of Neu rological Problem s. Ph iladel- d ovascu lar t reat m en t of cerebral an eu r ysm s. J Neu rosu rg 2006;105:
ph ia: W B Sau n ders; 1990:1742–1763 706–712
120. Yaşargil MG. Microneu rosurger y. New York: Th iem e-St rat ton ; 1984 141. Liang G, Li Z, Gao X, et al. Using Onyx in endovascular em bolization of in-
121. Hosobuchi Y. Giant intracranial aneurysm s. In: Wilkins RH, Rengachary SS, ternal carotid artery large or giant aneur ysm s. Eur J Radiol 2011
eds. Neurosurger y. New York: McGraw -Hill; 1985:1404–1414 142. Mawad ME, Cekirge S, Ciceri E, Saatci I. Endovascular treatm ent of giant
122. Heros RC. Man agem en t of gian t paraclin oid an eur ysm s. In : Kikuch i H, and large intracranial aneurysm s by using a com bination of stent place-
Fuku sh im a T, Wat an abe K, eds. In t racran ial An eur ysm s. Nigat a, Japan: m ent and liquid polym er injection. J Neurosurg 2002;96:474–482
Nish im u ra; 1986:273–282 143. Piske RL, Kan ash iro LH, Pasch oal E, Agn er C, Lim a SS, Aguiar PH. Evalua-
123. Sun dt TM Jr. Result s of surgical m an agem en t . In : Sun dt TM Jr, ed. Su rgi- t ion of Onyx HD-500 em bolic system in th e t reat m en t of 84 w ide-n eck
cal Techn iques for Saccular and Giant In tracranial An eurysm s. Baltim ore: in t racran ial an eu r ysm s. Neurosurger y 2009;64:E865–E875, discussion
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124. Au sm an JI, Diaz FG, Sadasivan B, Gon zeles-Por t illo M Jr, Malik GM, 144. Fisch er S, Vajda Z, Agu ilar Perez M, et al. Pip elin e em bolizat ion device
Deopujari CE. Gian t in t racran ial an eur ysm surger y: th e role of m icrovas- (PED) for n eu rovascu lar recon st r u ct ion : in it ial exp erien ce in th e t reat-
cular recon st r uct ion. Surg Neurol 1990;34:8–15 m en t of 101 in t racran ial an eu r ysm s an d d issect ion s. Neu rorad iology
125. Kat t ner KA, Bailes J, Fu kush im a T. Direct surgical m an agem en t of large 2012;54:369–382
bulbou s an d gian t an eur ysm s involving th e paraclin oid segm en t of th e 145. Fiorella D, Hsu D, Woo HH, Tarr RW, Nelson PK. Ver y late th rom bosis of
in tern al carot id arter y: report of 29 cases. Surg Neurol 1998;49:471– a pipelin e em bolizat ion device const ruct: case repor t . Neu rosu rger y
480 2010;67(3, Su ppl Operat ive):E313–E314, discussion E314
126. Sam son D, Batjer HH, Kopit n ik TA Jr. Curren t resu lt s of th e surgical m an - 146. Lop es DK, Joh n son AK. Evalu at ion of cerebral ar ter y p er forators an d
agem en t of an eu r ysm s of th e basilar apex. Neu rosu rger y 1999;44:697– t h e pipelin e em bolizat ion device using opt ical coh eren ce tom ography.
702, discussion 702–704 J Neu roin ter v Su rg 2012;4:291–294
127. Osaw a M, Hongo K, Tanaka Y, Nakam ura Y, Kit azaw a K, Kobayash i S. Re- 147. Puffer RC, Kallm es DF, Cloft HJ, Lan zin o G. Paten cy of th e oph th alm ic
sult s of direct surger y for an eur ysm al su barach n oid h aem orrh age: out- arter y after flow diversion t reat m en t of paraclin oid an eur ysm s. J Neuro-
com e of 2055 pat ient s w h o un der w en t direct an eur ysm surger y and surg 2012;116:892–896
profile of r u pt u red in t racran ial an eu r ysm s. Act a Neu roch ir (Wien ) 2001; 148. Fiorella D, Kelly ME, Albu qu erqu e FC, Nelson PK. Curat ive recon st ruct ion
143:655–663, discussion 663–664 of a gian t m idbasilar t r un k an eur ysm w ith th e pipelin e em bolizat ion
128. Law ton MT. Basilar apex aneurysm s: surgical results and perspectives from device. Neu rosu rger y 2009;64:212–217, discussion 217
an initial experience. Neurosurgery 2002;50:1–8, discussion 8–10 149. Ducruet AF, Crow ley RW, Albu qu erqu e FC, McDougall CG. Recon st ruct ive
129. Lozier AP, Kim GH, Sciacca RR, Con n olly ES Jr, Solom on RA. Microsurgical en dovascu lar t reat m en t of a rupt ured ver tebral ar ter y dissect ing aneu-
t reat m en t of basilar apex an eur ysm s: perioperat ive an d long-term clin i- r ysm using th e Pipelin e em bolizat ion device. J Neuroin ter v Surg 2013;
cal outcom e. Neurosurgery 2004;54:286–296, discussion 296–299 5:e20
130. Krish t AF, Krayen bü hl N, Sercl D, Bikm az K, Kadri PA. Result s of m icro- 150. Tateshim a S, Murayam a Y, Gobin YP, Duckw iler GR, Guglielm i G, Viñ uela F.
surgical clipping of 50 h igh com plexit y basilar apex aneu r ysm s. Neuro- Endovascular treatm ent of basilar tip aneurysm s using Guglielm i detach-
surger y 2007;60:242–250, discussion 250–252 able coils: anatom ic and clinical outcom es in 73 patients from a single insti-
131. Sh arm a BS, Gupt a A, Ah m ad FU, Suri A, Meh t a VS. Surgical m an agem en t tution. Neurosurgery 2000;47:1332–1339, discussion 1339–1342
of gian t in t racran ial an eur ysm s. Clin Neurol Neurosurg 2008;110:674– 151. Sh ibuya M, Sugit a AK. In t racran ial gian t an eu r ysm s. In : You m an s J, ed.
681 Neurological Surger y. Philadelph ia: W B Saun ders; 1996:1310–1319
132. Can tore G, San toro A, Guidet t i G, Delfin is CP, Colon n ese C, Passacan t illi E. 152. Xu BN, Sun ZH, Rom an i R, et al. Microsu rgical m an agem en t of large an d
Su rgical t reat m en t of gian t int racran ial an eu r ysm s: current view poin t . gian t paraclin oid an eur ysm s. World Neu rosu rg 2010;73:137–146, dis-
Neurosurger y 2008;63(4, Suppl 2):279–289, discussion 289–290 cussion e17, e19
133. San o H. Treat m en t of com p lex in t racran ial an eu r ysm s of an ter ior cir- 153. San ai N, Law ton MT. Microsu rgical m an agem en t of gian t in t racran ial an -
cu lat ion u sing m u lt ip le clip s. Act a Neuroch ir Suppl (Wien ) 2010;107: eur ysm s. In : Winn HR, ed. Youm an s Neurological Surger y, 6th ed. Ph ila-
27–31 delphia: Elsevier Saun ders; 2011:3953–3971

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154. Su n dt TMJ. Resu lt s of su rgical m an agem en t . In : Su n dt TMJ, ed. Su rgical 156. Yaşargil MG. Gian t in t racran ial an eu r ysm s. In : Yaşargil MG, ed. Micro-
Tech n iques for Saccular an d Giant In t racran ial An eur ysm s. Balt im ore: n eu rosu rger y II: Clin ical Con sid erat ion s, Su rger y of t h e In t racran ial
William s & Wilkins; 1990:19–23 An eur ysm s an d Result s. New York: Thiem e-St rat ton ; 1984:296–304
155. Sym on L, Vajda J. Surgical experien ces w ith gian t in t racran ial an eu - 157. On u m a T, Su zu ki J. Su rgical t reat m en t of gian t in t racran ial an eu r ysm s.
r ysm s. J Neu rosurg 1984;61:1009–1028 J Neu rosurg 1979;51:33–36

Neurosurgery Books Full


62 Incidental Aneurysms
Issam A. Aw ad, Mahua Dey, Jam es Brorson, and Seon-Kyu Lee

■ Epidemiology and Scope ■ Natural History Benchmarks:


of the Problem The ISUIA and Beyond
With an an n ual in ciden ce rate var ying from 6 to 16 per 100,000
ISUIA Background and Methods
w orldw ide (h ighest rates reported from Japan and Fin land), m ore
th an 15,000 Am erican s su ffer from an an eu r ysm al su barach n oid Th e In tern at ion al St u dy of Un r u pt u red In t racran ial An eu r ysm s
h em orrh age (SAH) each year.1 Ru pt u re of in t racran ial an eu r ysm s (ISUIA) w as a collaborat ion of Nor th Am erican an d European in -
accoun ts for as m any as 15% of all cerebrovascular acciden t s vest igators from 53 cen ters aim ing to assess th e n at ural h istor y
(CVAs), an d are associated w ith 30-day m or t alit y rates of 45 to of UIAs, as w ell as to evaluate th e m orbidit y an d m or talit y asso-
80%, w ith approxim ately h alf th e su r vivors sust ain ing irrevers- ciated w ith t reat m en t . Th e ISUIA con sisted of t w o par ts. In th e
ible brain dam age.1 Th e m ost effect ive st rategy for lessen ing th is first par t , publish ed in 1998,3 m edical records of 1,449 pat ien ts
h igh burden of m ort alit y an d disabilit y aim s at th e p rim ar y pre- diagn osed bet w een 1970 an d 1991 w ith UIAs w ere review ed to
ven t ion of SAH, an d h en ce a m ore rat ion al t reat m en t of un r up - provide ret rosp ect ive n at u ral h istor y dat a. In total, 1,172 of th ese
t ured in t racran ial an eu r ysm s (UIAs). With great advan cem en t s patients w ere enrolled in th e prospective evaluation of treatm ent
in the noninvasive im aging m odalities like com puted tom ography risks. Th e secon d par t , p u blish ed in 2003,4 exam in ed 4,060 p ro-
angiography (CTA) and m agnetic resonance angiography (MRA), spect ively en rolled pat ien t s (diagn osed bet w een 1991 an d 1998)
an in creasing n um ber of UIAs are being foun d in ciden tally or in for both th e n at u ral h istor y of un rupt u red an eur ysm s an d th e
associat ion w ith h eadach e or un related sym ptom s. Repor ted fre- procedu ral m orbidit y an d m or talit y in th ose p at ien ts for w h om
qu en cies of in ciden t al cerebral an eu r ysm s var y from 0.5 to 2%in su rgical or en dovascu lar th erapy w as elected. A key obser vat ion
im aging st udies an d 1 to 9% in au top sy st u dies, w ith a greater of ISUIA w as th e sign ifican ce of dist inguishing pat ien ts w ith un -
p revalen ce in old er p at ien t s.2 Man agem en t opt ion s for UIAs in - rupt ured an eur ysm s an d n o prior h istor y of rupt u re of an oth er
volve obser vat ion or in ter ven t ion by m icrosu rgical clip p in g or an eur ysm (group 1) from th ose w ith un r upt ured an eur ysm s ac-
en d ovascu lar coilin g, bu t t h e opt im al m an agem en t st rategy re- com panying an oth er previou sly r upt u red an eur ysm (group 2).
m ain s con t roversial. In ISUIA par t on e, pat ien ts w ith UIAs from 1970 to 1991 w ere
Th e n at u ral h istor y of UIAs an d th e ou tcom es of variou s in - iden t ified by ch art review, w ith exclu sion of n on saccu lar an eu -
ter ven t ion s are in flu en ced by (1) p at ien t factors, su ch as age, r ysm s, th ose w ith diam eters less th an 2 m m , th ose th at w ere
p reviou s an eu r ysm al SAH, fam ily h istor y of an eu r ysm or SAH, previously m an ipulated, th ose associated w ith an oth er w ise un -
an d coexist ing m edical con dit ion s; (2) an eur ysm ch aracterist ics, exp lain ed in t racran ial h em orrh age, an d th ose associated w ith a
su ch as size, locat ion , an d m orp h ology; an d (3) factors in m an - m align an t brain t um or. In th is series, UIAs w ere discovered be-
agem en t , su ch as th e experien ce of th e su rgical an d en dovascu - cau se of h eadach es in 36% of pat ien t s, isch em ic cerebrovascu lar
lar team s an d t h e t reat ing h osp it al. To date t h ere h ave been n o disease in 18%, cran ial n er ve deficits in 15%, an eu r ysm al m ass
p rosp ect ive ran d om ized t r ials of com p arat ive t reat m en t effec- effect in 6%, ill-defined spells in 5%, convulsive disorder in 4%, sub-
t iven ess, an d h en ce t h ere are n o evid en ce-based st an dard s for du ral or in t racerebral h em orrh age in 2.7%, brain t u m or in 1.7%,
clin ical m an agem en t . So clin ical d ecision s are gu id ed by t h e an d n er vous system degen erat ive disease in 0.5%. Assign m en t of
clin ician’s best an alysis an d judgm en t of variou s opt ion s, in ligh t pat ien ts w ith in ISUIA to su rgical, en dovascu lar, or con ser vat ive
of n at ural h istor y st udies an d th e publish ed experien ce w ith n on operat ive m an agem en t w as m ade on clin ical grou n ds “at th e
various t reat m en ts. Th is ch apter review s th e range of in form a- tim e the patient w as first seen at the ISUIA cen tre.”3 In the second
t ion regarding n at u ral risks an d t reat m en t ou tcom es of UIAs. We par t of ISUIA, a sim ilar coh or t of u n ru pt u red in t racran ial saccu -
present a m ultidisciplinary perspective of the problem , and focus lar an eur ysm s w as iden t ified an d p rosp ect ively follow ed, again
our discu ssion prim arily on an eu r ysm s discovered in ciden tally, w ith t reat m en t determ in ed on clin ical groun ds at th e discret ion
or in th e w orkup of h eadach e sym ptom s, w h ich m ay or m ay n ot of local clin ician s. Of 4,060 pat ien ts en rolled in the prospect ive
be related to th e an eur ysm . We exclude con siderat ion of dem on - phase of ISUIA, nearly half (1,917) underwent open surgical treat-
st rably sym ptom at ic or ru pt ured an eu r ysm s, for w h ich th ere is m en t , an d an oth er 451 h ad en dovascular procedures, leaving
less con t roversy regard ing m an agem en t . 1,692 pat ien ts (42%) w h o did n ot u n dergo an eu r ysm al repair.

748

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62 Incidental Aneurysm s 749

Results and Impact of ISUIA Th e secon d par t of t h e ISUIA also exam in ed p rocedu ral risks
p rosp ect ively in 1,917 p at ien t s u n d ergoin g op en su rger y an d
Th e resu lt s of th e first part of th e ISUIA, w h en p u blish ed in 1998,
in 451 p at ien t s su bjected to en d ovascu lar p roced u res am on g
w ere groun d-breaking, sh ow ing a ver y low risk of rupt ure, less
p at ien t s recru ited from 1991 to 1998. Rates of in t raprocedural
th an 0.05% per year, of an eu r ysm s less th an 10 m m in diam eter
rupt ure, cerebral in farct ion , periprocedural in t racran ial h em or-
in patients w ithout prior ruptured aneurysm s (group 1). A higher
rh age, an d im p aired cogn it ive fu n ct ion w ere su bst an t ial, p ro-
risk of ru pt u re of th ese sm all an eu r ysm s w as fou n d in p at ien t s
d u cin g overall m orbid it y an d m or t alit y rates in t h e su rgical
w ith prior rupt ure of an oth er an eur ysm (group 2), w ith a rup -
grou p at 1 year of 12.6% (grou p 1) an d 10.1% (grou p 2) an d in
t u re rate of 0.5% per year. In both grou p s, h igh er rates of r u pt u re
t h e en dovascu lar grou p of 9.8% (grou p 1) an d 7.1% (grou p 2).
w ere foun d in larger an eu r ysm s an d an eur ysm s located at th e
Risks of in ter ven t ion in creased w ith in creased age, w ith an eu-
basilar t ip, at th e ver tebrobasilar or posterior cerebral ar teries, or
r ysm diam eter > 12 m m , w ith posterior circulat ion locat ion of
at th e p osterior com m u n icat ing ar ter y. Rates of com bin ed surgi-
an eur ysm , an d w ith sym ptom at ic an eur ysm s. It w as n oted th at
cal m orbidit y an d m ortalit y were h igher than in previous reports,
m any of th e factors porten ding a h igh er risk of an eur ysm ru p -
m easured at 1 year as 15.7% in group 1 an d 13.1% in group 2,
t u re also w ere associated w ith h igh er su rgical risks.
w ith im paired m en tal stat u s, assessed by prospect ive cogn it ive
Th ese resu lt s con firm ed, in a p rosp ect ive fash ion , th at th e
assessm en ts, con t ribu t ing m u ch of th e m orbid it y. Th ese resu lts
n at ural h istor y of u n rupt ured an eur ysm s is st rongly depen den t
w ere in terpreted as suggest ing th at surgical risks far exceeded
on an eur ysm al size an d locat ion , an d th at , at least for sm all an -
th e n at u ral h istor y risk (over 7.5 years) for pat ien t s of grou p 1
eu r ysm s, associat ion w ith a p rior ru pt u red an eu r ysm im plies a
w ith un r upt ured an eur ysm s, an d th at associat ion of an un ru p -
h igh er risk of rupt ure of th e secon d an eu r ysm . Substan t ial risks
t u red an eu r ysm w ith p reviou s ru pt u re of an oth er an eu r ysm in
accom panying surgical or en dovascular in ter ven t ion s w ere also
th e sam e p at ien t , as w ell as an eu r ysm al size an d locat ion , w ere
con firm ed. Th e resu lt s of th e ISUIA im m ediately refram ed th e
im por t an t factors to con sider in determ in ing m an agem en t.
discu ssion s regarding th e p rop er m an agem en t of UIAs, p ar t icu -
Th e secon d p ar t of th e ISUIA provided, for th e first t im e, p ro-
larly for sm all an eu r ysm s. For t h e first t im e, solid dat a cou ld
sp ect ive n at u ral h istor y dat a regard ing UIAs, w h ich d em on -
guide m an agem en t decision s. Oth er st udies h ave con firm ed th at
st rated an overall rate of r u pt u re of 3%. As in th e ret rospect ive
posterior circulation aneurysm s portend sign ificantly greater risk
evalu at ion of un t reated an eur ysm s, th e risk of an eur ysm al rup -
of ru pt ure 5,6 ; on th e oth er h an d, in t racavern ous ICA an eu r ysm s
t u re w as fou n d to be st rongly p redicted by an eu r ysm al size an d
carr y a ver y ben ign SAH risk becau se th ey are seldom located in
locat ion . Un r u pt u red an eu r ysm s of less th an 7 m m in diam eter
th e subarach n oid space.7,8
rarely ru pt ured; th e rate w as sign ifican tly h igh er in th ose pa-
t ien ts w ith prior r u pt u re of an oth er an eu r ysm or in sm all an eu -
r ysm s of t h e p oster ior circu lat ion t h an in p at ien t s w ith ou t a Other Natural History Studies Examine
h istor y of SAH or th ose h arboring an eur ysm s in th e an terior cir-
culat ion (Table 62.1). In th e lat ter group, n o r upt ures occurred.
Inconsistencies and Limitations of the ISUIA
For an eu r ysm s ≥ 7 m m , th ere w ere n o sign ifican t differen ces in Several con cern s w ere raised abou t th e gen eralizabilit y of th e
rupt ure rates bet w een pat ien t s in group 1 an d th ose in group 2, ISUIA dat a. In p ar t icu lar, it w as rep eated ly obser ved t h at m ost
but th e overall risks of ru pt ure clim bed steeply w ith in creasing an eu r ysm s are in fact sm all at t h e t im e of r u pt u re.5 For an eu -
size, reach ing 40 to 50% over 5 years for gian t an eu r ysm s of di- r ysm s in th e an terior circulat ion th at w ere < 7 m m in diam eter,
am eter ≥ 25 m m (Table 62.1). th e ISUIA w ou ld h ave predicted a ru pt u re risk of zero (Fig. 62.1).

Table 62.1 Natural History Rupture Risks of Unruptured Intracranial Aneurysms (UIAs) in the International Study of
Unruptured Intracranial Aneurysms (ISUIA Parts 1 and 2), Stratified by Aneurysm Diameter3,4

ISUIA Part 1
(7.5-Year Risks) N < 10 mm 10–24 mm ≥ 25 mm

All group 1* 446 0.4% ~ 6% ~ 12%


All group 2* 438 ~ 4% ~ 5%

ISUIA Part 2
(5-Year Risks) N < 7 mm 7–12 mm 13–24 mm ≥ 25 mm

Anterior circulation (excludes cavernous 1037 Group 1: 0% 2.6% 14.5% 40%


carotid artery) Group 2: 1.5%
Posterior circulation (includes aneurysms 445 Group 1: 2.5% 14.5% 18.4% 50%
at posterior com municating artery) Group 2: 3.4%
*Groups 1 and 2 refer respectively to UIAs without and with prior history of SAH from another aneurysm in the same patient.

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750 V Cerebral and Spinal Aneurysms

a b

Fig. 62.1a,b A patient with a small cerebral aneurysm, 3 mm in maximum berry aneurysm (arrow). The aneurysm was extrem ely brit tle and blister-
diam eter, presented with sudden apoplectic catastrophic hemorrhage, like at surgery, with a rupture point in com m unication with the large hem a-
without prior warning. (a) Coronal computed tomography angiogram (CTA) tom a. The aneurysm was clipped, and the hem atom a was evacuated. If
reveals the sm all aneurysm (arrow) and massive intracerebral hem atom a. such an aneurysm was identified incidentally prior to rupture, it would have
(b) Three-dim ensional reconstruction of the sm all m iddle cerebral artery been predicted to have a zero risk of hemorrhage by the ISUIA data.

In effect , an eur ysm size alon e does n ot predict h ow th in th e w all low ed 419 patien ts w ith 529 IUAs w ith CTA ever y 6 m on th s for
of th e lesion , an d h en ce h ow brit tle an d vu ln erable to h em or- an average of 905 days, finding an annual rupt ure rate of 1.4%,
rh age a lesion m ay be (Fig. 62.2). In addit ion , th e select ion of and a cum ulative risk of 5.6%at 5 years.6 In depen den t risk factors
pat ien ts for in ter ven t ion s, n ot con t rolled by th e st u dy, m ay h ave for rupt ure in cluded histor y of prior SAH from anoth er an eur ysm ,
produced a group of patients w ith a m ore benign natural histor y posterior circulation aneur ysm location, and large aneurysm size,
than w ould h ave been obser ved in the overall group. con firm ing th e factors iden t ified in th e ISUIA. In th is st udy, h ow -
Oth er st u dies h ave con firm ed a greater an n ual risk of h em or- ever, th e an n ual rupt ure rate of sm all (less th an 5 m m in diam e-
rh age from UIAs, even in sm aller an eu r ysm s. Ish ibash i et al6 fol- ter) to m edium -sized (less th an 10 m m in diam eter) an eur ysm s

a b

Fig. 62.2a,b Incidental aneurysm s, 3 to 4 mm in diam eter, at the distal m atous parent artery. This older wom an had presented with recent-onset
anterior cerebral artery in t wo patients. (a) Atherom atous aneurysm, with headaches. Aneurysm s at distal arterial branches, with a high ratio of aneu-
a thick wall, was found at surgery, not likely vulnerable to im m inent bleed. rysm diam eter to parent artery diam eter, are thought to be m ore vulner-
This m iddle-aged man had presented with an unrelated ischemic stroke able to hem orrhage. In these cases, aneurysm size and shape alone (sm all
and heavy smoking history. (b) A sim ilarly sized 2- to 3-m m aneurysm , per- and without daughter sac lobulation in both cases), would not differentiate
fectly round but extremely brit tle and thin walled arising from an athero- the thin-walled lesion as being m ore vulnerable to a hem orrhage risk.

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62 Incidental Aneurysm s 751

w as som ew h at h igh er (rate 0.8% per an n u m for sm all an d 1.2%


for m edium -sized an eu r ysm s). Of th e eigh t sm all (3–4 m m ) an -
■ Practical Decision Making
eu r ysm s th at ru pt u red, fou r w ere in th e p osterior circu lat ion , Neurology Perspective
t w o of w h ich w ere in pat ien ts w ith SAH h istor y. How ever, th e
rem ain ing fou r sm all an eu r ysm s th at rupt u red w ere in th e an te- For th e in cid en t ally d iscovered sm all u n r u pt u red an eu r ysm ,
rior circu lat ion an d in pat ien ts w ith ou t a h em orrh age h istor y, w orking from th e foun dat ion of th e ISUIA data, th e decision re-
u n derm in ing th e reassu ran ce p rovided by th e ISUIA dat a for garding m an agem en t m ay seem fairly sim ple. Th e ISUIA invest i-
su ch an eu r ysm s. Th e au th ors con clu ded th at alth ough an eu r ysm gators con clu ded th at th e risks associated w ith surger y “greatly
size, h istor y of SAH, an d p osterior circu lat ion locat ion are pre- exceed ed ” t h e n ear-ter m r isks of r u pt u re of a sm all an eu r ysm
dictors of ru pt u re, size alon e sh ou ld n ot be taken as th e fin al in p at ien t s w it h ou t p reviou s an eu r ysm al r u pt u re. Su bsequ en t
determ in an t regarding th e decision for t reat m en t . qu an t it at ive m od elin g of t h e r isk/ben efit rat io 18,19 su p p or ted
An oth er n at u ral h istor y st udy from Fin lan d by Juvela et al9 t h is con clu sion , an d exper t gu idelin es from th e Am erican Hear t
follow ed 181 un rupt ured an eur ysm s over 2,575 person -years, Associat ion (AHA) h ave con cu rred as w ell, con clu ding th at in ci-
an d con clu ded th at UIAs carr y a 1.3% an n u al risk of r u pt ure. Th e den tal sm all an eu r ysm s in p at ien ts w ith ou t p reviou s SAH are
st u dy defin ed a cu m u lat ive risk of 10.5% at 10 years, 23% at 20 appropriately m anaged m edically.1 For sm all uncom plicated UIAs,
years, an d 30.3% at 30 years after diagn osis. Alth ough an eu r ysm par t icu larly th ose an eu r ysm s u n der 7 m m in size, th is p refer-
size w as also a risk factor for h em orrh age (relat ive risk 1.11 p er en ce for m edical m an agem en t sh ou ld st ill be th e st art ing p oin t
m illim eter in diam eter), th ere w as n o size th resh old protect ing for m an agem en t discussion s.
from r u pt u re, an d 17 of 33 first -t im e ep isodes of h em orrh age But m edical t reat m ent sh ou ld n ot be equated w ith no t reat-
from UIAs w ere fat al. In th is st u dy, you nger age an d cigaret te m ent. Sm oking, h eavy alcoh ol u se, an d hyper ten sion are im por-
sm oking w ere also sign ifican t risk factors of r u pt u re. Oth er st u d- tan t risk factors for SAH an d for an eur ysm al grow th , an d th ese
ies h ave also iden t ified you nger age, fem ale sex, hyperten sion , factors sh ould be aggressively addressed. Alth ough specific ben -
an d cigaret te sm oking as addit ive risks of ru pt u re in UIA.10,11 efit s to an eu r ysm m an agem en t of t reat in g ot h er vascu lar r isk
factors are un cer tain , th ese n eurovascu lar pat ien ts sh ould also
be su bject to careful m an agem en t of dyslipidem ia, diabetes, an d
lifest yle factors th at im p act vascular disease. Fin ally, a plan for
Aneurysm Grow th and Daughter Sacs as a Risk prospect ive m on itoring of th e UIA is n ecessar y (see below ).
of Rupture
A ret rospect ive an alysis by Yasui et al12 of 25 cases of ru pt ure of
Factors in Decision Making
con ser vat ively m an aged UIAs fou n d th at in 16 cases t h e size of
th e an eu r ysm at in it ial diagn osis w as < 5 m m . How ever, in m ost Alth ough in ter ven t ion s m ay n ot be gen erally in dicated for sm all
cases, th e diam eter at th e t im e of ru pt ure w as greater t h an th e UIAs, several factors m ay poten t ially in fluen ce th e “sim ple” deci-
diam eter at in it ial diagn osis. Mat su bara et al13 exam in ed th e sion regarding m an agem en t of an u n r u pt u red an eu r ysm . Th e
grow th of UIAs using serial CTAs an d iden t ified grow th in 16.4% ISUIA dat a, as w ell as su bsequ en t st u d ies, h ave clearly d ocu -
of 166 an eur ysm s follow ed, w ith 2.4% grow th in an eur ysm s m en ted t h e h igh r isk of r u pt u re of large an eu r ysm s of greater
m easu ring 2 to 4 m m , 9.1% in an eu r ysm s m easu ring 5 to 9 m m , t h an 10 to 12 m m d iam eter, an d if su rgical or en d ovascu lar
an d 50% in an eur ysm s m easuring 10 to 20 m m . Ch anges w ere obliterat ion can be safely ach ieved, su ch in ter ven t ion al t reat-
m ore frequ en tly fou n d in an eu r ysm s located at th e basilar ar ter y m en t w arran ts a st rong recom m en dat ion . How ever, for sm all to
bifu rcat ion an d th e in tern al carot id arter y. Using serial MRA, m edium -sized an eur ysm s larger th an 2 m m but less th an 10 m m
sim ilar resu lt s w ere rep or ted by Bu rn s et al.2 In th eir series 10% in d iam eter, a ran ge t h at in clu d es t h e large m ajor it y of in ci-
of 191 lesion s grew over a m edian follow -up period of 47 m on th s, d en tally discovered an eur ysm s, th e decision can be substan t ially
an d th e frequen cy of en largem en t w as 6.9%, 25%, an d 83% for m ore com plex. Beyon d th e clear in fluen ce of an eur ysm size on
an eur ysm s < 8 m m , 8 to 12 m m , an d >12 m m , respect ively. Th e rupt ure rate, factors such as pat ien t age, an eur ysm locat ion , an -
st u dy by So et al14 repor ted an even h igh er frequen cy of an eur ys- eu r ysm sh ap e, sym ptom s, an d pat ien t p referen ce m u st all be
m al grow th , of one-th ird of 285 an eur ysm s in 208 pat ien ts fol- con sidered, as w ell as accom p anying p at ien t con d it ion s th at m ay
low ed for a m ean of 21.8 m on th s. In th e first year alon e, 22.7%of affect the patient’s life expectancy and treatm ent outcom es. With
an eur ysm s en larged, an d th e m ean t im e to docum en tat ion of in clusion of th ese con siderat ion s, th is “sim p le” decision can rap -
grow th w as 15.9 m on th s. In th is series, 42.5%of an eur ysm s w ere idly becom e rath er com plex.
t reated by clipp ing or coiling. Perh ap s becau se of th is h igh rate of
in ter ven t ion , grow th did n ot p redict ru pt u re; on ly th ree of th e
Patient Age and Risk Factors
285 an eur ysm s r upt ured, an d on ly on e of th ese h ad grow n prior
to rupt ure. Th e only factor in depen den tly predict ing grow th w as With m edical m an agem en t , you ng p at ien ts presen t ing w ith UIA
excess alcoh ol con sum pt ion . m ust an t icipate m any decades of sur veillan ce. Sh ould a rupt u re
Along w ith size, locat ion , an d grow th rate, an oth er ch aracter- occur, th e result ing m orbidit y w ill be carried over m any years,
ist ic th at in flu en ces th e ru pt ure rate of an UIA is its m orph ology. alth ough th e sam e applies to any m orbidit y in curred w ith an in -
Several st u dies h ave con clu ded th at m u lt ilobu lated an eu r ysm s, ter ven t ion . With th e low er procedural risks in young pat ien ts,
th ose w ith daugh ter sacs, an d th ose w ith a h igh an eu r ysm -to– th ese h igh er lifet im e cu m u lat ive risks of con ser vat ive m an age-
paren t vessel diam eter rat io are all associated w ith in creased m en t favor st rong con siderat ion of defin it ive t reat m en t of sm all
rupt u re rate.15–17 to m edium -sized an eur ysm s in th is populat ion . An eur ysm s th at

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752 V Cerebral and Spinal Aneurysms

are already of m edium size at th e t im e of discover y, in addit ion sym ptom s prior to SAH an d fou n d th at 74% exp erien ced h ead,
to h aving a h igh er rate of r u pt u re in t h e sh or t ter m , sh ow a eye, or n eck pain in th e h ours leading up to th e recogn ized an eu-
h igh er rate of en largem en t over t im e, an d m ay be st rong can di- r ysm al rupt ure, an d a m in orit y of pat ien ts also reported visual,
dates for in ter ven t ion in you ng h ealthy p at ien t s. For elderly or m otor, an d sen sor y dist u rban ces during th is t im e period. Such
m edically com prom ised pat ien ts in w h om surgical an d en dovas- p at ien t s p resen t a d ilem m a as to w h et h er t h e h eadach e m ay
cular risks are excessive, a decision for m edical m an agem en t an d relate to an eur ysm al grow th an d rem odeling, im plying sin ister
an eur ysm m on itoring is m ore advan t ageou s. sign ifican ce, or rath er are t ru ly in ciden t al an d sh ou ld n ot in flu -
en ce th e m an agem en t of th e an eu r ysm . Clin ical ju dgm en t , an d a
judiciou s skept icism of easy con clusion s, is n eeded in such cases.
Aneurysm Location, Shape, and Association w ith Prior
Ruptured Aneurysm
Carotid Revascularization and Unruptured
As w as review ed previou sly, posterior circu lat ion an eu r ysm s,
Intracranial Aneurysm
an eu r ysm w ith lobu lat ion s an d daugh ter sacs, larger an eur ysm -
to–paren t vessel diam eter rat io (as seen w ith distal an eur ysm s Kap pelle et al23 review ed dat a from th e Nor th Am erican Sym p -
arising from t iny bran ch es) (Fig. 62.2), an d any UIA w ith dem on - tom at ic Carot id En dar terectom y Trial (NASCET) an d foun d 90
st rated grow th (Fig. 62.3) sh ou ld p rom pt st ronger con siderat ion pat ien ts w ith sym ptom at ic carot id sten osis an d UIAs, alm ost all
for t reat m en t regardless of size. Th e decision an d th resh old for of th em sm aller th an 10 m m in diam eter. On ly on e of th e 90 pa-
act ual in ter ven t ion sh ould con sider th e pat ien t’s preferen ces t ien ts exp erien ced an eu r ysm al ru pt u re, 6 days follow ing carot id
an d oth er risk factors n oted previously. In ad dit ion , th e presen ce en dar terectom y, an d in t h ese 90 p at ien t s t h e m arked ben efit s
of m u lt iple in t racran ial an eur ysm s m ay afford th e oppor t un it y of en dar terectom y over m ed ical t h erapy for st roke p reven t ion
to th e neurosurgeon or inter vention alist of elim inating m ore th an m atch ed th ose of th e overall NASCET populat ion . Th e auth ors
on e an eu r ysm in th e sam e proced ure. Fin ally, th e con firm ed 10- recom m en d m oving ah ead w ith en darterectom y for sym ptom -
fold h igh er risk of ru pt u re for sm all an eur ysm s in pat ien ts w ith at ic carot id stenosis, regardless of th e p resen ce of UIA. Th e n eed
previou s r u pt u red an eu r ysm , th e ISUIA’s grou p 2 p at ien t s, re- for carot id en dar terectom y sh ould n ot be taken as an in depen -
qu ires th at greater con siderat ion for in ter ven t ion be offered in den t factor favoring an eu r ysm in ter ven t ion . Decision s are often
th ese cases of sm all in ciden t al an eu r ysm s, p ar t icu larly in you ng m ore com plicated in patients in w hom the carotid stenosis is se-
pat ien ts. vere but asym ptom atic, and the aneur ysm m ay be sym ptom atic,
h as dem on st rated grow th , or is of sufficien t size or m orph ology
to w ar ran t t reat m en t . In su ch cases, in d ivid u alized d ecision s
Significance of Symptoms
abou t st aging of t reat m en t are often un der t aken .
Th e occu rren ce of sym ptom s associated w ith a UIA su ch as cra-
n ial n er ve com pression or m ass effect h as gen erally been taken
Patient Preference
to suggest an eur ysm al grow th , th reaten ing im m in en t rupt u re,
and a clear indication for aneur ysm obliteration.1 Sym ptom s from Pat ien t preferen ce m u st also be con sidered. Th e kn ow ledge of
su spected th rom boem bolism from an an eu r ysm h ave also been a life-th reaten ing lesion in on e’s h ead can produce con siderable
con sidered a reason for in ter ven t ion .1 an xiet y, esp ecially am ong h eadach e sufferers or pat ien t s w ith a
More com m on ly, h ead ach e is t h e sym ptom accom p anyin g fam ily h istor y of an eur ysm r u pt ure. Som e p at ien t s w ould prefer
UIAs. In th e first par t of th e ISUIA, h eadach e w as th e reason for to con fron t an up -fron t risk w ith an in ter ven t ion rath er th an en -
th e in it ial brain scan th at disclosed th e UIA in 36% of th e p a- dure the un certain t y an d psychic burden of w aiting an d w atch ing.
t ien ts, an d as h igh -resolu t ion m agn et ic reson an ce im aging (MRI) Th e econ om ic an d h ealth bu rden of m on itoring an u n ru pt u red
scan n ing h as proliferated, th is p ercen t age w ou ld on ly h ave in - an eur ysm over t im e m ust also be w eigh ed. For som e, a con clu -
creased. Most often th e an eur ysm is t ruly in ciden tal, an d n ot sive disp osit ion w ou ld h old valu e, even if carr ying risks of m or-
causal, to th e h eadach e. Never th eless, several st u dies h ave ob - bidit y up fron t , equ ivalen t to th ose dist ributed over decades of
ser ved su bst an t ial im p rovem en t in p at tern s of ch ron ic h eadach e t im e w ith con ser vat ive m an agem en t .
w ith an eu r ysm coiling or clipping.20,21 Qu est ion s rem ain as to
w h eth er th ese obser ved im provem en t s are m ore likely due to a
Monitoring of Unruptured Intracranial Aneurysms:
placebo effect rath er th an to a path op hysiological relat ion sh ip of
Practical Recommendations
th e h eadach es to th e an eu r ysm , an d gen erally, th e p resen ce of a
h eadach e sh ould n ot be con st r ued as a st rong reason for in ter- After in itial discovery of an UIA, if m edical m anagem ent is chosen ,
ven t ion in an UIA. n on invasive m on itoring sh ou ld be un der taken . Th ere is a cum u-
A clear except ion m ust be m ade for a severe, sudden h ead- lat ive risk an d n o added ben efit of rep eated cath eter angiogra-
ach e of th e th un derclap t ype. Such a sen tin el h eadach e can often phy in th e m ajorit y of cases w ith UIAs. Th e ch oice of m odalit y of
represen t a sm all h em orrh age, an eu r ysm w all dissect ion or re- im aging can be based on local p referen ce an d exper t ise. Eith er
m odeling, or ar terial vasospasm , an d in dicates a n eed to regard MRA or CTA can be effect ive, n on invasive m odalit ies for detec-
th e an eu r ysm as p ossibly sym ptom at ic an d in n eed of u rgen t tion of expansion of size of a know n aneurysm . In part icular, high
evalu at ion for poten t ial t reat m en t . In addit ion , occasion ally pa- field st rength MRA ach ieves in t racran ial vascu lar im aging w ith
t ien t s p resen t w ith a n ew, u n u su al p ersist ing h eadach e, w ith ou t h igh resolu t ion an d reliabilit y, w ith ou t exposure to ion izing ra-
a prior sim ilar h eadach e pat tern , an d a UIA is discovered, per- diat ion or to in t raven ou s con t rast agen t s.
h aps in th e sam e cran ial locat ion as th e h eadach e. Sam ejim a et Th e optim al schedule of im aging is not w ell established. A rea-
al22 quest ion ed 92 pat ien ts w ith SAH regarding th eir subject ive son able approach is to obtain one early follow -up vascular im age

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62 Incidental Aneurysm s 753

Fig. 62.3a–c A m iddle-aged m an with incidental left m iddle cerebral ar-


tery unruptured intracranial aneurysm (UIA). (a) Aneurysm at presentation
on computed tom ography angiogram (CTA) with calcification and broad
neck, maxim um diam eter 11 × 7 m m , with lobulations. (b) The three-
dim ensional reconstruction of the aneurysm showed a fusiform dilation of
the M2 segm ent with a saccular eccentric aneurysm al bulge. Close follow-
up was initially elected, with im aging planned at 6 m onths and then yearly,
or sooner if new symptom s arose. (c) At the 1-year im aging (CTA) follow-
up, the aneurysm was noted to have enlarged to 14 × 9 m m . The patient
had at tempted to optim ize vascular risk factors and was asymptom atic.
Surgical intervention was now recom m ended, but the patient was hesitant,
so we urged a follow-up visit in the presence of his spouse, to discuss the
aneurysm enlargement. On the day prior to the scheduled follow-up the
patient suffered a rupture from the aneurysm under surveillance. The sac-
cular bulge of the aneurysm , which was the source of hem orrhage, was
surgically clipped em ergently, and the patient survived, but with significant
neurologic disabilit y. c

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754 V Cerebral and Spinal Aneurysms

w it h t h e ch osen m odalit y of m on itoring w it h in 3 to 6 m on t h s palsy or m ore severe h eadach e localizable to th e region of th e


of th e in it ial detect ion of an un ru pt ured an eur ysm , to est ablish a an eur ysm , w arran t an urgen t con siderat ion for t reat m en t of UIA.
baselin e w ith th e ch osen m odalit y an d to screen for any rapid
en largem en t . Th ereafter, an n u al st u d ies sh ou ld be con d u cted
Management Strategies and Outcome :
for at least 3 years. W h eth er th e frequen cy of m on itoring can be
Microsurgical Clipping
safely redu ced after establish ing an in it ial p eriod of stabilit y is
n ot kn ow n . Given t h e cost an d bu rd en of yearly m on itor ing, it In m ost cases, invasive catheter cerebral angiography is not needed
m ay be reason able to d ecrease t h e frequ en cy of n on invasive to assess an eur ysm size, locat ion , recen t grow th , or relevan t
m on itoring to on ce ever y 3 years, part icularly w ith sm aller UIAs, m orph ological feat ures (lobulat ion s, daugh ter sac, calcificat ion s)
to be con t in ued for as long as th e pat ien t w ould be a can didate prior to su rgical in ter ven t ion . Oth er relevan t in form at ion , su ch
for in ter ven t ion . as precise n eck diam eter, perforator angioarch itect ure, an d ath -
erom atou s ch ange are best assessed at surger y. In experien ced
h an ds, sim ilar ou tcom es of surger y for UIAs h ave been repor ted
Neurovascular Surgery Perspective w h en guided by h igh -qualit y CTA alon e.25 On th e oth er h an d, al-
Pract ical decision m aking for t reat m en t of UIA from a n eurovas- th ough MRA h as been sh ow n to provide sim ilar in form at ion to
cular surgeon’s perspect ive is alw ays a balan cing act bet w een CTA for detect ing an d m on itoring an eur ysm s, it t ypically offers
risk of su rger y an d ben efit of t reat m en t in a disease w ith an u n - less an atom ic resolu t ion to gu ide su rgical in ter ven t ion .26 At th e
cer t ain n at ural h istor y. Microsu rgical clip p ing offers th e greatest auth ors’ cen ter, CTA is used to guide th e vast m ajorit y of t reat-
cer t ain t y of defin it ive t reat m en t by excluding an an eur ysm from m en t decision s an d surgical plan n ing for UIAs. Cath eter cerebral
th e circulat ion . In a popu lat ion -based st u dy, Brit z et al24 evalu- angiography is n ot perform ed rout in ely prior to surger y for UIAs,
ated th e long-term su r vival of p at ien ts w ith an eu r ysm s u n der- u n less a specific qu est ion arises abou t diagn osis (an eur ysm ver-
going clipping by review ing th e clin ical course of 4,619 pat ien ts su s in fu n dibu lu m ), or in th e cou rse of assessing en dovascu lar
h ospitalized w ith cerebral an eur ysm s, an d foun d th at surgical opt ion s. Th is approach can ach ieve subst an t ial risk an d cost re-
clipp ing of UIAs w as associated w ith both sign ifican tly h igh er du ct ion in th e t reat m en t of UIAs.
su r vival est im ates (h azard rate of death , 30%; p < 0.001) an d sig-
n ifican tly less n eu rologically related causes of death (5.6 vs 2.3%;
Surgical Adjuncts
p < 0.001).
Factors p reviou sly discu ssed, in clu d ing th e p at ien t’s age, an - A det ailed con siderat ion of surgical adjun cts is beyon d th e scope
eu r ysm size, locat ion , m orp h ology, an d prior h em orrh age from of th is ch apter, but th ese factors are crit ical to ach ieving th e best
an oth er an eu r ysm , all in fluen ce th e th resh old of t reat m en t. Pa- su rgical ou tcom e w ith th e least risk. In gen eral, m ost an eu r ysm s
t ien t p referen ces are taken in con siderat ion , in clu ding lifest yle, at th e circle of Willis an d m iddle cerebral ar ter y (MCA) are ap -
w illingn ess or abilit y to follow th e lesion regu larly, an d the psy- proach ed via m odificat ion s of th e fron totem p oral pterion al cra-
ch ological im p act in h eadach e su fferers an d in p at ien t s w ith n iotom y, w ith flush exp osu re an d th e fron t al base an d radical
fam ily m em bers w h o su ffered an eu r ysm ru pt u re. resect ion of th e lesser w ing of t h e sph en oid. Wide split t ing of
Many of th e sam e factors, n ot ably th e p at ien t’s age, an eu r ysm th e sylvian fissu re is don e, avoiding th e u se of lu m bar cerebro-
size, an d locat ion , also in flu en ce th e t reat m en t risks. Medical co- spin al fluid drain age or prolonged m ech an ical ret ract ion . Orbito-
m orbidities are thoroughly assessed and optim ized prior to treat- zygom at ic rim resect ion an d oth er skull base approach es are n ot
m en t , w h ere th e in ter ven t ion is t yp ically n on u rgen t . Sign ifi- deployed routin ely by m any experienced neurovascular surgeons,
can tly greater m orbidit y is associated w ith th e su rgical t reat m en t reser ving th ese tech n iques for selected cases such as h igh lying
of large or gian t an eu r ysm s, an d th ose w ith m ural calcificat ion s or gian t an eur ysm s, an d th ose at som e posterior fossa locat ion s
of th e an eu r ysm or adjacen t p aren t ar ter y.4 Th ese factors are (t ran scon dylar for ver tebral ar ter y–posterior in ferior cerebellar
w eigh ed in can did discu ssion w ith th e pat ient , t aking in to con - ar ter y an eu r ysm s; presigm oid for m idbasilar t r un k an d an terior
siderat ion pu blish ed resu lt s of su rgical in ter ven t ion an d th e su r- inferior cerebellar artery aneurysm s). CTA im age guidance is used
geon’s ow n experien ce an d outcom es w ith sim ilar lesion s. in t raop erat ively for m ore distal m iddle cerebral an d an terior ce-
More difficu lt or su rgically risky an eu r ysm s are also con sid- rebral arter y an eu r ysm s, en abling opt im izat ion of flap design
ered for en dovascu lar t reat m en t . On e m u st art icu late th e low er an d m ore focused an d safer exposure st rategies.27 En dovascular
ch an ce of du rable cu re an d greater risk of h em orrh age w ith en - or open su rgical proxim al con t rol is prepared at the cer vical ca-
dovascu larly t reated UIAs, th an after su rgical clip ping. Th e su r- rot id arter y for any p araclin oid an eu r ysm w h ere drilling of th e
geon m ust also em ph asize th e n eed for m ore judicious follow -up clin oid p rocess or op en ing of th e du ral ring m igh t be n eed ed
and the higher likelihood of retreatm ent w ith endovascular treat- (open ing of th e falciform ligam en t alon e is sufficien t for th e safe
m en t (see below ). Less experien ced su rgeon s sh ou ld con sider clip ping of m any sm aller op h th alm ic ar ter y an eu r ysm s). An eu -
referral of pat ien t s w ith UIAs to h igh er volu m e cen ters, or sh ou ld r ysm s n ear rich ban ks of perforators are gen erally approach ed
perform th e p rocedu re w ith a m ore experien ced colleagu e to op - w ith a lateral to m edial angle of view, so as to directly view an d
t im ize t reat m en t ou tcom e. Th e st rategy of expect an t follow -u p sw eep aw ay perforators.
an d un cer tain t ies about risks an d th eir con sequen ces are also In t raop erat ive elect roen cep h alograp hy an d som atosen sor y
discu ssed w ith th e p at ien t . All poten t ial com plicat ion s an d re- evoked p oten t ial m on itor ing is u sed w h en ever p ossible, facili-
cover y scen arios from su rgical in ter ven t ion , or from a p oten t ial t at ing brain protect ion an d alert ing th e su rgeon to occult isch -
h em orrh age in un t reated or subopt im ally t reated cases, are re- em ic insults or other injuries.28 Tem porar y clip application is used
view ed . Recen t grow th an d n ew sym ptom s, such as cran ial n er ve w it h ou t h esit at ion , esp ecially w it h larger lesion s. Tan d em an d

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62 Incidental Aneurysm s 755

in terlockin g clip st rategies an d sp ecial fen est rated clip s h ave an eur ysm s, good in 3.7%, an d poor in 3.7%, on e pat ien t died. An -
evolved a great d eal, an d th ese are u sed read ily an d creat ively oth er sim ilar st u dy looked at th e clip ping of 103 UIAs in pat ien t s
to ach ieve p erfect an eu r ysm n eck recon st ru ct ion w h ile preser v- older t h an 70 years of age an d con clu d ed t h at su rger y for elec-
ing p aren t arter y bran ch es.29 Min i-clip s are u sed to rein force t ive UIAs in t h e eld erly sh ou ld be con sid ered in sym ptom at ic
(“pin ch ”) residual “dog-ears.” In t raoperat ive verificat ion of an - p at ien t s w ith sim ple an eur ysm s th at can be clipped w ith out th e
eu r ysm obliterat ion an d th e preser vat ion of relevan t vessels are u se of tem porar y clips.35 Becau se on e of th e m ajor in dicat ion s
aided by sac p u n ct u re, circu m feren t ial m icrosu rgical exp lora- for t reat m en t of UIA is to preven t rupt ure, an d because an older
t ion , m icro -Dop p ler in son at ion , an d , m ore recen t ly, in d ocya- age at presen tat ion im p lies a sh or ter period of risk, th e in creased
nine green videoangiography.30 In traoperative an d postoperat ive su rgical m orbid it y rate is p ar t icu larly im p or t an t , favor ing ex-
cath eter angiograp hy is n ot n ecessarily or rou t in ely dep loyed, p ect an t m ed ical m an agem en t for sm aller, st able an eu r ysm s in
except in p ar t icu larly ch allenging cases. old er p at ien t s.
An eur ysm factors like size, m orph ology, an d specific locat ion
con t r ibu te to su rgical ou tcom e. Gian t an eu r ysm s requ ire sp e-
Management Outcome
cialized su rgical an d adju n ct ive tech n iqu es 36,37 an d car r y t h e
Th e u lt im ate goal of th e t reat m en t of UIAs is com p lete an d du - greatest risk, w ith ap proxim ate m or t alit y an d m orbidit y rates as
rable exclu sion of t h e an eu r ysm from th e circulat ion . Microsur- h igh as 20%an d 50%, respect ively, for posterior circulat ion an eu -
gical clipping accom plish es th at goal in 90 to 95%of cases w ith a r ysm s. Several st udies h ave reported th at an eur ysm size st rongly
ver y low recurren ce rate.31 How ever, t h e ben efit of t h e su rger y cor related w it h su rgical m orbid it y an d m or t alit y rates, w it h
h as to be balan ced again st th e risks associated w ith th e surger y sm aller an eu r ysm s associated w ith bet ter rates.33,36 An eu r ysm s
an d r isks an d ben efit s of ot h er t reat m en t st rategies like en d o - w ith large ill-defin ed or fusiform n ecks, th ose arising from ath -
vascular coiling an d obser vat ion . A w ide range of m or talit y an d erosclerot ic or ect at ic vessels, th ose th at in corp orate m ajor in -
m orbidit y rates associated w ith surger y h as been reported, var y- t racran ial bifu rcat ion s, an d th ose located p ar t ially w ith in th e
ing from 0 to 7% for m or talit y an d 4 to 15.3% for m orbidit y.1 In a cavern ou s sin u s or arising from th e m id por t ion of th e basilar
m et a-an alysis by King et al32 of data on 733 pat ien ts, th e auth ors ar ter y h ave a less w ell-defin ed n at ural h istor y, an d all require
con clu ded th at elect ive su rger y for asym ptom at ic UIAs h as low special tech n iques an d m ay be associated w ith in creased surgi-
rates of m orbidit y (4.1%) and m ort alit y (1.0%). An oth er sim ilar cal m orbidit y rates.1 As a group , an eu r ysm s arising in th e poste-
m et a-an alysis by Raaym akers et al33 involving 2,460 pat ien ts re- rior circu lat ion h ave been th ough t to pose a greater surgical risk
por ted a low su rgical m or t alit y rate of 2.6% an d a m orbidit y rate th an th ose in th e an terior circu lat ion . An eu r ysm s at t h e basilar
of 10.9%. How ever, n on e of t h e st u d ies con t ain ed a su fficien t ap ex are in t im ately associated w it h brain stem an d t h alam ic
n um ber of pat ien ts to w arran t draw ing a con clusion regarding p er forat ing ar teries, an d th ese can be injured du ring open sur-
th e predictors of ou tcom e after su rger y. Th e ISUIA rep or ted on ger y 38 or w ith en dovascular procedures.39 In th e m et a-an alysis
t w o grou ps t reated w ith cran iotom y for UIAs: pat ien ts w ith an d by Raaym akers et al,33 posterior circulat ion an eur ysm locat ion
pat ien ts w ith ou t a p rior h istor y of SAH. In 798 p at ien ts w ith ou t w as associated w ith th e h igh est su rgical risk, p ar t icu larly for
a p r ior SAH, m or t alit y rates w ere 2.3% at 30 days an d 3.8% at gian t an eu r ysm s, for w h ich th e m ortalit y rate w as 9.6% an d th e
1 year, w h ereas in t h ose w it h a p rior SAH from a t reated an eu - m orbidit y rate w as 37.9%. A recen t ret rospect ive an alysis of 157
r ysm , m or t alit y rates w ere 0% at 30 days an d 1% at 1 year. In UIAs t reated w ith open surgical clipping reported th at size by
ad dit ion , both pat ien t groups w ere foun d to h ave n eu rologic it self did n ot h ave an adverse affect on ou tcom e; h ow ever, th e
m orbidit y rates of 12%at 1 year, w h ich in clu ded disabilit y due to presen ce of calcificat ion in an an eu r ysm w as th e sole m arker of
m ajor cogn it ive im pairm en t .3 Th e factors in flu en cing su rgical adverse outcom e.40 Larger an eu r ysm s are m ore likely to be calci-
outcom e can be grouped in to pat ien t ch aracterist ics (age, sym p - fied , an d clip p in g or clip recon st r u ct ion of calcified an eu r ysm s
tom s, an d m edical con dition), an eur ysm ch aracteristics (size, lo- is a sign ifican t source of m orbidit y in th e t reat m en t of un rup -
cat ion , an d m orph ology), an d oth er factors (h ospit al an d su rgical t u red an eu r ysm s.40 Never th eless, as experien ce w ith m icrosur-
team experien ce). Each of th ese factors sh ou ld also be con sid- gical tech n iques in creases, an eur ysm locat ion m ay becom e less
ered in th e assessm en t of t reatm en t altern at ives. More recen tly, of a factor in in fluen cing outcom e. In deed, several st udies from
m an agem en t m orbidit y an d m ort alit y after t reat m en t of UIAs exp erien ced cen ters h ave rep or ted lit tle or n o in crease in m or-
h as d ecreased sign ifican tly.24 Th is is in p ar t du e to bet ter p at ien t bidit y rates due to focal n eurologic deficit s in cases of n on -gian t
select ion , su rgical experien ce an d adju n cts, an d poten t ially th e an eur ysm of th e p osterior circu lat ion .37,41
region alizat ion of t reat m en t in h igh er volum e cen ters.
Age is clearly an im por t an t pat ien t factor th at in fluen ces su r-
Surgical Experience and Patient Referral Patterns
gical outcom e as illu st rated by th e ISUIA. In th is st udy, th e com -
bin ed m orbidit y an d m or talit y rate w as 6.5% for pat ien ts < 45 Su rgical experien ce h as been sh ow n to in flu en ce ou tcom e after
years of age, 14.4% for pat ien ts 45 to 64 years of age, an d 32% for in t racran ial an eu r ysm surger y. In a st udy of in -h ospit al death s
pat ien ts ≥ 65 years of age.3 Age is often a su rrogate m arker for after cran iotom ies perform ed for UIA bet w een 1987 an d 1993 in
oth er m edical com orbidit ies th at in creases th e risk of surgical New York St ate h osp it als, th ere w as a 53% decrease in m ort alit y
in ter ven t ion ; h ow ever, w ith advan ces in m edicin e an d an in - rate w h en th e 21 h ospit als th at each perform ed ≥ 10 cran ioto-
crease in th e size of th e h ealthy aging populat ion , th is pict ure is m ies per year w ere com pared w ith th e 89 h ospitals th at each
boun d to ch ange. Ju ng et al34 publish ed a single-cen ter experi- perform ed < 10 cran iotom ies p er year (5.3% vs 11.2% m ort alit y
en ce in su rgical t reat m en t of 54 UIAs in pat ien t s bet w een 70 an d rate, respect ively). Th e m ajorit y of New York St ate h ospit als w ere
78 years of age and reported 3-m onth excellent outcom es in 92.6% fou n d to rarely perform an eur ysm surgeries, an d th ose h ospitals

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756 V Cerebral and Spinal Aneurysms

h ad m ore th an t w ice th e in -h ospit al m or talit y rate.42 An oth er cern about low er obliterat ion rates an d h igh er rates of bleeding
st u dy from New York St ate exam in ing th e im p act of h osp it al an d ret reat m en t after coiling th an after su rgical clip p ing. In a
ch aracterist ics on ou tcom e after th e t reat m en t of ru pt u red an - system at ic review of pu blish ed rep or ts, com p iled by Lan tern a et
eur ysm s and UIAs found that hospital volum e had m ore of an ef- al,50 p roced u re-related m or t alit y an d m orbidit y of en dovascu lar
fect on outcom e after aneur ysm clipping than after endovascular coiling w as 0.6% an d 7%, respect ively, in th e sam e range as th at
th erapy. Th is st u dy m ade a case for a p rogram of regionalizat ion rep orted w ith su rgical clipping. Procedural m orbidit y after coil-
an d select ive referral for th e t reat m en t of cerebral an eur ysm s.43 ing has been less related to age 4 an d also less related to in st it u -
In a n at ionw ide st u dy of 3,498 p at ien t s t reated for UIAs bet w een t ion al volu m e of exp erien ce th an is m icrosurger y.51 How ever,
1996 an d 2000 looking at th e risk of adverse outcom e after sur- rebleeding rates h ave been reported con sisten tly aroun d 0 to
gical t reat m en t of UIAs, Barker et al44 con cluded th at surger y 2.6%(m ean 0.9%) per year after coiling of UIAs,50 m ostly in larger
p er for m ed at h igh -volu m e in st it u t ion s or by h igh -volu m e su r- in com pletely coiled an eu r ysm s. Th is is a rate sim ilar to th e n at u-
geon s w as associated w it h sign ifican t ly low er m orbid it y an d ral h istor y of m any UIA lesion s 9 an d m u ch low er th an rep or ted
m odestly low er m or t alit y. How ever, h igh volu m e alon e is n ot a long-term rates after m icrosurgical clipp ing.52
n ecessar y criterion for favorable ou tcom es of t reat m en t of UIAs, Th e p at ien t -associated factors su ch as old age, cardiovascu lar
an d good results h ave been repor ted by experien ced su rgeon s in disease, an d m edical com orbidit ies w ill t ypically ju st ify exp ect-
som e low -volu m e set t ings.45 In creasingly, p at ien ts an d in surers an t m edical th erapy rath er th an eith er surgical or en dovascular
w ill be dem an ding th at surgical experien ce in fluen ce w h ere an d in ter ven t ion . How ever, larger or grow ing an eur ysm s in such pa-
by w h om an an eur ysm is t reated . t ien t s can be d eter m in in g factors for recom m en d in g en d ovas-
cu lar coiling for an UIA, becau se th ese factors less likely im pact
en dovascular procedu ral m orbidit y.4
Endovascular Perspective, Strategies, An eur ysm factors play an im por tan t role in con sidering po-
tent ial en dovascular th erapy. Tradit ion ally, a favorable an eu r ysm
and Outcome for en dovascu lar coiling h as been iden t ified as h aving a n arrow
Sin ce th e p u blicat ion of th e resu lt s of th e In tern at ion al Su b - an eur ysm n eck w ith a n eck-to-dom e rat io of less th an 0.5.53
arach n oid An eur ysm Trial (ISAT), w ith favorable outcom e of en - Wide-n ecked an eu r ysm s h ave n ot been con sidered good can di-
dovascu lar coiling in com p arison to m icrosu rgical clip ping after dates for en dovascular coiling. How ever, recent tech nical advance-
an eur ysm al SAH,46,47 en dovascu lar t reat m en t of an eu r ysm s h as m en t s, such as th e balloon or sten t-assisted coiling tech n iques,
increased approxim ately 5-fold in the United States.48 Even though h ave pract ically rem oved th e tech n ical barriers of a w ide-n ecked
th e ISAT st u dy d id n ot address UIAs, th ere h as been a su bst an t ial an eur ysm an d en abled coiling. In addit ion , th e recen t laun ch of
sh ift tow ard con sid erat ion of en d ovascu lar th erapy in u n r u p - flow diverters sign ifican tly expan ds th e capacit y/abilit y of th e
t u red an d ot h er in cid en t al an eu r ysm s.49 In gen eral, carefu lly en d ovascu lar t reat m en t opt ion .54 On th e oth er h an d, th ese n ew
selected cases of UIAs m ay un dergo favorable obliterat ion after en dovascu lar tech n iqu es are associated w ith an in crease in p ro-
en d ovascu lar coiling (Fig. 62.4). How ever, th ere rem ain s a con - cedu re-related m orbidit y.55 Th is is m ost likely at t ributed to th e

a b

Fig. 62.4a,b A 48-year-old wom an with a previous history of subarach- arrows). She elected endovascular treatm ent. (b) The 7-m onth follow-up
noid hem orrhage (SAH) from a left posterior com m unicating artery (PCoA) angiography after stent-assisted coiling showed complete obliteration of
aneurysm treated with m icrosurgical clipping. (a) The patient was found to the aneurysm . Note the proxim al stent m arkers (white arrows). Although
harbor another unruptured right middle cerebral artery (MCA) aneurysm MCA aneurysm s are generally challenging for endovascular treatm ent, ex-
(long arrow). Note the surgical clip shadow on the left PCoA artery area (short cellent results can be obtained in select cases.

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62 Incidental Aneurysm s 757

a b c

Fig. 62.5a–c A 46-year-old m an with a basilar tip aneurysm treated with required another endovascular treatment. Considering the relatively young
endovascular coiling. (a) The 6-month follow-up angiography showed signifi- age of the patient, and the large and significant recanalization potential of
cant recanalization of the aneurysm base. (b) The recurrence was re-treated this aneurysm, surgical clipping could have accomplished a m ore definitive
with a stent-assisted coiling technique. (c) Repeat 6-m onth follow-up angi- result for this aneurysm .
ography showed significant recanalization of the aneurysm base, which

in creasing procedu ral com p lexit y an d p ossibly longer procedure ■ Summary of Evidenced-Based
t im es. In addit ion , th e sten t-assisted coiling tech n iqu e h as re-
sulted in pat ien ts n eeding long-term an t ip latelet th erapies.
Guidelines
Furth er, th e locat ion of target an eu r ysm is an im portan t fac- In 2000, th e guidelin es for th e m an agem en t of un rupt u red an eu -
tor for deciding t reat m en t opt ion s. For exam ple, MCA an eur ysm s r ysm s from th e AHA w ere publish ed.1 Th ey con clu ded th at th e
sh ow ed bet ter ou tcom es w h en t reated w ith m icrosu rgical clip - literat ure provides level IV an d level V eviden ce an d can suppor t
ping.56 Sm all an eu r ysm s, par t icu larly at th e an terior com m u n i- grade C recom m en dat ion s. Con sidering act ive t reat m en t w as
cating artery, m ay have a substan tially higher procedural rupt ure recom m en ded for an eu r ysm s of all sizes in pat ien t s w ith prior
rate during coiling, associated w ith seriou s m orbidit y.57,58 Th ese SAH, for an eu r ysm s at th e basilar apex, an d for asym ptom at ic
an eur ysm s are m ore easily, safely, an d effect ively t reated w ith an eur ysm s of ≥ 10 m m in diam eter.1 Eviden ce from ISUIA par t
m icrosu rgical clipp ing. Conversely, en dovascu lar coiling of m any t w o, an d from oth er st u dies accru ing sin ce th ese gu idelin es w ere
paraclin oid an d p osterior fossa an eu r ysm s can sh ow bet ter ou t- pu blish ed in 2000, w ou ld also suggest th at a m easu rable in -
com e w it h coilin g t h an w it h su rgical clip p in g. Th e relat ive ou t - creased risk for rupt ure is presen t in an eur ysm s of m edium size
com e t h at m ay be ach ieved w it h eit h er tech n iqu e for a given (in th e 7- to 10-m m range), th ose in th e p osterior circu lat ion (in -
an eur ysm is st rongly related to th e experien ce an d expert ise of clu ding at th e p osterior com m u n icat ing ar ter y), an d th at th ese
variou s m em bers of th e t reat ing team . feat ures m ay be reason s to con sider inter ven t ion s in appropriate
Many of th e an eu r ysm s th at are m ore difficu lt su rgically, su ch low -risk can didates. Em erging evidence also supports early treat-
as at th e basilar ap ex, are also broad based an d subject to term i- m en t of an eu r ysm s of oblong or com plex m u lt ilobed sh ape an d
n al ar ter y h em odyn am ic st resses an d are h en ce m ore likely to th ose w ith h igh size rat io as com p ared w ith th e paren t vessel
recan alize after en dovascu lar t reat m en t (Fig. 62.5). Th e greater lu m en . Sm all an eu r ysm s in th e 2- to 7-m m range in you nger p a-
n eed for invasive follow -up an d poten t ial ret reat m en t after en - t ien t s, esp ecially w ith h igh an eu r ysm -to–p aren t vessel rat io are
dovascu lar in ter ven t ion s, an d con cern abou t h igh er bleed rates con sidered in dividu ally. Pat ien t s’ experien ces, biases, an d per-
from the treated aneurysm after coiling, w ill con tinue to influen ce son al preferen ces in flu en ce th e decision to t reat an d sh ou ld be
th e decision of ch oosing clip ping as a poten t ially m ore effect ive con sidered. Any an eu r ysm th at is docu m en ted to in crease in
an d du rable in ter ven t ion . size, to d evelop a com p lex sh ape, or to produ ce n ew sym ptom s
Th u s, d esp ite t h e recen t sp ike in p op u lar it y of coil u se, id en - w ould w arran t m ore pressing surgical con siderat ion .
t ifying an d recom m en ding th e best m an agem en t opt ion for in - Overall, factors th at favor surger y include a young pat ient w ith
t racran ial an eu r ysm s m u st be assessed w ith all factors in m in d. a long life expectan cy, previou sly ru pt ured an eur ysm s, a fam ily
Overall, th e availabilit y of exp er t ise on both en dovascu lar coiling h istor y of an eu r ysm rupt u re, large an eur ysm s, sym ptom at ic an -
an d open surgical clipping is an im por tan t factor, because n ot all eu r ysm s, obser ved an eu r ysm grow th , an d est ablish ed low t reat -
an eur ysm s can be effect ively m an aged by on e m eth od alon e, an d m en t risks. Factors th at favor con ser vat ive m an agem en t in clu de
at t im es a com bin ed m icrosu rgical-en dovascu lar app roach m ay old er pat ien t age, decreased life expectan cy, m edical com orbidi-
provide th e best t reat m en t opt ion .59 t ies, an d asym ptom at ic sm all an eu r ysm s.1

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758 V Cerebral and Spinal Aneurysms

Th e select ion of m icrosu rgical clipp ing versu s en dovascu lar su m ably h arbored th e biological p redisp osit ion before th e first
in ter ven tion is h igh ly in dividu alized, w eigh ing th e risks of th e bleed. Th e classificat ion of UIAs as grou ps 1 an d 2 is h elpful but
proposed procedu re for th e specific an eu r ysm an d pat ien t an d a bit Dar w in ian , im plying th at th e pat ien t w ould n eed to sur vive
th e team ’s exp erien ce. In gen eral, UIAs th at are w ell am en able to a first bleed before being iden t ified as vu ln erable. Fam ilial cases
su rgical clip ping are bet ter t reated w ith su rger y, often w ith ou t w ith in ciden t al an eu r ysm s often bleed at a younger age th an do
cath eter angiograp hy, by m ore experien ced su rgeon s an d team s oth er UIAs, in cluding frequen t an ecdot al cases of fam ilial cases
offering th e greatest likelih ood of durable an eur ysm obliterat ion bleed ing at abou t t h e sam e age. Th ese factors cou ld im p ly an
w ith th e least n um ber of invasive in ter ven t ion s an d risks. En do- in h er ited p red isp osit ion to r u pt u re, an d n ot ju st to t h e gen esis
vascu lar tech n iqu es are con sid ered in an eu r ysm s an d p at ien t s of an eu r ysm s. Gen om ic app roach es are n eeded to iden t ify ge-
w ith h igh er su rgical risks. n et ic or ep igen et ic var ian t s t h at p red isp ose to r u pt u re. Th ose
Ad d it ion al recom m en dat ion s for con ser vat ively m an aged cases w ou ld w ar ran t m ore vigilan t su r veillan ce or aggressive
an eur ysm s sh ould in clu de m et iculous blood pressure con t rol, t reat m en t .
con cer ted effor t s at sm oking cessat ion , an d t reat m en t of oth er Un an sw ered qu est ion s rem ain as to w h ich in ciden tal an eu -
est ablish ed gen eral vascu lar risk factors. Mon itoring sh ou ld be r ysm s are m ore vuln erable to h em orrh age. Size an d m orph ology
un der t aken by n on invasive vascu lar im aging, on a regu lar basis, an d an eur ysm locat ion are m arkers of in creased risk, but th ey
for as long as th e pat ien t m igh t st ill be a poten t ial can didate for are im perfectly predict ive. Group stat ist ical risks are n ot accept-
in ter ven t ion if t h e an eu r ysm w ere to sh ow ch an ge in size or able in th e era of in dividu alized m edicin e, especially w h en th e
m orp h ology. con sequ en ces of an eu r ysm ru pt u re are so dire. Hem odyn am ic,
biophysical, an d m olecu lar vascular w all im aging w ill n eed to be
develop ed, h igh ligh t ing m ore sen sit ive an d reliable predictors of
th e “vu ln erable an eur ysm ” w ith im pen ding rupt ure.
Much rem ain s to be elucidated in com parat ive effect iven ess
■ Conclusions st udies of various m an agem ent approaches. Mega-databases have
Th e greater risk of ru pt u re, at sm aller size of UIAs in ISUIA grou p been u sed to glean t h e sign ifican t effect of su rgical exp erien ce
2 (th ose w ith a previous h em orrh age from an oth er lesion in th e an d m u lt id iscip lin ar y in tegrat ion on ou tcom e in t h is d isease.
sam e p at ien t), suggest s an in h eren t biological risk of r u pt u re in Prosp ect ive st u d ies sh ou ld con t in u e to refin e t h is in for m at ion ,
th e predisposed h ost . Clearly, all UIA cases in grou p 2 w ere in in cluding th e object ive assessm en t of n ovel diagn ost ic, su rgical,
fact group 1 cases un t il th e first h em orrh age; h ow ever, th ey pre- an d en dovascu lar st rategies an d adjun ct s.

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su rger y for asym ptom at ic, un rupt ured, in t racran ial aneu r ysm s: a m et a- tem at ic review of th e literat ure. Neurosurger y 2004;55:767–775, discus-
an alysis. J Neurosurg 1994;81:837–842 sion 775–778
33. Raaym akers TW, Rin kel GJ, Lim burg M, Algra A. Mor t alit y an d m orbidit y 51. Johnston SC, Zhao S, Dudley RA, Berm an MF, Gress DR. Treatm ent of unrup -
of surger y for un r upt ured in t racran ial aneu r ysm s: a m et a-analysis. St roke tured cerebral an eur ysm s in Californ ia. Stroke 2001;32:597–605
1998;29:1531–1538 52. CARAT Invest igators. Rates of delayed rebleeding from in t racran ial an eu-
34. Ju ng YJ, Ah n JS, Park ES, Kw on H, Kw u n BD, Kim CJ. Su rgical resu lt s r ysm s are low after surgical an d en dovascular t reat m ent . St roke 2006;
of u n r u pt u red in t racran ial an eu r ysm s in t h e eld erly: sin gle cen ter ex- 37:1437–1442
p er ien ce in t h e p ast ten years. J Korean Neu rosu rg Soc 2011;49:329– 53. Joh n ston SC, Higash ida RT, Bar row DL, et al; Com m it tee on Cerebro-
333 vascu lar Im aging of t h e Am er ican Hear t Associat ion Cou n cil on Cardio-
35. Kash iw agi S, Yam ash it a K, Kato S, Takasago T, Ito H. Elect ive n eck clipping vascu lar Radiology. Recom m en dat ion s for th e en dovascu lar t reat m en t of
for u n r u pt u red an eu r ysm s in eld erly p at ien t s. Su rg Neu rol 2000;53: in t racran ial an eu r ysm s: a st atem en t for h ealt h care p rofession als from
14–20 t h e Com m it tee on Cerebrovascu lar Im aging of t h e Am er ican Hear t As-
36. Wirth FP, Law s ER Jr, Piepgras D, Scot t RM. Surgical t reat m en t of inciden - sociat ion Cou n cil on Cardiovascu lar Radiology. St roke 2002;33:2536–
t al in t racran ial an eur ysm s. Neurosurger y 1983;12:507–511 2544

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760 V Cerebral and Spinal Aneurysms

54. Nelson PK, Lylyk P, Szikora I, Wet zel SG, Wan ke I, Fiorella D. Th e pipelin e 57. Lum C, Narayan am SB, Silva L, et al. Outcom e in sm all an eur ysm s (<4 m m )
em bolizat ion device for th e in t racran ial t reat m en t of an eu r ysm s t rial. treated by endovascular coiling. J Neurointerv Surg 2012;4:196–198
AJNR Am J Neuroradiol 2011;32:34–40 58. Pierot L, Barbe C, Spelle L; ATENA investigators. Endovascular t reatm ent of
55. Piot in M, Blan c R, Spelle L, et al. Sten t-assisted coiling of in t racran ial an - ver y sm all unruptured aneur ysm s: rate of procedural com plications, clini-
eu r ysm s: clin ical an d angiograph ic result s in 216 consecu t ive an eur ysm s. cal outcom e, and an atom ical results. Stroke 2010;41:2855–2859
St roke 2010;41:110–115 59. Kaku Y, Wat arai H, Koku zaw a J, Tanaka T, An doh T. Treat m en t of cerebral
56. van Dijk JM, Groen RJ, Ter Laan M, Jeltem a JR, Mooij JJ, Met zem aekers JD. an eur ysm s: surgical clipping an d coil em bolizat ion . In ter v Neuroradiol
Surgical clipping as th e preferred t reat m en t for an eur ysm s of th e m iddle 2007;13(Suppl 1):68–72
cerebral ar ter y. Act a Neurochir (Wien ) 2011;153:2111–2117

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63 Flow -Diverting Stents in the
Management of Complex Aneurysms
David Fiorella

An eur ysm s th at are ch allenging to t reat using conven t ion al sur- is often tem p orar y, an d th e lesion s con t in ue to recur locally an d
gical or en d ovascu lar ap p roach es are regard ed as “com p lex.” en large.
Com plexit y is t ypically associated w ith size (ver y large or gian t),
m orph ology (dysplast ic or fusiform ), or recurren ce after t reat-
m en t . Th e in t rod u ct ion of flow -d iver t in g sten t s u n equ ivocally Modes of Failure w ith Conventional
rep resen t s a con siderable advan ce in th e t reat m en t of th ese an - Endovascular Therapy
eu r ysm s, often allow ing a con st ru ct ive, defin it ive, an d du rable Com plex an eu r ysm s are often n ot su ccessfu lly t reated by con -
t reat m en t opt ion . Exist ing data h ave su pp or ted th e safet y an d ven t ion al en dovascular t reat m en t for t w o m ain reason s. First ,
efficacy of th e tech n iqu e. At th e sam e t im e, ou r un derst an ding of even w ith th e m ost careful tech n iqu e, it is ch allenging to ach ieve
th e opt im al ap p licat ion an d poten t ial lim itat ion s of th e tech n ol- high levels of volum etric packing densit y of platinum coils w ithin
ogy con t in ues to evolve. th ese an eu r ysm s. In sm all, n arrow -n ecked an eu r ysm s, packing
den sit ies of 40%are possible, an d at th is level of an eu r ysm occlu -
sion , recan alizat ion is u n com m on . How ever, for larger an d gian t
an eur ysm s, packing den sit ies are t ypically 20%, w h ich m ay n ot
■ Theoretical Background for provide th e st ru ct u ral in tegrit y to su p por t a du rable an eu r ysm
Flow Diversion occlusion .13–15 Th is is a par t icular problem if th e an eu r ysm con -
tains a large volum e of soft, intralum inal throm bus. With tim e, the
Clinical Need for Flow Diverters coil m ass can th en becom e com pacted in to th e th rom bu s leading
Th e en dovascu lar t reat m en t of an eu r ysm s h as been predicated to relat ively rapid an d large recan alizat ion s (Fig. 63.1). Secon d,
on filling th e an eur ysm al sac w ith em bolic m aterial, t ypically w h en th e an eur ysm – paren t vessel in terface to be recon st ru cted
plat in u m coils. Th is app roach to an eu r ysm t reat m en t can lead to com prises a sign ifican t length an d circu m feren ce of th e p aren t
clin ical ou tcom es th at are as good as, if n ot bet ter th an , th ose of ar ter y, it is ver y difficu lt to recon st ru ct a h om ogen eou s, sm ooth ,
su rger y for m ost ru pt u red an d u n ru pt u red an eu r ysm s en cou n - an d con t in uous surface w ith coils (even w ith th e use of an ad-
tered in clin ical p ract ice.1–6 jun ct ive device such as a balloon or conven t ion al sten t-assisted
Most an eu r ysm s can be addressed by conven t ion al en d osac- coiling). In m ost cases, th e in terface is irregu lar. Th is in com plete
cular coil occlusion . How ever, a sign ifican t percen t age of an eu- n eck recon struction provides an environm ent for recanalizat ion.
r ysm s are eith er un am en able to th is t reat m en t or h ave dem on -
st rated a sign ifican t rate of in com p lete occlu sion or recu rren ce,
The Concept of Flow Diversion
or both , after t reat m en t. In par t icular, large an d gian t an eur ysm s
h ave ver y h igh rates of in com plete occlusion (50% an d 85%) an d Th e con cept of flow diversion fu n dam en t ally d iffers from th at
recurrence (40–70%), and frequently require m ultiple treatm ents of conventional endovascular, endosaccular aneurysm treatm ent.
an d ret reat m en t s.7–11 Th ese t reat m en t s an d ret reat m en t s, along In fact , it is m ore sim ilar to an op en su rgical ap p roach to t h e
w ith th e progression of th e an eur ysm , result in a con siderable lesion . Th e gen eral con cept u n derlying flow diversion is to t reat
level of cum ulative m orbidit y and m ortalit y for larger aneurysm s. the aneur ysm by reconst ruct ing the diseased paren t artery rather
Jah rom i et al7 calcu lated rates of p er t reat m en t m or talit y an d th an by addressing th e saccu lar p or t ion of th e an eu r ysm it self. A
m orbidit y of 8% an d 20%, respect ively, w ith an overall cum ula- h igh -den sit y m esh cylin drical t u be is deployed th rough a m icro-
t ive m orbidit y an d m or t alit y of rate 55% for th e en d ovascu lar cath eter, bridging th e an eu r ysm n eck, sp an n ing from n orm al
t reat m en t of gian t an eu r ysm s. An eu r ysm s for w h ich in it ial en - vessel proxim ally to n orm al vessel distally.16,17
dovascu lar t reat m en t fails to p rovid e a cu re, regard less of t h eir Curat ive recon st ru ct ion of th e paren t arter y w ith an eur ysm
size, also rep resen t a ch allenging subt ype of lesion s w ith about occlu sion occu rs over days to m on th s th rough t h e sequen ce de-
a 50% ch an ce of yet an oth er recu rren ce after ret reat m en t .11 scribed below.18
Fusiform , circum feren t ial, an d ver y w ide-n ecked an eur ysm s
p resen t sim ilar d ifficu lt ies for bot h conven t ion al su rgical an d
Mechanical
en d ovascu lar t h erapy. Th e conven t ion al t reat m en t of t h ese le-
sion s is associated w ith a relat ively h igh rate of p erip rocedu ral Flow disr u pt ion (im m ediate): Th e con st ru ct disru pt s both th e
an d in t raprocedural com plicat ion s, par t icularly w h en a recon - in flow an d ou tflow of blood w ith in th e an eu r ysm , redirect ing
st r uct ive ap p roach (rath er th an a vessel occlu sion ) is requ ired.12 th e pr im ar y vector of blood flow along th e cou rse of t h e an a-
W h en a conven t ion al con st r u ct ive ap proach is t aken , th e resu lt tom ically reform ed paren t ar ter y. Alth ough th e an eur ysm m ay

761

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762 V Cerebral and Spinal Aneurysms

Fig. 63.1a–f (a) Subtracted angiographic image in the anterior


projection shows a large, ruptured carotid-ophthalm ic segm ent
aneurysm. (b) Subtracted angiographic im age in the anterior
projection shows a sm all am ount of residual filling at the aneu-
rysm neck after successful coil em bolization. (c) Native and (d)
subtracted angiographic im ages in the anterior projection dem -
onstrate m arked dissipation of the intra-aneurysm al coil m ass
with a very large recanalization of the aneurysm. (e) Coronal and
(f) axial fluid-at tenuation inversion recovery (FLAIR) sequences
show extensive throm bus m ass surrounding the angiographi-
cally evident recanalization with associated m ass effect and
perianeurysm al edem a throughout the basal forebrain and deep
capsular white m at ter. (Courtesy of The Research Foundation for
the State Universit y of New York.)

a b

c d

e f

st ill fill w ith con t rast , th e in t raan eu r ysm al flow is disru pted an d Biological
sh ear forces on th e an eu r ysm w all are redu ced.
Con st r u ct en doth elializat ion an d th rom bu s resorpt ion (m on th s):
W h en th e an eu r ysm is com p letely occlu ded, th e con st r u ct m ay
Physiological
becom e endothelialized. A perm anent biological seal form s across
An eur ysm th rom bosis (days to w eeks): Disrupt ion of th e in t ra- th e an eu r ysm –p aren t ar ter y in terface fu n ct ion ally bridging th e
an eur ysm al flow creates an environ m en t con du cive to progres- n or m al p roxim al an d d ist al p aren t ar ter ial segm en t s. W h en
sive th rom bosis. W h en t h is p rocess is com p lete, angiograp h ic t h e an eu r ysm is com p letely exclu ded from th e circu lat ion , th e
im aging d em on st rates com p lete occlu sion . Cross-sect ion al im - th rom bu s m ass begin s to resorb an d th e en t ire an eu r ysm m ass
aging sh ow s a th rom bu s m ass w ith in th e an eu r ysm . Th e rate of begin s to collapse aroun d th e periph er y of th e con st ru ct . Sym p -
th is th rom bosis varies sign ifican tly w ith an eu r ysm size, loca- tom s related to an eu r ysm m ass effect or p u lsat ion m ay resolve
t ion , an d degree of n eck coverage. Clin ically, local m ass effect or at th is p oin t (to th e exten t th at th ey are reversible).
t ran sm u ral in flam m ator y ch anges related to th e th rom bosis m ay Th e porosit y of th e flow -diver t ing sten ts m ust be sufficien t to
exacerbate the pat ient’s original clinical sym ptom s. In som e cases, reliably in du ce th e th rom bosis of an eu r ysm s. At th e sam e t im e,
n ew sym ptom s such as h eadach e or cran ial n eu rop athy develop. th ey m u st be p orou s en ough to allow th e p aten cy of any covered
Th ese n ew sym ptom s can at t im es be alleviated w ith steroids. region al side bran ch es. Alth ough an eu r ysm s fill solely du e to th e

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63 Flow-Diverting Stents in the Management of Complex Aneurysms 763

trajector y of inflow and outflow vectors, regional branches fill on Clinical Trials
the basis of arterial-to-venous pressure gradients. These pressure
After th is in it ial clin ical experien ce w ith PED, t w o prospect ive
gradien t s drive flow th rough th e bran ch es an d sup port th eir pa-
t rials w ere con du cted to dem on st rate th e efficacy of th e device.
ten cy despite substan t ial degrees of m etal coverage over th eir
Th e Pip elin e for th e In t racran ial Treat m en t of An eu r ysm s (PITA)
ost ia.1,9 Th u s, th e opt im ally design ed flow -diver t ing sten t w ou ld
st u dy w as a single-arm p rosp ect ive t rial p erform ed to dem on -
be of a p orosit y t h at efficien t ly in d u ces an eu r ysm occlu sion
st rate th e safet y an d feasibilit y of th e PED for cerebral an eu r ysm
w h ile reliably allow ing t h e con t in u ed p aten cy of region al elo-
treatm en t. Th e Pipeline for Un coilable or Failed An eur ysm s (PUFS)
qu en t bran ch es covered by th e con st ru ct .
w as a p ivotal, p rosp ect ive case-con t rol t rial th at led to th e pre-
m arket ap proval of th e PED w ith in th e Un ited States.
Preclinical Data for Flow Diversion
Most of th e p reclin ical dat a evalu at ing flow diversion exist s for PITA Trial
th e Pip elin e (Covidien /ev3, Man sfield, MA) an d th e Su rpass (Su r- Th e PITA t rial in clu ded 31 pat ien t s w ith in t racran ial an eu r ysm s,
pass Medical Ltd ., Tel Aviv, Israel) devices im p lan ted across ex- m ost of w h ich arose (28 of 31) from th e in tern al carot id ar ter y.
perim en tal elast ase-in du ced an eu r ysm s in rabbit s.19–22 In th ese Th e an eu r ysm s w ere large (average size 11.5 m m ) w ith w ide
experim en ts, the auth ors verified that flow -diverting devices im - n ecks (average 5.8 m m ). Treat m en ts w ere ach ieved w ith a ver y
plan ted across th e an eu r ysm –p aren t ar ter y in terface resulted in h igh level of tech n ical success (96.8%). Th ere w as an u nprece-
a reliable occlusion of th e an eur ysm s w ith physiological rem od- d en ted rate of com p lete an eu r ysm occlu sion after 6 m on th s
eling of th e paren t arter y. At th e sam e t im e, th e d evices w ere of (28 of 30 pat ien ts, 93.3%). Th ese results w ere ach ieved w ith an
su fficien t porosit y to allow con t in u ed p aten cy of covered ar terial acceptable rate of p erip rocedu ral m orbidit y. On ly t w o of th e 31
side bran ch es. W h en m u lt iple overlap ping d evices (as m any as pat ien ts experien ced a m ajor periprocedural st roke.26
th ree) w ere im plan ted w ith in th e rabbit aor t a, region al lu m bar
ar teries rem ain ed paten t at all t im e poin ts evaluated (as long as
12 m on th s).23
PUFS Trial
Th e PUFS t rial in clu ded 108 p at ien t s w ith large or gian t (> 10
m m ), w ide-n ecked (> 4 m m ) in t racran ial an eur ysm s of th e in ter-
n al carot id ar ter y. Th e device w as evalu ated using t w o sim ulta-
■ Application of Flow Diverters to n eou s en d poin ts: a prim ar y effect iven ess en d poin t of “PED
Treat Intracranial Aneurysms: t reat m en t su ccess,” an d a p rim ar y safet y en d p oin t of m ajor ip si-
lateral st roke or n eu rologic death by 180 days. PED t reat m en t
Clinical Experience and Data su ccess w as d efin ed as com p lete occlu sion of th e t arget an eu -
Available Devices r ysm , ach ieved w ith th e PED alon e, w ith ou t > 50% sten osis or
occlusion of the parent arter y at 180-day angiographic follow -up.
The Pipeline Em bolization Device (PED; Covidien/ev3) is the only Th ese en d p oin t s w ere com p ared w ith com p osite rates derived
flow diverter th at h as been cleared by th e Un ited States Food an d from th e exist ing literat u re for sim ilarly sized an eu r ysm s. Th is
Drug Adm in ist rat ion an d h as CE (Con form ité Européen n e) Mark literat u re review yielded ben ch m arks of < 30% com p lete occlu -
approval in Eurpoe. Th e PED is com m ercially available in th e sion an d 10 to 15% rates of st roke or death associated w ith con -
Un ited States an d w orldw ide. Ou tside of th e Un ited States, th e ven t ion al th erapies.
Silk+ (Balt Extrusion, Mont m orency, France) and the Surpass flow Pat ien t s en rolled in PUFS h ad both large (m ean size 18.2 m m )
diver ters h ave CE Mark ap proval an d are com m ercially available an d w ide-n ecked (m ean 8.8 m m ) an eur ysm s. Th ese lesion s w ere
in Eu rope. Th e presen t d iscu ssion of h u m an u se is rest ricted to t reated w ith a ver y h igh level of tech n ical su ccess (97.7%). At
th e PED, for w h ich th e m ost data are available. 6 m on th s, com plete angiograph ic occlusion w as ach ieved in 81
of th e 106 an eu r ysm s th at u n der w en t angiograph ic assessm en t
Pipeline Embolization Device : (76.4%). Major ipsilateral st roke or n eurologic death occu rred in
six of 108 su bjects (5.6%) by 180 days.27
Initial Human Experience
Th e in it ial cases t reated w ith th e PED predated it s regu lator y ap - Summary of Trial Data
proval an d w ere m ost often “com p assion ate u se” cases, in w h ich
case-sp ecific regu lator y clearan ces w ere obt ain ed for an eu r ysm s Th e exist ing t r ial dat a dem on st rated th at th e PED p rovided a
n ot am en able to t reat m en t w ith conven t ion al surgical or en do- technically feasible, highly effect ive, an d relat ively safe tech nique
vascular approaches. Many of these cases yielded dram atic results for the treatm ent of the m ost ch allenging of cerebral aneur ysm s.
an d p rovid ed t h e first “p roof of con cept ” t h at flow diversion
cou ld be u sed su ccessfu lly an d safely in p at ien t s lacking oth er
t reat m en t opt ion s (Fig. 63.2).
Both an terior an d posterior circulation aneur ysm s were treated
■ Practical Considerations for the
effect ively, w ith th e device yielding com plete an eu r ysm th rom - Application of Flow Diversion
bosis, physiological vessel rem odeling, resolution of regional m ass
effect , an atom ic restorat ion of a n orm al ap p earan ce on cross-
Patient Selection
sect ion al im aging, an d con t in u ed p aten cy of region al eloqu en t In th e Un ited States, th e PED h as Prem arket Approval Applicat ion
bran ch vessels.17,24,25 (PMA) clearan ce for th e en dovascular t reat m en t of adu lt s (> 22

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764 V Cerebral and Spinal Aneurysms

Fig. 63.2a–e (a) Anterior subtracted angiographic


projection dem onstrates a giant m idbasilar trunk
aneurysm . No conventional surgical or endovascular
approaches to treatm ent were offered. (b) Anterior
native projection after treatm ent with the Pipeline
Em bolization Device (PED), with an eight-device con-
struct built across the lesion. (c) One-year follow-up
angiogram confirm s complete occlusion of the aneu-
rysm and physiological rem odeling of the basilar ar-
tery. (d) Sagit tal reconstruction of the pretreatment
computed tom ography angiography (CTA) dem on-
strates the m ass effect exerted by the aneurysm on
the brainstem . (e) Sagit tal im age from T1-weighted
magnetic resonance imaging (MRI) after 1 year shows
resorption of the thrombus mass and anatomic resto-
ration of the posterior fossa anatomy. (Courtesy of
The Research Foundation for the State Universit y of
New York.)

a b

c e

years) w ith large or gian t , w ide-n ecked, in t racran ial an eu r ysm s exp erien ced op erators can t reat th ese lesion s w ith a h igh degree
from th e p et rou s to th e su perior hyp ophyseal segm en t s of th e of tech n ical an d clin ical success.
in tern al carot id ar ter y. How ever, as th e PED is a PMA device, Im por t an t tech n ical con siderat ion s for th e t reat m en t of in ter-
physician s in th e Un ited States m ay elect to u se th e device ou t- n al carot id an eu r ysm s w ith PED in clude th e follow ing:
side th e labeled in dicat ion s at th eir discret ion . Sim ilarly, ou t side
th e Un ited St ates, regu lator y bodies h ave n ot p laced specific an a- 1. In d icat ion s for t reat m en t: Asym ptom at ic ext rad u ral an eu -
tom ic rest rict ion s on th e applicat ion of th e PED. Our discussion r ysm s, regardless of th eir size, pose lit tle risk to pat ien t s an d
of pat ient select ion sh ould n ot be con sidered an en dorsem en t of are seldom appropriate can didates for t reat m en t w ith flow
off-label u se in th e Un ited States; rath er, it is a sum m ar y of th e d iversion . In t ract able p ain an d p rogressive opt ic n eu rop at hy
available w orldw id e experien ce. are excellen t in d icat ion s for th e t reat m en t of caver n ou s
an eur ysm s.28–30
2. Pat ien t’s age: An advan ced age is often associated w ith h ost ile
Carotid Aneurysms
cer vical carot id an atom y an d ath erosclerot ic vascular disease.
Th e largest am ou n t of exist ing dat a su p p or t ing th e u se of flow Th ese p at ien t s n ot on ly p ose m ore tech n ical ch allenges to
d iversion is from sid ew all an d circu m feren t ial an eu r ysm s in - t reat m en t , bu t also are far less resilien t an d can be bad ly in -
volving th e in tern al carot id ar ter y. W h en ap propriately selected, jured even after a m in or p erip rocedu ral com plicat ion .

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63 Flow-Diverting Stents in the Management of Complex Aneurysms 765
Fig. 63.3a–d (a) Townes projection of large aneurysm aris-
ing from the vertebrobasilar junction (VBJ) and proxim al basi-
lar trunk. (b) Post treatm ent angiogram shows reconstruction
of the right VBJ with t wo Pipeline Em bolization Devices (PEDs)
and deconstruction of the contralateral left distal vertebral
artery. The contralateral vertebral artery was deconstructed
to avoid a direct endovascular leak around the outside of the
construct and into the aneurysm . (c) Six-m onth follow-up an-
giogram confirm s complete occlusion of the aneurysm with
m inim al stenosis (arrow) at the distal aspect of the construct.
This relatively common observation represents immature neo-
intim al tissue growth along the course of the construct. As
the tissue becom es more organized with tim e, these stenoses
often regress spontaneously. (d) One-year follow-up angio-
gram confirms durable cure of the aneurysm , physiological
rem odeling of the basilar artery, and resolution of the m ild
distal in-construct stenosis. (Courtesy of The Research Foun-
dation for the State Universit y of New York.)

a b

c d

3. Carot id an atom y: Tor t uou s cer vical an d in t racran ial carot id ecdot ally, several feat ures of th ese m ore com plex an eur ysm s
an atom y frequen tly poses a con siderable tech n ical ch allenge seem to be associated w ith poorer clin ical ou tcom es:
to the deliver y and accurate deploym en t of flow diverters. The
m ore flexible distal in t racran ial access guiding cath eters are 1. Bran ch vessel(s) arising from th e an eur ysm : Posterior circula-
im p or tan t tools in overcom ing su ch an atom ic feat u res. tion an eur ysm s and m ore distal an terior circulation aneurysm s
4. An t iplatelet m edicat ion com pat ibilit y: Pat ien t s t reated w ith often in corporate eloquen t bran ch vessels th at represen t th e
flow diverters require long-term dual antiplatelet m edications. sole source of blood flow to brain paren chym a. Altern at ively,
Th e su rgeon sh ou ld con sid er screen ing p at ien t s for kn ow n th ese an eu r ysm s m ay involve vascu lar bifu rcat ion s. In eith er
bleed in g d isord ers, resist an ce to an t ip latelet m ed icat ion s, circum st an ce, th e in corporat ion of bran ch es in to th e act ual
m ed icat ion n on com p lian ce, any requ irem en t for long-term an eur ysm h as been associated w ith con t in u ed paten cy of th e
an t icoagu lat ion (e.g., at r ial fibr illat ion ), or any kn ow n n eed an eur ysm , progressive grow th , an d occasion ally rupt u re.32,33
for fu t u re invasive p roced u res (e.g., d en t al recon st r u ct ion , Any bran ch es in corp orated in to th e an eu r ysm at th e t im e of
or th opedic surger y) th at m ay require in terru pt ion of an t i- PED t reat m en t sh ou ld be decon st ru cted w ith coils to avoid
p latelet th erapy. con t in ued in flow, w h ich m ay lead to grow th or rupt ure (Fig.
63.3).
2. Prim ar y isch em ic presen t at ion : An eur ysm s arising from dif-
Noncarotid Aneurysms
fu sely diseased, dolich oect at ic vessels, p ar t icu larly th ose th at
Con siderably few er data are available on th e t reat m en t of m ore m an ifest w ith prim ar y isch em ic sym ptom s related to pro-
d ist al an ter ior circu lat ion an eu r ysm s or p oster ior circu lat ion gressive perforator in terrupt ion , h ave alm ost invariably h ad
an eu r ysm s. Th ese an eu r ysm s, p ar t icu larly t h ose involving t h e dism al outcom es after t reat m en t w ith flow diversion .
p oster ior circu lat ion , h ave been associated w it h h igh rates of 3. Old age: Alth ough younger pat ien t s dem on st rate rem arkable
periprocedu ral com plicat ion s an d poor clin ical ou tcom es.31 An - vascular rem odeling over long segm en t s after flow diversion ,

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766 V Cerebral and Spinal Aneurysms

older pat ien ts often do n ot . Th is ten den cy can be at t ributed to Stable Distal Access
th e obser vat ion th at you nger p at ien t s ten d to h ave localized
Th is is best ach ieved in th e an terior circu lat ion w ith a long (80
disease over a vascu lar segm en t (even if it is a relat ively long
cm ) 6-Fren ch (F) guiding sh eath in th e carot id ar ter y (Neuron -
segm en t) w ith com pletely n orm al vascu lar segm en ts proxi-
Max, Pen u m bra In c., Alam eda CA), w ith an in tern al 6F dist al ac-
m al an d distal to th e an eu r ysm . Su ch an atom y en ables th e
cess gu iding cath eter exten ding in to th e cavern ou s segm en t of
su rgeon to bridge from on e n orm al vascu lar segm en t to th e
th e in t racran ial carot id ar ter y (Neu ron , Pen u m bra In c.; Reflex,
oth er.
Reverse Medical Corp., Ir vin e, CA). In th e p osterior circu lat ion ,
Corresp on dingly, th e best an eu r ysm s for flow diver ters are sim ilar st abilit y of access can t yp ically be ach ieved w it h a 6F
th ose w ith sidew all or fu siform m orp h ology w ith ou t in corp o- lon g Arrow Flex sh eat h (Teleflex Medical, Research Tr ian gle Park,
rated bran ch es, occu rring in young p eop le presen t ing eith er in - NC) exten ding in to th e su bclavian ar ter y, w ith a 6F dist al access
ciden tally or w ith h eadach e.17 gu id ing cath eter p osit ion ed w ith in th e d ist al (p referably th e
proxim al in t racran ial segm en t) ver tebral ar ter y.
Aggressive pret reat m en t of the target arter y w ith an ant ispas-
Patient Preparation m odic agen t (e.g., verapam il or n icardipin e) can h elp preven t va-
Adequate an t iplatelet prem edicat ion is an im portan t com pon en t sosp asm . In cases w h ere th e cer vical an atom y is st raigh tfor w ard,
of p at ien t p rep arat ion for vascu lar recon st r u ct ion w it h flow th e gu iding cath eter can be m an ipu lated in to th e in t racran ial
d iver ters. Th e h igh m et al su r face area coverage ch aracterist ic circulation over a standard 0.035-inch guidew ire. In m ore difficult
of th ese devices presen t s a large, th rom bogen ic in terface to th e cases, th is n avigat ion is ach ieved over th e Marksm an (Covidien /
paren t ar ter y du ring an d im m ediately after im plan t at ion . ev3 En dovascular In c., Plym outh , MN) m icrocath eter an d a m i-
Th e m ost com m on prep rocedu ral an t ip latelet p rotocols for crow ire. In t h e cases w it h ext rem e cer vical tor t u osit y or ot h er
th ese pat ien t s con sist of daily clop idogrel (75 m g) for a m in i- evid en ce of h ost ile an atom y (e.g., fibrom u scu lar dysp lasia), t h e
m um of 5 to 7 days an d aspirin daily (81–325 m g) for a m in im um gu id ing cath eter can be n avigated d ist ally first by n avigat ing a
of 48 h ou rs. Many su rgeon s h ave gravit ated tow ard using a 600- 4 × 20 m m Hyperglide balloon (Covidien /ev3) distally in to th e
m g loading dose of clop idogrel, given th e faster on set of act ivit y in t racran ial (t ypically cavern ou s segm en t) circu lat ion , in flat ing
(as lit tle as 2 h ou rs after adm in ist rat ion ) an d poten t ially m ore it to create a distal “an ch or,” an d th en gen tly ret ract ing th e bal-
rep roducible th erapeu t ic in h ibit ion of platelet s.34–44 Test ing of loon as th e gu iding cath eter is advan ced distally. Th is m an euver
platelet fu n ct ion after th e adm in ist rat ion of aspirin an d clopid o- h elps to cen ter th e guiding cath eter w ith in th e vessel, m in im iz-
grel rem ain s con t roversial. How ever, n eu roin ter ven tion ists are ing th e t raum a created by prim arily pu sh ing th e guiding cath eter
perform ing th ese tests w ith greater frequ en cy.45,46 Clopidogrel- over a w ire.
resistan t pat ien t s are som et im es reloaded an d m ain t ain ed on a
h igh er dose (150 m g/day) to ach ieve respon sivit y; how ever, th is Intraprocedural Imaging
ap p roach m ay n ot n ecessar ily t ran slate to bet ter p at ien t ou t -
Each im plan ted device m ust be p osit ion ed appropriately, fully
com es.47–49 In p at ien t s w h o d o n ot resp on d to clop id ogrel, p ra-
exp an ded, an d in good ap p osit ion to th e p aren t ar ter y to create
sugrel m ay represen t an effect ive an d m ore reliable oral P2Y12
an effect ive con st r uct . Alth ough m ore radiopaque th an m ost of
in h ibitor.50
th e exist ing in t racran ial sten t s, flow diver ters can be ch allenging
to visualize over their en t ire length on ce th ey are im planted, par-
Procedure ticularly w h ere vascular segm en t s overlap th e skull base. During
deploym en t , it is p ossible for th e devices to be su bject to torsion
Th e m et h od s of t h e d eliver y an d d ep loym en t of t h e PED are or to form an oval an d to open in com p letely. Th is con figurat ion
d iscu ssed in det ail in oth er publicat ion s.17,18,25 Th is ch apter fo- results in an ineffective construct and m ay even com prom ise flow
cuses on a few im port an t com pon en ts th at are key to procedural lead ing to vascu lar occlu sion .
su ccess. In t rap roced u ral angiograp h ic com p u ted tom ograp hy (CT),
(e.g., con e beam volu m e CT; Dyn aCT, Siem en s Medical Solut ion s,
Precise Delineation of the Angiographic Anatomy Erlangen , Germ any) is invalu able for obt ain ing a det ailed d ep ic-
t ion of th e con figu rat ion of th e im p lan ted flow diver ters in sit u .
A clear un derstanding of the an atom y of the aneurysm is required Th is m odalit y p rovides a h igh -resolu t ion CT im age th at con firm s
to efficien tly cross th e lesion an d build an effect ive con st ruct . th at th e device is fu lly op en ed an d w ell app osed to th e p aren t
Rot at ion al angiograp hy an d th ree-dim en sion al recon st ru ct ion ar ter y. After deploym en t , an d in th e case of PED, recapt ure of th e
en able th e delin eat ion of opt im ized w orking t w o-dim en sion al deliver y w ire, it is frequ en tly valu able to perform angiograp h ic
project ion s. In it ially, th ese p roject ion s are opt im ized to provide CT to con firm accept able d ep loym en t w h ile st ill m ain t ain in g
th e su rgeon w ith an accu rate bip lan ar localizat ion of th e an eu - access across th e con st ruct (Fig. 63.4).
r ysm outlet . Doing so is part icularly im port an t for ver y large an d
gian t cavern ous an eur ysm s, w h ich are ch allenging to n avigate
beyon d. On ce th e an eur ysm is crossed, th e surgeon m ay ch oose
Postprocedural Management
to adjust th e project ion s to opt im ally depict th e distal an d proxi- Th e p ost p rocedu ral m an agem en t of p at ien t s after flow diversion
m al lan ding zon es. In con t rast to conven t ion al en dosaccular coil is h igh ly con t roversial, an d few dat a are available to guide th ese
em bolizat ion , u n derst an ding of th ese lan ding zon es is m ore im - decision s. For th is reason , I presen t th e cu rren t m an agem en t
p or t an t t h an con sisten t visu alizat ion of t h e an eu r ysm –p aren t st rategies u sed at ou r cen ter, w h ich are based on p erson al exp e-
ar ter y in terface. rien ce an d are con t in uou sly evolving.

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63 Flow-Diverting Stents in the Management of Complex Aneurysms 767

a b

c d

Fig. 63.4a–d (a) Lateral projection, native view of a t wo-Pipeline Em boli- vation, the Marksman microcatheter was exchanged for a 4 × 15 mm Hyper-
zation Device (PED) construct placed across a carotid-ophthalmic segm ent glide balloon (Covidien/ev3), and angioplast y was performed (c) to improve
aneurysm . The distal aspect of the construct (arrow) appears to have been apposition of the devices. (d) Reconstructed im age from follow-up intra-
m alpositioned. (b) Reconstructed DynaCT source im ages in the axial plane cranial artery DynaCTA source data dem onstrated that after angioplast y
with the Marksm an m icrocatheter (Covidien/ev3, Irvine, CA) in place across the t wo devices were well apposed with no gap bet ween the components
the construct. The DynaCT im ages confirm that within the distal aspect of of the construct. (Courtesy of The Research Foundation for the State Uni-
the construct the t wo implanted devices are poorly apposed with a gap versit y of New York.)
bet ween the surfaces of the t wo devices (arrow). On the basis of this obser-

Antiplatelet Therapy rem ain on du al an t ip latelet m edicat ion s for 1 year. If angiogra-
phy dem on st rates com p lete occlu sion at 1 year, p at ien ts are
For pat ien ts t reated w ith flow diver ters, an t ip latelet th erapy var- m ain tain ed on aspirin th erapy an d h alf-dose clopidogrel th erapy
ies w ith th e com plexit y of th e an eu r ysm an d th e length of th e for an oth er year. After 2 years, clopidogrel is discon t in ued an d
recon st ru cted vessel. For m ore st raigh tfor w ard lesion s, in w h ich pat ien ts con t in ue aspirin in defin itely (81 m g/day).
a relat ively sh or t segm en t of an eu r ysm al involvem en t separates We do n ot recom m en d th e discon t in u at ion of clop idogrel
n orm al vascular segm en ts, pat ien t s rem ain on dual an t iplatelet w h en blood flow p ersist s t h rough t h e con st r u ct an d in to t h e
t h erapy for 6 m on t h s. If an giograp hy d em on st rates com p lete an eur ysm . In such cases, pat ien t s t ypically con t in ue dual an t i-
an eur ysm al occlu sion at 6 m on th s, pat ien t s rem ain on aspirin platelet th erapy an d w ait , or addit ion al devices are p laced across
th erapy at t radit ion al doses an d redu ce th eir clop idogrel dose by th e rem ain ing ar ter y rem n an t .
on e-h alf. After 12 m on th s, clopidogrel is discon t in u ed, an d pa- Th is relat ively con ser vat ive ap p roach to th e discon t in u at ion
t ien ts rem ain on aspirin th erapy (81 m g/daily) for life. For m ore of dual an t iplatelet th erapy is based on th e obser vat ion of th e
com p lex an eu r ysm s in w h ich m u lt icon st r u ct d evices are u sed ver y late th rom bosis of flow -diver t ing con st ructs, 1 year or lon -
to bridge large circum feren t ial an eur ysm al segm en ts, pat ien ts ger after th e in it ial t reat m en t .51,52

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768 V Cerebral and Spinal Aneurysms

Blood Pressure Management aneurysm m ight actually “protect” the aneurysm w all from blood
flow, th e opposite m ay be t rue. Acu te th rom bus m ay in du ce
After th e PED recon st ruct ion of an terior circulat ion an eu r ysm s,
isch em ic, in flam m ator y, an d dest r u ct ive ch anges in th e adjacen t
it is pr uden t to en su re n orm oten sion . Several case reports an d
an eur ysm w all after t reat m en t , leading to th in n ing an d, in som e
sm all case series h ave described delayed spon t an eou s ip silateral
cases, to com p lete dissolu t ion .33 A sim ilar ph en om en on h as been
paren chym al h em orrh ages after th e recon st r u ct ion of an terior
obser ved in par t ially th rom bosed abdom in al aor t ic an eur ysm s.
circulation aneur ysm s w ith flow diverters.53,54 The cause of these
Abdom in al aor t ic an eu r ysm s grow m ore rapidly if th ey are p ar-
h em orrh ages is un kn ow n . Th ey h ave been docum en ted to occur
t ially th rom bosed , an d th ey t yp ically r u pt u re from t h e p or t ion
at in ter vals ranging from 1 day to alm ost 3 w eeks after th e p ro-
of th e w all adjacen t to th e th rom bus.57–61
cedu re. Alth ough th e et iology is u n clear, th e avoidan ce of peri-
Predict ing w h ich ver y large an eu r ysm s w ill be su scept ible to
procedu ral hyp er ten sion m ay h elp redu ce th e in ciden ce or th e
delayed r u pt ure can n ot be don e a priori. How ever, som e invest i-
severit y of th ese h em orrh ages sh ou ld th ey occu r.
gators h ave obser ved th at bran ch vessels in corporated in to th e
an eur ysm m ay perpet uate con t in u ed blood flow th rough th e
Steroids con st r u ct an d p reven t or delay com p lete an eu r ysm occlu sion .32,33
Ot h ers h ave n oted t h at sym ptom at ic an eu r ysm s or t h ose t h at
We d o n ot rou t in ely t reat p at ien t s w it h steroid s in t h e p er ip ro-
h ave d em on st rated recen t grow t h m ay be p ar t icu larly su scep -
cedural period. We t ypically reser ve steroids for pat ien t s w h o
t ible to r upt u re after flow diversion .55
develop n ew or w orsen ing sym ptom s of m ass effect or p erian eu -
r ysm al edem a after t reat m en t .
Delayed Ipsilateral Parenchymal Hemorrhage
Angiographic Follow -Up Delayed ipsilateral paren chym al h em orrh age h as been described
prim arily after th e t reat m en t of an terior circu lat ion an eu r ysm s
After flow diversion, w e t ypically perform angiographic follow -up w ith flow diverters.27,53,54 In distinction from delayed aneur ysm al
at 3 to 6 m on th s an d th en at 9 to 15 m on th s. Typically, w e per- rupt ure, delayed paren chym al h em orrh ages are n ot associated
form m agn et ic reson an ce im aging (MRI) at th ese sam e in ter vals w ith th e act ual an eur ysm . Rath er, th ey appear to be poten t ially
to m on itor th e expected, progressive resolu tion of th e an eur ysm – related to th e act u al flow -diversion procedure. Th e h em orrh ages
th rom bu s m ass. If th e secon d angiogram con firm s com p lete an - h ave occurred bet w een 24 h ours an d 3 w eeks after w h at h as
giograph ic occlusion of th e an eur ysm an d th ere is n o eviden ce of t ypically been an u n com plicated p rocedure. Th e h em orrh ages
in -con st ru ct sten osis, fu r th er follow -u p is p erform ed w ith MRI h ave been in th e vascular dist ribut ion of th e t reated an eur ysm
u n t il th e an eur ysm –th rom bu s m ass h as su bstan t ially resolved. but an atom ically rem ote from th e lesion itself. Th e dist ribut ion
of h em or rh age h as been eit h er exclu sively or p red om in an t ly
in t rap aren chym al. Th ese even t s seem to be in d ep en d en t of
th e size, m orph ology, or preoperat ive sym ptom at ic st at u s of th e
■ Intravenous Complications Related to an eur ysm .
Flow Diversion Prop osed et iologies for th is obser vat ion h ave in clu ded (1) re-
perfu sion bleeds in to sm all, clin ically silen t p rocedu ral in farcts;
Th e im m ed iate p er ip roced u ral com p licat ion s related to flow (2) foreign body em boli produced during flow -diver ter place-
d iversion are sim ilar to th ose associated w it h st an dard sten t - m en t; (3) a “hyp er p er fu sion ” p h en om en on resu lt in g from ex-
assisted coiling an d are w ell described elsew h ere.10 clu sion of a h igh -volu m e, large cap acit an ce an eu r ysm from t h e
In addit ion to th e conven t ion al perioperat ive com plicat ion s vascular circu it; an d (4) th e in du ct ion of a ch ange in vascu lar
t radit ion ally seen du ring en dovascu lar sten t-assisted an eu r ysm com plian ce over th e recon st r u cted segm en t , resu lt ing in a loss of
t reat m en t , several delayed com p licat ion s, w h ich are u n iqu e to th e Win dkessel effect an d th e t ran sm ission of a less dam p en ed
th e tech n ology, h ave been described after flow diversion . Th ese ar terial w aveform to th e cerebral vascu lat ure.54
com plicat ion s m ay be obser ved days to w eeks after an in it ially Clin ically, th e severit y of presen tat ion of p aren chym al h em -
un com plicated proced u re. orrh ages h as ranged from m in or n eurologic im pairm en t to death
(Fig. 63.5). Th e m an agem en t of pat ien ts w ith ipsilateral h em or-
rh age is ch allen ging in t h e im m ed iate p er ip roced u ral p er iod ,
Mural Destabilization given t h e d ifficu lt ies involved in reversin g an t ip latelet m ed ica-
Several case rep or t s an d sm all case ser ies h ave d escr ibed t h e t ion s to con t rol th e progression of h em orrh age in a p at ien t w ith
d elayed r upt ure of previously un rupt u red an eur ysm s after flow a n ew ly im plan ted, th rom bogen ic flow -diver ter con st ru ct .
diversion .32,33,55,56 Th is p h en om en on h as been lim ited to ver y Mu ral dest abilizat ion an d delayed ru pt u re are p h en om en a
large an eu r ysm s (> 15 m m ). Th e ru pt u res h ave been docu m en ted lim ited to ver y large an d gian t an eu r ysm s, w h ich h ave a w ell-
to occur days to m on th s after an eur ysm t reat m en t .55 In m ost docu m en ted m align an t n at ural h istor y an d few, if any, com pa-
cases w h ere im aging is available, th e an eu r ysm s h ave dem on - rable altern ative treatm ents. How ever, the sam e is not the case for
st rated a large volu m e of accu m u lat ing in t ra-an eu r ysm al th rom - delayed ip silateral p aren chym al h em orrh age. Th is p h en om en on
bus at th e t im e of ru pt u re. h as been descr ibed w it h bot h large an d sm all cerebral an eu -
Th e origin of th is p h en om en on is u n cert ain , bu t it h as been r ysm s.54 Con sequen tly, th is com plicat ion represen ts a sign ifican t
ascribed to a destabilizat ion of th e an eur ysm w all by the evolv- barrier to th e expan sion of th e in dicat ion s of flow diver ters to
ing in t ra-an eur ysm al th rom bu s th at is in du ced by flow diver- t reat sm aller cerebral an eu r ysm s am en able to oth er t reat m en t
sion .32,55 Alth ough it in t u it ively seem s th at th rom bu s w ith in th e opt ion s su ch as en d ovascular coiling.

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63 Flow-Diverting Stents in the Management of Complex Aneurysms 769
Fig. 63.5a–f (a) Subtracted im age in the right ante-
rior oblique projection dem onstrates recanalization of a
giant right carotid-ophthalmic aneurysm. (b) Subtracted
im age after reconstruction with four Pipeline Em boliza-
tion Devices (PEDs) shows m arked disruption of inflow
into the aneurysm . (c) Subtracted and (d) native angio-
graphic images in the late venous phase image after PED
reconstruction demonstrates the four-PED constructs
in place across the aneurysm neck with persistent stasis
of contrast within the aneurysm . (e) Axial im age from a
diffusion sequence from a baseline post treatment mag-
netic resonance im aging (MRI) study obtained 48 hours
after the procedure dem onstrates no evidence of re-
stricted diffusion. The patient rem ained neurologically
intact and was discharged. The patient rem ained well
a b until 19 days after the procedure when she experienced
the acute onset of left-sided hem iplegia. (f) Axial com -
puted tom ography (CT) scan showed a spont aneous
ipsilateral parenchym al hem orrhage within the right
centrum sem iovale. (Courtesy of The Research Founda-
tion for the State Universit y of New York.)

c d

e f

Very Late Thrombosis con t in u at ion of clopidogrel in resp on se to th e obser vat ion of a
sm all am ou n t of residu al an eu r ysm filling at th e p at ien ts’ 1-year
Th e rate of in -con st r u ct sten osis or occlu sion of flow d iver ters
follow -up exam in at ion . For th is reason , w e t ypically m ain t ain
at in term ediate-term (6–12 m on th ) follow -up is sim ilar to w h at
pat ien ts on du al an t ip latelet m edicat ion s u n t il com plete an eu -
h as been described for oth er in t racran ial an eu r ysm sten ts.62 In
r ysm occlu sion is d ocu m en ted on angiograp hy (as d iscu ssed
th e PUFS t rial, six of 91 p at ien t s (6.6%) w ith angiograph ic follow
above). If a persisten t rem n an t is iden t ified, w e often place ad-
up h ad in -sten t sten osis (n = 2) or con st r uct th rom bosis (n = 4) at
dit ion al flow diver ters over th e involved segm en t as n eeded to
follow -u p. On ly t w o (2.2%) of th ese pat ien ts w ere sym ptom at ic.
augm en t surface coverage an d to en courage progression to com -
For m ost bare m etal sten ts, in -stent sten osis or delayed throm -
plete occlu sion .
bosis is ext rem ely rare after 12 m on th s. In th e case of coron ar y
bare m etal sten t s, such an even t is essen t ially repor table: on ly 22
cases h ave been rep or ted (of m illion s of u n it s im p lan ted) based
on a review publish ed in a 2009.63 How ever, th ere h ave already
been th ree repor ted cases associated w ith ver y late th rom bosis
■ Future Directions
of flow -diver t ing con st ru ct s 1 year or longer after th eir im plan - In th e n ear fut ure, tech n ical advan ces w ith respect to th e deliv-
tat ion .51,52 In t w o cases, th e delayed th rom bosis follow ed th e dis- ery system s for flow -diverting devices should m ake their deliver y

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770 V Cerebral and Spinal Aneurysms

an d d ep loym en t easier an d m ore reliable t h an is t h e case for th e safet y an d efficacy of th ese devices an d of th e com plicat ion s
cu r ren t devices. Hybrid devices th at n ot on ly w ill p rovide flow associated w ith th eir u se. As un derst an ding of th ese issues im -
diversion bu t also w ill allow t ran scon st ru ct cath eterizat ion for proves, it m ay be plau sible to design clin ical t rials th at cou ld su p -
en d osaccular an eur ysm coiling are being d eveloped.64 por t th e exten sion of th is tech n ology from a device reser ved for
With resp ect to th e ap p licat ion of th e cu rren t tech n ology, fur- th e m ost ch allenging cerebral an eu r ysm s to on e th at can be ap -
th er clin ical st u dies are w arran ted to im p rove u n d erst an d ing of plied to conven t ion al an eur ysm s.

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1. John ston SC, Zhao S, Dudley RA, Berm an MF, Gress DR. Treat m en t of un - Aires exp er ien ce. Neu rosu rger y 2009;64:632–642, d iscu ssion 642–643,
ruptured cerebral aneurysm s in California. Stroke 2001;32:597–605 quiz N6
2. McDougall CG, Spet zler RF, Zabram ski JM, et al. Th e Barrow Rupt ured An - 17. Fiorella D, Kelly ME, Albuquerqu e FC, Nelson PK. Cu rat ive recon st ru ct ion
eur ysm Trial. J Neurosurg 2012;116:135–144 of a gian t m idbasilar t r un k an eu r ysm w ith th e pipelin e em bolizat ion de-
3. Molyn eu x A, Kerr R, St rat ton I, et al; In tern at ion al Subarach n oid An eu- vice. Neu rosu rger y 2009;64:212–217, d iscu ssion 217
r ysm Trial (ISAT) Collaborat ive Group. In tern at ion al Su barach n oid An eu- 18. Fiorella D, Lylyk P, Szikora I, et al. Curat ive cerebrovascular recon st ruct ion
r ysm Trial (ISAT) of n eurosu rgical clipping versus en dovascular coiling in w ith th e Pipelin e em bolizat ion device: th e em ergen ce of defin it ive en do-
2143 pat ien t s w ith rupt ured in t racran ial aneur ysm s: a ran dom ised t rial. vascu lar th erapy for in t racran ial an eur ysm s. J Neuroin ter v Surg 2009;1:
Lan cet 2002;360:1267–1274 56–65
4. Molyn eu x AJ, Kerr RS, Yu LM, et al; In tern at ion al Subarach n oid An eur ysm 19. Sadasivan C, Cesar L, Seong J, Wakh loo AK, Lieber BB. Treat m ent of rabbit
Trial (ISAT) Collaborat ive Grou p . In tern at ion al su barach n oid an eu r ysm elast ase-in duced an eur ysm m odels by flow diver ters: developm en t of
t rial (ISAT) of n eurosurgical clipping versus en dovascular coiling in 2143 quant ifiable in dexes of device perform an ce using digit al subt ract ion an-
pat ien t s w ith ru pt u red in t racran ial an eu r ysm s: a ran d om ised com pari- giography. IEEE Tran s Med Im aging 2009;28:1117–1125
son of effect s on sur vival, depen den cy, seizures, rebleeding, subgroups, 20. Sadasivan C, Cesar L, Seong J, et al. An origin al flow diversion device for
an d an eu r ysm occlu sion . Lan cet 2005;366:809–817 th e t reat m en t of in t racran ial an eu r ysm s: evalu at ion in th e rabbit elast ase-
5. W h ite PM, Lew is SC, Gh olkar A, et al; HELPS t rial collaborators. Hydrogel- in duced m odel. St roke 2009;40:952–958
coated coils versu s bare p lat in u m coils for t h e en d ovascu lar t reat m en t 21. Kallm es DF, Ding YH, Dai D, Kadir vel R, Lew is DA, Cloft HJ. A second-
of in t racran ial an eu r ysm s (HELPS): a ran d om ised con t rolled t rial. Lan cet gen erat ion , en dolu m in al, flow -d isru pt ing device for t reat m en t of saccu -
2011;377:1655–1662 lar an eu r ysm s. AJNR Am J Neuroradiol 2009;30:1153–1158
6. W h ite PM, Lew is SC, Nah ser H, Sellar RJ, Goddard T, Gh olkar A; HELPS 22. Kallm es DF, Ding YH, Dai D, Kadir vel R, Lew is DA, Cloft HJ. A n ew en dolu-
Trial Collaborat ion . HydroCoil En dovascu lar An eur ysm Occlu sion an d m inal, flow -disrupting device for treatm ent of saccular aneur ysm s. Stroke
Packing St u dy (HELPS t rial): proced u ral safet y an d op erator-assessed ef- 2007;38:2346–2352
ficacy resu lt s. AJNR Am J Neuroradiol 2008;29:217–223 23. Dai D, Ding YH, Kadir vel R, Rad AE, Lew is DA, Kallm es DF. Paten cy of
7. Jahrom i BS, Mocco J, Bang JA, et al. Clin ical an d angiograph ic outcom e branches after coverage w ith m ultiple telescoping flow -diverter devices: an
after en dovascu lar m an agem en t of gian t in t racran ial an eu r ysm s. Neu ro- in vivo st udy in rabbit s. AJNR Am J Neuroradiol 2012;33:171–174
surger y 2008;63:662–674, discussion 674–675 24. Fiorella D, Woo HH, Albuquerque FC, Nelson PK. Defin it ive recon st ruct ion
8. Nelson PK, Sah lein D, Sh apiro M, et al. Recen t steps tow ard a recon st ruc- of circu m feren t ial, fu sifor m in t racran ial an eu r ysm s w it h t h e p ip elin e
t ive en dovascular solut ion for the orph an ed, com plex-n eck an eur ysm . em bolization device. Neurosurger y 2008;62:1115–1120, discussion 1120–
Neurosu rger y 2006;59(5, Suppl 3):S77–S92, discussion S3–S13 1121
9. Weh m an JC, Han el RA, Levy EI, Hopkin s LN. Gian t cerebral an eur ysm s: 25. Fiorella D, Albuqu erque F, Gon zalez F, McDougall CG, Nelson PK. Recon -
en dovascular ch allenges. Neurosurger y 2006;59(5, Suppl 3):S125–S138, st ru ct ion of th e righ t an terior circu lat ion w ith th e Pipelin e em bolizat ion
discussion S3–S13 device to ach ieve t reat m en t of a p rogressively sym ptom at ic, large carot id
10. Fiorella D, Albu qu erqu e FC, Woo H, Rasm u ssen PA, Masar yk TJ, McDougall an eu r ysm . J Neu roin ter v Su rg 2010;2:31–37
CG. Neuroform sten t assisted an eur ysm t reat m en t: evolving t reat m en t 26. Nelson PK, Lylyk P, Szikora I, Wet zel SG, Wanke I, Fiorella D. Th e pipelin e
st rategies, com plicat ion s an d result s of long term follow -up. J Neuroin - em bolizat ion device for th e in t racran ial t reat m en t of an eur ysm s t rial.
ter v Surg 2010;2:16–22 AJNR Am J Neuroradiol 2011;32:34–40
11. Raym on d J, Guilber t F, Weill A, et al. Long-term angiograph ic recurren ces 27. Covidien. Pipeline Em bolization Device Sponsor Executive Sum m ary. 2011.
after select ive en dovascu lar t reat m ent of an eur ysm s w ith det ach able 28. St iebel-Kalish H, Kalish Y, Bar- On RH, et al. Presen t at ion , n at ural h istor y,
coils. St roke 2003;34:1398–1403 and m an agem en t of carot id cavern ous an eur ysm s. Neurosurger y 2005;
12. Devulapalli KK, Ch ow dh r y SA, Bam bakidis NC, Selm an W, Hsu DP. En do- 57:850–857, discussion 850–857
vascular treatm ent of fusiform intracranial aneur ysm s. J Neuroin ter v Surg 29. Kupersm ith MJ, St iebel-Kalish H, Hun a-Baron R, et al. Cavern ous carot id
2013;5:110–116 an eu r ysm s rarely cause subarach n oid h em orrh age or m ajor n eurologic
13. Slu zew ski M, Men ovsky T, van Rooij W J, Wijn alda D. Coiling of ver y large m orbidit y. J St roke Cerebrovasc Dis 2002;11:9–14
or gian t cerebral an eur ysm s: long-term clin ical an d serial angiograph ic 30. Kupersm ith MJ, Hu rst R, Beren stein A, Choi IS, Jafar J, Ran soh off J. Th e
result s. AJNR Am J Neuroradiol 2003;24:257–262 ben ign course of cavern ous carot id arter y an eur ysm s. J Neurosurg 1992;
14. Slu zew ski M, van Rooij W J, Slob MJ, Bescós JO, Slum p CH, Wijn alda D. Re- 77:690–693
lat ion bet w een an eu r ysm volu m e, packing, an d com p act ion in 145 cere- 31. Siddiqui AH, Abla AA, Kan P, et al. Pan acea or problem : flow diverters in
bral an eu r ysm s t reated w ith coils. Rad iology 2004;231:653–658 t h e t reat m en t of sym ptom at ic large or gian t fu sifor m ver tebrobasilar
15. Wakh loo AK, Goun is MJ, San dh u JS, Akkaw i N, Sch en ck AE, Lin fan te I. an eu r ysm s. J Neurosurg 2012;116:1258–1266
Com p lex-sh ap ed p lat in u m coils for brain an eu r ysm s: h igh er packing 32. Ham pton T, Walsh D, Tolias C, Fiorella D. Mural dest abilizat ion after an eu-
den sit y, im proved biom ech an ical st abilit y, an d m idterm angiograph ic r ysm t reat m ent w ith a flow -diver t ing device: a report of t w o cases. J Neu-
outcom e. AJNR Am J Neuroradiol 2007;28:1395–1400 roin ter v Surg 2011;3:167–171
16. Lylyk P, Miran da C, Cerat to R, et al. Curat ive en dovascular recon st ruct ion 33. Ch ow M, McDougall C, O’Kelly C, Ash for th R, Joh n son E, Fiorella D. Delayed
of cerebral an eur ysm s w ith th e pipelin e em bolizat ion device: the Buen os spon t an eous rupt ure of a posterior in ferior cerebellar ar ter y an eur ysm

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63 Flow-Diverting Stents in the Management of Complex Aneurysms 771

follow ing t reat m en t w ith flow diversion : a clin icopath ologic st udy. AJNR 47. Pr ice MJ, Angiolillo DJ, Teirstein PS, et al. Platelet react ivit y an d cardio-
Am J Neuroradiol 2012;33:E46–E51 vascu lar ou tcom es after p ercu t an eou s coron ar y in ter ven t ion : a t im e-
34. Pat t i G, Bárczi G, Orlic D, et al. Outcom e com parison of 600- an d 300-m g dep en den t an alysis of t h e Gauging Resp on siven ess w it h a Ver ifyNow
loading doses of clopidogrel in patients undergoing prim ar y percutaneous P2Y12 assay: Im pact on Th rom bosis an d Safet y (GRAVITAS) t rial. Circula-
coron ar y in ter vent ion for ST-segm en t elevat ion m yocardial in farct ion : t ion 2011;124:1132–1137
result s from th e ARMYDA-6 MI (An t iplatelet th erapy for Reduct ion of 48. Price MJ, Berger PB, Teirstein PS, et al; GRAVITAS Invest igators. St an dard-
MYocardial Dam age during Angioplast y-Myocardial In farct ion ) ran dom - vs h igh -d ose clop id ogrel based on p latelet fu n ct ion test in g after p ercu -
ized st udy. J Am Coll Cardiol 2011;58:1592–1599 t an eou s coron ar y in ter ven t ion : t h e GRAVITAS ran d om ized t r ial. JAMA
35. Lin GM, Li YH. Com parison of 600 versus 300-m g clopidogrel loading dose 2011;305:1097–1105
in pat ien t s w ith ST-segm en t elevat ion m yocardial in farct ion un dergoing 49. Price MJ, Berger PB, Angiolillo DJ, et al. Evaluat ion of in dividualized clopi-
prim ar y coron ar y angioplast y. Am J Cardiol 2011;107:641 dogrel th erapy after drug-elu t ing sten t im plan t at ion in p at ien t s w ith h igh
36. Man giacap ra F, Mu ller O, Nt alian is A, et al. Com p ar ison of 600 versu s residual platelet react ivit y: design an d rat ionale of th e GRAVITAS t rial.
300-m g Clopidogrel loading dose in pat ien t s w ith ST-segm en t elevat ion Am Heart J 2009;157:818–824, e1
m yocardial in farct ion un dergoing prim ar y coron ar y angioplast y. Am J 50. Fin tel DJ. Oral an t ip latelet t h erapy for at h erot h rom bot ic d isease: over-
Cardiol 2010;106:1208–1211 view of curren t an d em erging t reat m en t opt ion s. Vasc Health Risk Man ag
37. Feldm an DN, Fakorede F, Min utello RM, Bergm an G, Moussa I, Wong SC. 2012;8:77–89
Efficacy of h igh -dose clop idogrel t reat m en t (600 m g) less th an t w o h ours 51. Fiorella D, Hsu D, Woo HH, Tarr RW, Nelson PK. Ver y late th rom bosis of a
before p ercu t an eou s coron ar y in ter ven t ion in p at ien t s w it h n on -ST- pipelin e em bolizat ion device con st ruct: case repor t . Neurosurger y 2010;
segm en t elevat ion acu te coron ar y syn drom es. Am J Cardiol 2010;105: 67(3, Suppl Operat ive):E313–E314, discussion E314
323–332 52. Klisch J, Tu rk A, Turner R, Woo HH, Fiorella D. Ver y late th rom bosis of
38. Motovska Z, Widim sky P, Pet r R, et al. Opt im al pret reat m en t t im ing for flow -diver t ing con st r u ct s after th e t reat m en t of large fu siform p osterior
h igh load dosing (600 m g) of clopidogrel before plan n ed percut an eous circulat ion an eur ysm s. AJNR Am J Neuroradiol 2011;32:627–632
coron ar y in ter ven t ion for m axim al an t iplatelet effect iven ess. In t J Cardiol 53. Velat GJ, Fargen KM, Law son MF, et al. Delayed in t raparen chym al h em or-
2010;144:255–257 rh age follow ing pipelin e em bolizat ion device t reat m en t for a gian t re-
39. Yong G, Ran kin J, Ferguson L, et al. Ran dom ized t rial com paring 600- w ith can alized oph th alm ic an eur ysm . J Neu roin ter v Su rg 2012;4:e24
300-m g loading dose of clopidogrel in pat ient s w ith n on -ST elevat ion 54. Cru z JP, Ch ow M, O’Kelly C, et al. Delayed ipsilateral paren chym al h em or-
acu te coron ar y syn drom e u n dergoing p ercu t an eou s coron ar y in ter ven - rh age follow ing flow diversion for th e t reat m ent of an terior circulat ion
t ion : result s of th e Platelet Respon siven ess to Aspirin an d Clopidogrel an d an eur ysm s. AJNR Am J Neuroradiol 2012;33:603–608
Trop on in In crem en t after Coron ar y in ter ven t ion in Acu te coron ar y Le- 55. Kulcsár Z, Houdar t E, Bon afé A, et al. In t ra-an eur ysm al th rom bosis as a
sion s (PRACTICAL) Trial. Am Hear t J 2009;157:e1–e9 possible cause of delayed an eu r ysm rupt ure after flow -diversion t reat-
40. Su ri MF, Hu ssein HM, Abd elm ou la MM, Divan i AA, Qu resh i AI. Safet y m en t . AJNR Am J Neu roradiol 2011;32:20–25
an d tolerabilit y of 600 m g clop idogrel bolu s in p at ien t s w it h acu te 56. Turow ski B, Mach t S, Kulcsár Z, Hänggi D, St u m m er W. Early fat al h em or-
isch em ic st roke: p relim in ar y exp erien ce. Med Sci Mon it 2008;14:PI39– rhage after en dovascular cerebral an eur ysm t reat m en t w ith a flow di-
PI44 ver ter (SILK-Sten t): do w e n eed to reth in k ou r con cept s? Neu roradiology
41. L’Allier PL, Ducrocq G, Pran n o N, et al; PREPAIR St udy Invest igators. Clopi- 2011;53:37–41
dogrel 600-m g d ou ble loading d ose ach ieves st ronger p latelet in h ibit ion 57. Vorp DA, Lee PC, Wang DH, et al. Associat ion of in t ralum in al th rom bus in
th an conven t ion al regim en s: result s from th e PREPAIR ran dom ized st udy. abdom in al aor t ic an eu r ysm w ith local hypoxia an d w all w eaken ing. J Vasc
J Am Coll Cardiol 2008;51:1066–1072 Surg 2001;34:291–299
42. Cu isset T, Frere C, Qu ilici J, et al. Ben efit of a 600-m g load ing d ose of 58. Sten baek J, Kalin B, Sw eden borg J. Grow th of th rom bu s m ay be a bet ter
clop idogrel on p latelet react ivit y an d clin ical ou tcom es in p at ien t s w ith predictor of ru pt u re th an diam eter in pat ien t s w ith abdom in al aor t ic an -
n on -ST-segm en t elevat ion acute coron ar y syn drom e un dergoing coro- eu r ysm s. Eur J Vasc En dovasc Surg 2000;20:466–469
n ar y stent ing. J Am Coll Cardiol 2006;48:1339–1345 59. Sat t a J. Exp an sion an d ru pt u re of abdom in al aor t ic an eu r ysm s. An n Ch ir
43. Wolfram RM, Torguson RL, Hassan i SE, et al. Clopidogrel loading dose Gyn aecol 1998;87:63
(300 versus 600 m g) st rategies for pat ien t s w ith st able angin a pectoris 60. Sat t a J, Läärä E, Juvon en T. In t ralu m in al th rom bu s pred ict s r u pt u re of an
subjected to percu t an eous coron ar y in ter ven t ion . Am J Cardiol 2006;97: abdom in al aort ic an eur ysm . J Vasc Surg 1996;23:737–739
984–989 61. Dobrin PB, Baker W H, Gley WC. Elastolyt ic an d collagen olyt ic st u dies of
44. Kast rat i A, von Beckerath N, Joost A, Pogat sa-Murray G, Gorch akova O, arteries. Im plicat ion s for th e m ech an ical propert ies of aneur ysm s. Arch
Sch öm ig A. Loading w ith 600 m g clopidogrel in pat ien t s w ith coron ar y Surg 1984;119:405–409
ar ter y disease w ith an d w ith out ch ron ic clopidogrel therapy. Circulat ion 62. Fiorella D, Albuquerque FC, Woo H, Rasm u ssen PA, Masar yk TJ, McDougall
2004;110:1916–1919 CG. Neuroform in -sten t sten osis: in ciden ce, nat ural h istor y, an d t reat-
45. Prabh akaran S, Wells KR, Lee VH, Flah er t y CA, Lopes DK. Prevalen ce an d m en t st rategies. Neurosurger y 2006;59:34–42, discu ssion 34–42
risk factors for aspirin an d clopidogrel resist an ce in cerebrovascular 63. Lem esle G, Pin to Slot tow TL, Waksm an R. Ver y late stent th rom bosis after
sten t ing. AJNR Am J Neu roradiol 2008;29:281–285 bare-m et al sten t im plant at ion : case repor t s an d review of th e literat ure.
46. Lee DH, Arat A, Morsi H, Sh alton i H, Har r is JR, Maw ad ME. Du al an t i- J Invasive Cardiol 2009;21:E27–E32
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J Neu roradiol 2008;29:1389–1394 2013;5:157–160

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64 Aneurysms of Spinal Arteries
Sam uel Kalb, Luis Pérez-Orribo, Mark E. Oppenlander,
M. Yashar S. Kalani, and Robert F. Spetzler

Aneur ysm s of the spinal arteries are rare lesions. Indeed, the true Th e ASA origin ates from bran ch es of each ver tebral ar ter y be-
in ciden ce, dem ograph ics, an d n at u ral h istor y of th ese lesion s are fore th ey u n ite to form th e basilar ar ter y. Th e ASA descen ds on
n ot w ell un derstood. Th e m ajorit y of spin al ar ter y an eur ysm s th e su rface of th e en t ire an terior sp in al cord an d exten ds ven -
rep or ted h ave been associated w ith vascu lar m alform at ion s, an d t rally to th e an terior m edian fissu re (Fig. 64.1b). Th e paired PSAs
th eir occu rren ce, in depen den t of oth er h em odyn am ic in su lt s run longit u din ally along th e posterolateral surface of th e spin al
(vascular m alform at ion s or t raum a), is rarely repor ted. Given th e cord m edial to th e p osterior n er ve root s. Th e PSAs can arise from
scarcit y of th ese lesion s, pract ice gu idelin es an d t reat m en t op - t h e ver tebral ar ter ies or from t h e p oster ior in fer ior cerebellar
t ion s for th ese lesion s are lacking an d ill-defin ed, an d th e litera- arteries (PICAs). Th ey are iden t ified as dist in ct single vessels on ly
t u re on t reat m en t opt ion s is lim ited to case rep or ts.1–5 Herein w e at th eir origin . Th ereafter, th ey becom e an astom osing ch an n els,
review the presen tation, sym ptom atology, and treatm ent option s largely ret ain ing th eir em br yon ic plexiform design .10 Th e ar ter y
for th ese lesion s based on five cases (Table 64.1) t reated at ou r of Adam kiew icz (also called th e ar teria radicularis m agn a, th e
in st it u t ion over th e p ast decade. great radicular ar ter y, an d th e ar ter y of lum bar en largem en t) is
th e largest vessel th at reach es th e spin al cord . It supplies a qu ar-
ter of t h e sp in al cord in 50% of p eop le, an d in m ost cases, t h is
ar ter y t ravels w it h root s from T9 to T12. Th e ar ter y of Adam kie-
■ Vascular Anatomy of the w icz is m ost ly fou n d on t h e left sid e, an d w h en it join s t h e ASA,
it bran ch es in to a sm all ascen ding bran ch an d a large descen ding
Spinal Cord bran ch .6,11,12 Th e lateral spin al ar teries (LSAs) arise at th e level of
Th e spin al cord vascu lat u re can be divided in to a cen t ral an d a the m edulla, from eith er the PICAs or th e intradural vertebral ar-
periph eral system . Th e cen t ral system derives from th e an terior teries, and descend inferolaterally, anterior to the posterior spinal
spin al ar ter y (ASA) an d supplies blood to th e an terior t w o-th irds n er ve roots. Th ese ar teries supply th e spin al accessor y n er ve an d
of th e spin al cord (Fig. 64.1a). Th is system su p p lies th e an terior th e p osterior an d lateral su rfaces of th e spin al cord. Th e ar ter y
gray m at ter, an terior por t ion of th e posterior gray m at ter an d term in ates at C4 or C5, w h ere it an astom oses w ith th e PICA.13
posterior w h ite colu m n s, in n er h alf of th e an terior an d lateral
w h ite colum n s, an d base of th e posterior w h ite colum n s. In th e
periph eral system , th e blood flow s cen t ripet ally from th e p oste-
rior spin al ar teries (PSAs) an d p ial ar terial p lexu s. Th is system ■ Aneurysms of Spinal Arteries
su p plies th e ou ter port ion of th e an terior an d lateral w h ite col-
u m n s an d th e posterior por t ion of th e posterior gray m at ter an d Th e first case of an angiograp h ically p roven sp in al ar ter y an eu -
posterior w h ite colu m n s.6–8 Th e variou s segm en t s of th e sp in al r ysm w as reported in 1981.14 Prior to th is repor t , th ere w ere five
cord are disp rop or t ion ately vascu larized, w ith th e cer vical cord cases of sp in al ar ter y an eu r ysm s in th e literat u re.15,16 In deed ,
presen t ing a large p erip h eral an d large cen t ral ar terial sup ply, sin ce th e p u blicat ion of Vin cen t’s rep or t 14 th ere h ave been less
w h ereas th e th oracic region h as large periph eral an d sm all cen - th an 50 oth er rep or ted cases of spin al ar ter y an eu r ysm s.1,17–19
t ral su pply, an d th e lu m bar an d u pp er sacral region s h ave a sm all An eu r ysm s of th e sp in al ar ter y u su ally are associated w ith vas-
periph eral an d large cen t ral su pp ly.6 cu lar lesion s t h at in crease t h e blood flow t h rough t h e sp in al
In th e upper cer vical spin e, th e radiculom edullar y ar teries ar ter ies, in clu d in g ar ter ioven ou s m alfor m at ion s (AVMs), d u ral
are fed by in ter ver tebral bran ch es of th e ver tebral ar teries an d ar terioven ous fist u las, coarctat ion of th e aor ta, bilateral ver te-
t h eir d escen d in g ram i. In t h e low er cer vical sp in e, t h e segm en - bral arter y occlusion , an d m oyam oya disease in w h ich th e ASA
t al arteries (w h ich feed th e radiculom edullar y arteries) arise ser ves as a collateral blood sup ply. Th ese an eur ysm s h ave n ot
from th e deep cer vical ar ter y, th e costocer vical ar ter y (from th e been associated w ith oth er in t racran ial an eu r ysm s. In addit ion ,
su bclavian ar ter y), an d t h e ascen ding cer vical ar ter y.9 In t h e u n derlying con dit ion s leading to in fect ion /in flam m at ion or vas-
t h oracic cord, th e distan ce bet w een sou rces of blood sup p ly is cular wall weakness such as syphilis, pseudoxanthom a elasticum ,
greater. At th is site, radicu lom edu llar y arteries origin ate from a fibrom uscular dysplasia, Beh çet’s disease, system ic can didiasis,
few in tercostal ar teries deriving from th e subclavian ar ter y an d rh eum atoid arth rit is, an d Sjögren syn drom e h ave been repor ted
aor ta. In th e lu m bar region ar teries exten d from th e aort a an d as precon dit ion ing factors.17,20,21 How ever, if a spin al ar ter y an -
in to th e body w all w h ere radicular arteries arise from th em , eu r ysm is n ot associated w it h a p recip it at in g factor, it is called
som e of w h ich m ay be radicu lom edu llar y ar teries. Th e segm en - an “isolated sp in al an eur ysm .”
tal ar teries in th e sacral region are su p p lied w ith blood from th e As is th e case for th e p ath op hysiology u n derlying an eu r ysm s
lateral sacral ar teries. w ith cerebral AVMs, th e coexisten ce of an eur ysm s an d spin al

772

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64 Aneurysms of Spinal Arteries 773
Table 64.1 Presentation and Demographic Information for Five Patients Treated at Barrow Neurological Institute

Follow -Up
Diagnosis Approach Findings Treatment Complications Outcome (Months)

Lumbar puncture with Thoracotomy with Aneurysm at Wrapping Hemothorax Intact 12


xanthochrom ia, MRI T11 vertebrectomy nonterm inal
with flow voids; spinal branch
angiogram
CT and MRI head for T5–T7 Laminectomy Dissecting aneurysm Resection with None Intact 0.5
SAH; angiogram of at nonterm inal end-to-end
the head negative; branch reconstruction
MRI spine with SAH of vessel
and flow voids at T6-
T7; spinal angiogram
of possible aneurysm
MRI thoracic and lumbar T11–L1 Laminectomy Dissecting aneurysm Resection None Intact 14
spine with SAH and at terminal branch
flow voids at T12;
spinal angiogram with
T12 aneurysm
MRI thoracic and lumbar T12–L2 laminectomy Dissecting aneurysm Resection CSF leak Intact 6
spine with SAH and at terminal branch
spinal angiogram with resected
posterior spinal artery
aneurysm
MRI lumbar spine with T9–L3 laminectomy Dissecting aneurysm Resection None Paraplegic after 1
SAH and spinal mass at terminal branch initial bleed
with sensory
level to T10
Abbreviations: MRI, m agnetic resonance im aging; CT, computed tom ography; SAH, subarachnoid hemorrhage; CSF, cerebrospinal fluid.
Source: Modified from Gonzalez LF, Zabram ski JM, Tabrizi P, Wallace RC, Massand MG, Spet zler RF. Spontaneous spinal subarachnoid hem orrhage secondary to spinal
aneurysm s: diagnosis and treatm ent paradigm . Neurosurgery 2005;57:1127–1131, discussion 1127–1131.

cord AVMs h as been associated w ith h em odyn am ic factors, con - an d 10% w ere you nger th an 10 years of age.25 Most spin al ar ter y
gen it al defect s of ar terial w alls, or som e in teract ion bet w een an eu r ysm s are sm all, w it h diam eters of less th an 3 m m . Sp in al
th ese factors.22 Th e an eur ysm is often located on th e AVM’s af- an eur ysm s can arise in associat ion w ith vascular m alform at ion s
feren t arteries an d regresses after em bolizat ion or su rgical t reat- or in isolat ion . Pat ien t s w ith isolated an eur ysm s are m ore likely
m en t of th e AVM. Spin al an eur ysm s sign ifican tly differ in m any to presen t w ith h em orrh age th an are th ose w h ose spin al an eu-
respect s from in t racran ial an eu r ysm s. Spin al an eur ysm s often r ysm is associated w it h a vascu lar m alfor m at ion . Less t h an 1%
occur along the course of an arter y but seldom at branching points, of all subarach n oid h em orrh ages (SAHs) arise from spin al an eu-
th e caliber of th e spin al ar ter y is m u ch sm aller, an d sp in al an eu - r ysm s. Pat ien t s w ith such an eu r ysm s m ay presen t w ith spin al or
r ysm s ten d to be less affected by ath erosclerosis. In addit ion , in t racran ial SAH (or both ), h em atom yelia, m ass effect , or th rom -
m ost spin al an eur ysm s are fu siform dissect ing dilat ion s an d lack bosis of th e paren t vessel.26 Th e specific clin ical p resen t at ion of
a su rgical n eck.17,23 Th e ASA is involved in th e m ajorit y of cases, a pat ien t w ith a rupt ured spin al an eur ysm depen ds on th e level
but an eur ysm s can also arise from th e PSA, LSA, an d segm en tal an d severit y of h em orrh age, alth ough th e sudden on set of pain
ar teries such as the ar ter y of Adam kiew icz 1,13,20,24 (Fig. 64.2). appears to be un iversal. Patien ts w ith an eur ysm s in th e upper
Most ASA an eu r ysm s are located at th e th oracic an d lu m bar spi- cer vical region u su ally are sym ptom at ic an d p resen t w it h SAH
n al cord an d m ore rarely at th e cer vical region . Nearly all PSA or qu adrip aresis,27 w h ereas an eur ysm s in th e th oracic spin e can
an eur ysm s are located close to th e ben d of th e supplying radicu- cau se acu te p araparesis, radicu lar pain , an d low back pain .23
lopial ar ter y, w h ere it reach es th e cord su rface. LSA an eur ysm s Th e diagn osis of spin e an eu r ysm s can be d ifficu lt an d gen er-
are often th e result of vascular en largem en t from distal ver tebral ally delayed due to its rarit y. W h en ever an SAH is proven by cere-
ar ter y occlusion , as th e LSA ser ves as an im por tant collateral brospin al flu id (CSF) st udies, a spin al origin sh ould be su spected
path w ay bet w een th e proxim al an d dist al ver tebral arteries. w hen th e in it ial com puted tom ography (CT) of th e h ead is n ega-
t ive for SAH or w h en th e blood is localized p red om in an tly in th e
posterior fossa an d th e cerebral angiograp hy is n egat ive.20 Sp in al
Presentation and Diagnosis SAH is essentially confirm ed by T1-weigh ted and fluid-at tenuated
Given th e rarit y of sp in al an eur ysm s, th e m ajorit y of th e litera- inversion recover y (FLAIR) m agn et ic reson an ce im aging (MRI)
t u re on th ese lesion s is lim ited to case rep or ts. In a recen t sys- sequ en ces. An in t radu ral m ass or p ou ch w ith a w ell-dem arcated
tem at ic an alysis, th e m ean age of p at ien t s at p resen t at ion w as in t ram edullar y lesion w ith su rroun ding low sign al in ten sit y, in -
38 years. Nearly 50% of pat ien t s w ere older th an 38 years of age dicating an aneur ysm al w all w ith h em osiderin, m ay be seen w ith
(text cont inues on page 776)

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774 V Cerebral and Spinal Aneurysms

Fig. 64.1a,b (a) Vascularization of the lum bar


spinal cord, dem onstrating the contribution of
the anterior spinal artery (ASA) and the poste-
rior spinal artery (PSA) in supplying the blood
to the spinal cord. a., artery/arterial. (b) Antero-
lateral view of lum bar spinal cord. (Courtesy of
Nicholas Theodore, MD.) b

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64 Aneurysms of Spinal Arteries 775

a b

c d

Fig . 64.2a– g A 63-year-old m an present s with acute lower back pain


and paraplegia with a sensory level to T10. The patient was scheduled for
an m agnetic resonance im aging (MRI) scan. (a) T2-weighted sagit t al and
(b) axial lum bar spinal MRI reveals an epidural m ass behind the bodies of
the L1–L3 levels compressing the thecal sac. The patient was taken to the
operating room for evacuation of the m ass via L1–L3 lam inectom ies. Intra-
operatively the dura was noted to be under significant tension, and antero-
lateral dissection revealed no epidural m ass or compression. Opening of
the dura revealed subarachnoid and subdural blood, which extended ros-
trally. The lam inectom ies were extended to T9. (c,d) At the level of T9 a
throm bosed aneurysm of the artery of Adam kiewicz was identified. Indo-
cyanine green angiograph (e ) noted no flow within the aneurysm . The
decision was made to resect this aneurysm and to decompress the spinal
e cord. (continued on page 776)

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776 V Cerebral and Spinal Aneurysms

f g

Fig. 64.2a–g (continued ) (f,g) Postoperative angiography revealed no flow within the artery of Adamkiewicz. (Courtesy of Barrow Neurological Institute.)

T2-w eigh ted MRI. In cases of a large am ou n t of su barach n oid th e ASA an d it s devast at ing con sequ en ces. In addit ion , en dovas-
blood t h at m ay obscu re a sou rce, sh or t -term follow -u p (1–2 cular t reat m en t is part icularly em ployed in cases of coexisten t
w eeks) w ith MRI could be con sidered. Neverth eless, su praselec- AVMs w ith spin al an eur ysm s, because som e an eur ysm s regress
t ive sp in al angiograp hy is th e best diagn ost ic m odalit y for th e after th e blood flow of th e m alform at ion is reduced.22 An addi-
detect ion of sp in al an eu r ysm s to precisely localize th e an eu r ysm tional treatm en t option is th e “w ait-an d-see” strategy, w ith w h ich
an d avoid any t ype of bran ch occlu sion th at can poten t ially be com plete spontaneous resolution of the lesion is possible in som e
devast at ing, esp ecially for ASA an eu r ysm s.26 Th e oth er vascu lar cases.30,31 The clin ical outcom es am ong the different surgical p ro-
diagn ost ic m odalit ies su ch as m agn et ic reson an ce angiography ced u res are gen erally favorable, alt h ough , given t h e rar it y of
an d CT angiograp hy h ave a low er sp at ial resolu t ion an d m ay th ese lesion s, solid an d con clu sive st atem en t s can n ot be m ade.
easily m iss th e sm all-diam eter spin al an eu r ysm s.28 Th e decision on th e t yp e of proced ure is depen den t on th e m or-
ph ology of th e lesion , th e presen tat ion of th e p at ien t , an d th e
su rgeon’s com fort level w ith th e en dovascu lar or m icrosu rgical
t reat m en t opt ion s.
■ Treatment Options
Th e t reat m en t of sp in al an eu r ysm s varies accord ing to th e m or-
ph ological p resen t at ion of su ch lesion s an d to th e p resen ce or
absen ce of blood distal to th e p aren t vessel. Ideally, th ese an eu -
■ Conclusion
r ysm s sh ould be su rgically occlu ded; h ow ever, because m ost of An eur ysm s of th e spin al ar teries are rare lesion s th at frequen tly
th ese lesion s are fusiform , occu r along in trad ural p or t ion s of ra- presen t w ith oth er vascu lar m alform at ion s. Th e m ost frequ en t
dicu lar ar teries as th ey cou rse to th e sp in al cord, an d lack a su r- presen tat ion of a pat ien t w ith a spin al ar ter y an eu r ysm is back
gical n eck, direct clipping is usu ally n ot feasible. If distal flow is pain . Given th e sm all n u m ber of th ese lesion s reported, th e in ci-
absen t at surger y or in angiograph ic im ages, th e an eu r ysm m ay dence, nat ural history, and treat m ent paradigm s for these lesions
be resected an d t h e p aren t vessel sacrificed or em bolized by are n ot clear. From a t reat m en t perspect ive, in cases w h ere angi-
en dovascu lar tech n iqu e. If th ere is eviden ce of dist al blood flow ography dem onstrates flow distal to the lesion, w e advocate pres-
an d direct clipping of th e an eu r ysm is n ot possible, preser vat ion er vat ion of flow w ith an eur ysm al rein forcem en t or an eu r ysm
of th e paren t vessel is essen t ial. In th ese cases, th e lesion can be resection and end-to-end anastom osis of the vessel. In cases w here
rein forced w ith m uslin w rap ping, or it can be su rgically resected angiography does n ot sh ow flow dist al to th e an eur ysm , th ese
by direct m icrovascular recon st r uct ion .23,26,29 En dovascular pro- lesion s sh ou ld be resected or em bolized to preven t a rebleeding
cedures w ith select ive coiling can be used w h en th e an eur ysm even t . From our lim ited experien ce, it appears th at th e outcom e
h as a saccular m orph ology an d sm all n eck. Em bolizat ion w ith for th ese pat ien t s is, as a w h ole, sat isfactor y, but given th e sm all
liquid m aterials is n ot suggested becau se of th e risk of occlu ding sam ple size, n o defin it ive t reat m en t gu idelin es can be provided.

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64 Aneurysms of Spinal Arteries 777

References
1. Massan d MG, Wallace RC, Gon zalez LF, Zabram ski JM, Spet zler RF. Sub - 18. Sm it h BS, Pen ka CF, Er ickson LS, Mat su o F. Su barach n oid h em or rh age
arach n oid h em orrh age du e to isolated sp in al ar ter y an eu r ysm in fou r p a- du e to an terior spin al ar ter y an eur ysm . Neurosurger y 1986;18:217–219
t ien t s. AJNR Am J Neu roradiol 2005;26:2415–2419 19. Mohsenipour I, Ortler M, Tw erdy K, Schm ut zhard E, At tlm ayr G, Aichner F.
2. Morigaki R, Satom i J, Sh ikat a E, Nagah iro S. An eur ysm of th e lateral spin al Isolated an eur ysm of a spinal radicular ar ter y presen t ing as spin al sub -
ar ter y: a case repor t . Clin Neu rol Neu rosu rg 2012;114:713–716 arach n oid h aem orrh age. J Neurol Neu rosurg Psych iat r y 1994;57:767–768
3. On da K, Yosh ida Y, Arai H, Terada T. Com plex ar terioven ous fist ulas at C1 20. Geibprasert S, Krings T, Apit zsch J, Reinges MH, Nolte KW, Han s FJ. Sub -
causing h em atom yelia th rough an eur ysm al r upt ure of a feeder from th e arachn oid hem orrhage follow ing posterior spinal arter y aneur ysm . A case
anterior spin al ar ter y. Act a Neuroch ir (Wien ) 2012;154:471–475 report an d review of th e literat ure. In ter v Neuroradiol 2010;16:183–190
4. Nogu eira RG, Kasp er E, Walcot t BP, et al. Lateral sacral ar ter y an eu r ysm 21. Klingler JH, Gläsker S, Shah MJ, Van Velthoven V. Rupt ure of a spin al ar ter y
of th e lu m bar spin e: h em orrh age result ing in cauda equ ina syn drom e. an eur ysm at t ribut able to exacerbated Sjögren syn drom e: case repor t .
J Neu roin ter v Su rg 2010;2:399–401 Neurosurger y 2009;64:E1010–E1011, discussion E1011
5. Lucas JW, Jon es J, Farin A, Kim P, Gian n ot t a SL. Cer vical spin e dural ar te- 22. Lavoie P, Raym on d J, Roy D, Gu ilber t F, Weill A. Select ive t reat m en t of an
rioven ous fist u la w ith coexist ing spin al radiculopial ar ter y an eur ysm an terior spin al ar ter y an eur ysm w ith en dosaccular coil th erapy. Case re-
presen ting as subarachn oid hem orrh age: case report. Neurosurger y 2012; port . J Neurosurg Spin e 2007;6:460–464
70:E259–E263, discussion E263 23. Gonzalez LF, Zabram ski JM, Tabrizi P, Wallace RC, Massand MG, Spetzler RF.
6. Mar t irosyan NL, Feuerstein JS, Th eodore N, Cavalcan t i DD, Spet zler RF, Spon t an eous spin al subarach n oid h em orrh age secondar y to spin al an eu-
Preul MC. Blood su pply an d vascular react ivit y of th e spin al cord u nder r ysm s: diagn osis an d t reat m en t paradigm . Neurosurger y 2005;57:1127–
norm al and pathological conditions. J Neurosurg Spine 2011;15:238–251 1131, discussion 1127–1131
7. Turn bull IM. Ch apter 5. Blood supply of th e spin al cord: n orm al an d path - 24. Vish teh AG, Brow n AP, Spet zler RF. An eur ysm of th e int radural arter y of
ological con siderat ion s. Clin Neu rosu rg 1973;20:56–84 Adam kiew icz t reated w ith m u slin w rapping: tech n ical case repor t . Neu -
8. Tveten L. Spin al cord vascularit y. III. Th e spin al cord ar teries in m an . Act a rosurger y 1997;40:207–209
Radiol Diagn (Stockh ) 1976;17:257–273 25. Madh ugiri VS, Am bekar S, Roopesh Kum ar VR, Sasidh aran GM, Nan da A.
9. Lazor th es G, Gouaze A, Zadeh JO, San t in i JJ, Lazor th es Y, Bu rdin P. Ar terial Spin al an eur ysm s: clin icoradiological feat ures an d m an agem en t para-
vascularizat ion of th e spin al cord. Recen t st udies of th e an astom ot ic sub- digm s. J Neurosurg Spin e 2013;19:34–48
st it u t ion path w ays. J Neu rosurg 1971;35:253–262 26. Pelt ier J, Bougeois P, Baron cin i M, Th in es L, Leclerc X, Lejeun e JP. Ult ra-
10. Gillilan LA. Th e ar terial blood su pply of th e h um an spin al cord. J Com p early rebleed ing of an an terior spin al ar ter y an eu r ysm . Br J Neu rosu rg
Neurol 1958;110:75–103 2010;24:468–470
11. Sliw a JA, Maclean IC. Isch em ic m yelopat hy: a review of spin al vascu la- 27. Goto Y, Kam ijyo Y, Yon ekaw a Y, Kiku ch i H. Ru pt u red an eu r ysm of t h e
t u re an d related clin ical syn d rom es. Arch Phys Med Reh abil 1992;73: p osterior spinal ar ter y of th e upper cer vical spin al cord: case report . Neu-
365–372 rosurger y 1988;22:558–560
12. Parke W W, W h alen JL, Bunger PC, Set tles HE. Int im al m uscu lat u re of th e 28. Koc O, Ozbek O, Paksoy Y, Kocaogullari Y. Neurological pict ure. An terior
low er an terior spin al ar ter y. Spin e 1995;20:2073–2079 sp in al ar ter y an eu r ysm p resen t ing w ith sp in al cord com p ression : MRI
13. Ch en CC, Bellon RJ, Ogilvy CS, Put m an CM. An eur ysm s of th e lateral spin al an d MRI angiograp h ic fin dings. J Neurol Neurosu rg Psych iat r y 2010;81:
arter y: report of t w o cases. Neurosurger y 2001;48:949–953, discussion 771–772
953–954 29. Longat t i P, Sgubin D, Di Paola F. Bleeding spin al ar ter y an eur ysm s. J Neu-
14. Vin cen t FM. An terior spin al ar ter y an eur ysm presen t ing as a subarach - rosurg Spine 2008;8:574–578
n oid h em orrh age. St roke 1981;12:230–232 30. Iih osh i S, Miyat a K, Murakam i T, Kan eko T, Koyan agi I. Dissect ion an eu-
15. Yon as H, Pat re S, W h ite RJ. An terior spin al ar ter y an eu r ysm . Case rep or t . r ysm of th e radiculom edullar y bran ch of th e ar ter y of Adam kiew icz w ith
J Neu rosurg 1980;53:570–573 subarach n oid h em orrh age. Neu rol Med Ch ir (Tokyo) 2011;51:649–652
16. Garcia CA, Dulcey S, Dulcey J. Rupt ured an eur ysm of th e spin al ar ter y of 31. Berlis A, Sch eufler KM, Sch m ah l C, Rauer S, Göt z F, Sch um ach er M. Soli-
Adam kiew icz during pregn an cy. Neurology 1979;29:394–398 t ar y spin al arter y aneu r ysm s as a rare source of spin al subarach n oid
17. Rengach ar y SS, Duke DA, Tsai FY, Kragel PJ. Spin al ar terial an eur ysm : case h em orrh age: poten t ial et iology an d t reat m en t st rategy. AJNR Am J Neuro-
report . Neu rosurger y 1993;33:125–129, discussion 129–130 radiol 2005;26:405–410

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65 Cerebral Aneurysms: To Clip or Coil?
Brian P. W alcot t and Christopher S. Ogilvy

Microsurgical clip placem en t and endovascular coil em bolizat ion 2:1 iden t ifies an eu r ysm s th at are likely able to be coiled. Oth er
rep resen t t w o of th e m ost w idely em p loyed tech n iques available con siderat ion s in clu de th e n eck size (< 5 m m is favorable) an d
to obliterate in tracranial aneurysm s. Historically, clip obliteration close relat ion sh ip to a n eigh boring ar ter y (u n favorable).7 Th e
of th e cerebral vasculat ure h as its roots t raced to th e foun ding n eu rovascular surgeon m ust be able to see in h is or h er “m in d’s
fath ers of n eu rosu rger y. Har vey Cu sh ing 1 h ad in it ially described eye” th e abilit y to deliver a coil m ass th at both obliterates th e
th e u se of silver “clip s” for th e “occlu sion of vessels in accessible aneurysm and does not com prom ise surrounding vessels, sim ilar
to th e ligat u re.” Alth ough th is in n ovat ion w as in ten ded to pro- to envisioning m icrosurgical clip placem ent. Certain adjuncts can
vide h em ost asis du ring brain t u m or surger y, a m odified clip w as assist w ith coiling, such as in t ralum in al sten t devices an d bal-
soon u sed by Walter Dan dy 2 to specifically obliterate an eur ysm s loon assist an ce. En dovascu lar th erapy w ith flow -diver t ing sten t
of th e in t racran ial carot id arter y. In con t rast , en dovascular coil placem en t alon e is also an em erging t reat m en t variat ion .8 With
em bolizat ion is a relat ively con tem porar y m ean s of an eu r ysm th ese m eth ods, m any p reviou sly u n coilable or even u n t reat able
obliterat ion . Th e first en dovascular delivered coils (Guglielm i de- an eur ysm s are n ow am en able to en dovascular t reat m en t .
tach able coils) w ere used to t reat pat ien ts in th e early 1990s.3 Oth er an eur ysm ch aracterist ics can poten t ially play an even
Desp ite en dovascu lar coil t reat m en t deriving from a m ore m od- bigger role in determ in ing t reat m en t m odalit y, par t icularly loca-
ern h istoric p eriod an d con sequ en t ially h aving less cu m u lat ive t ion . En dovascu lar coiling of p osterior circu lat ion an eu r ysm s h as
exp erien ce an d n o long-term follow -u p, it h as been sh ow n th at becom e a popular altern at ive to surgical clipping, par t icularly
both m eth ods are effect ive at th e ult im ate prim ar y goal of an eu- du e to th e h igh su rgical risk associated w ith th ese lesion s (Fig.
r ysm t reat m en t—to safely elim in ate blood flow in to th e an eu- 65.1).9,10 It sh ou ld be em p h asized th at th ere st ill rem ain s a role
r ysm . A recen t an alysis of th e total an eur ysm su rgical pract ice in for m icrosu rger y for an eu r ysm s of t h e p oster ior circu lat ion ,
th e Un ited St ates p rovides st rong eviden ce for th e p op u larit y of p ar t icu larly th ose of th e su perior cerebellar ar ter y, P1 segm en t
both tech n iques, w ith just over h alf of all an eu r ysm s n ow t reated posterior cerebral artery, distal anterior inferior cerebellar artery,
w ith en dovascu lar coiling.4 Alth ough a m ajor, m u lt i-in st it u t ion , an d posterior in ferior cerebellar ar ter y.11 Alth ough m icrosurger y
prosp ect ive ran dom ized t rial h as at tem pted to p rovide a direct can st ill be u sed to t reat lesion s of th e P2 segm en t p osterior ce-
com parison bet w een t h e t w o m odalit ies,5,6 sign ifican t n u an ces rebral ar ter y, basilar t r un k, basilar apex, proxim al an terior in fe-
exist in in dividual pat ien ts th at can n ot n ecessarily be accoun ted rior cerebellar ar ter y, an d ver tebral ar ter y, en d ovascular coiling
for in clin ical trials. Because th e vast m ajorit y of aneur ysm s can be is gen erally favored. Th ese are gen eralizat ion s, an d an eur ysm
obliterated via eith er m eth od, a m ult im odalit y provider capable t reat m en t ch oices sh ou ld be determ in ed on an in dividu al basis.
of bot h m et h od s can t h orough ly evalu ate each u n iqu e clin ical On rare occasion s, ext raordin arily com plex lesion con figu rat ion s
scen ario an d an eu r ysm con figu rat ion . At n eu rovascu lar cen ters, requ ire th e n eed for m icrosu rgical revascu lar izat ion 12,13 or car-
t h e qu est ion to “clip or coil” really t ran slates in to a st im u lat in g d iac st an d st ill,14 tech n iqu es t h at sh ou ld on ly be p er for m ed at
d ialogu e th at em p h asizes t h e best p ossible p at ien t care. Th is exp erien ced cen ters (Fig. 65.2).
ch apter decon st r u ct s th e dich otom y of clip or coil an d h igh ligh t s
specific feat ures, available evidence, and technical considerations
th at favor on e t reat m en t m odalit y over th e oth er.

■ High-Grade Ruptures
Su barach n oid h em orrh age related to an eu r ysm ru pt u re can p re-
sen t w ith devastat ing effect s. For pat ien t s w h o sur vive, an d pre-
■ General Considerations sen t for m edical care, th e clin ical scen ario is t yp ically st rat ified
Th e m ajorit y of an eu r ysm s can be t reated via eith er clip or coil by several available validated grading system s; th e purpose of
obliterat ion . Many an eu r ysm s th at are coiled cou ld in stead be th ese system s is to p redict th e ou tcom e. Th ese grading system s
clipp ed; m any clipp ed an eu r ysm s cou ld be coiled. Th ey are both act n ot on ly to gu id e p oten t ially in ten sive t h erapy, bu t also to
viable tech n iqu es for t h e m ajor it y of lesion s. Th e ar t of n eu ro- d irect p at ien t an d provider expectat ion s. For exam ple, in th e
vascular su rger y resides in being able to discern th e an t icipated Ogilvy an d Car ter scale (determ in ing th e Massach uset ts Gen eral
risks an d ben efit s of differen t t reat m en t m et h ods for th e sam e Hospit al grade), an eld erly pat ien t p resen t ing w ith a r u pt u red
unique aneurysm . This involves the evaluation of patient-specific gian t posterior circulat ion an eur ysm an d diffuse subarach n oid
an d an eu r ysm -specific factors. h em orrh age in a com a w ou ld receive a 5 on th e 5-poin t scale,
Pat ien t -specific factors gen erally relate to th e in t rin sic an eu - m ean ing “h igh -grad e,” w h ich is in d icat ive of a likely p oor ou t -
r ysm con figu rat ion . Classically, a n eck-to-d om e asp ect rat io of com e or n on su r vival.15,16 Many pat ien ts w h o presen t w ith h igh -

778

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65 Cerebral Aneurysms: To Clip or Coil? 779

a b c

Fig. 65.1a–c Coiling of ruptured posterior circulation aneurysm . A 61- orrhage with a diffuse pat tern, it can be predicted that the irregular, largest
year-old wom an presented with “the worst headache of [her] life” and dif- aneurysm was the source. The basilar apex aneurysm was obliterated with
fuse subarachnoid hem orrhage. Computed tom ography angiogram (CTA) coils, and the patient m ade a full recovery. (c) Towne projection vertebral
revealed the presence of m ultiple aneurysm s including a 7.5-m m basilar artery angiography reveals obliteration of the basilar apex aneurysm . She
artery apex aneurysm , and sm aller superior cerebellar and m iddle cerebral has been followed with serial angiography. Treatment planning for the re-
artery aneurysm s. (a,b) Towne projection and lateral vertebral artery angi- maining aneurysm s is ongoing.
ography, respectively, dem onstrate the aneurysm s. In the context of hem -

grade r u pt ures suffer from elevated in t racran ial pressure, irre- m ed ical m an agem en t can n ot relieve in t racran ial hyper ten sion ,
spect ive of th e presen ce of a m ass occupying h em atom a (Fig. decom p ressive cran iectom y p rovid es rap id an d su st ain ed con -
65.3). On e of th e m ain goals in t h e im m ed iate care of t h ese t rol of in t racran ial p ressu re 17 an d m ay h ave ut ilit y in im proving
p at ien t s is em ergen t in t racran ial p ressu re con t rol. Th is can be n eu rologic outcom es.18,19
ach ieved in som e, bu t n ot all, w it h t h e aid of ven t r icu lostom y. An altern at ive m an agem en t st rategy for h igh -grade r upt ures
For t h ose p at ien t s for w h om cerebrosp in al flu id d rain age an d is en dovascular coil em bolizat ion .20,21 Th is m odalit y also en ables

a b

Fig. 65.2a,b Clip obliteration of aneurysm and hematom a evacuation for configuration, pointing anteriorly and inferiorly (b). An external ventricu-
com atose 35-year-old m an, who presented with loss of consciousness lostomy was placed em ergently, dem onstrating an opening pressure of
while working in an office. He was found to have hydrocephalus, intraven- 32 cm H2 O. Intracranial pressure was controlled with careful drainage. He
tricular hem orrhage, m ild scat tered subarachnoid hem orrhage, and a large was t aken to the operating room em ergently for successful hem atom a
intraparenchym al hem orrhage of the inferior frontal lobe noted on non- evacuation and clip obliteration of his aneurysm . His ventriculostomy was
contrast computed tomogram (a). Computed tomography angiogram (CTA) weaned without incident. He is currently undergoing intensive inpatient
revealed a 5-m m anterior com m unicating artery aneurysm in a “windsock” rehabilitation.

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780 V Cerebral and Spinal Aneurysms

a b c

Fig. 65.3a–c Complex vessel reconstruction of dissecting fusiform aneu- possible extracranial-to-intracranial bypass. Fenestrated, right-angle aneu-
rysm . A 37-year-old m an presented to the em ergency room with “the rysm clips were successfully placed sequentially to reconstruct the wall of
worst headache of [his] life.” He was discovered to have subarachnoid hem - the vessel. The patient made a full recovery and has done well since. (b,c) A
orrhage resulting from a dissecting, fusiform aneurysm of the left m iddle 2-year follow-up angiogram is shown, dem onstrating no residual aneurysm
cerebral artery. (a) Computed tom ography angiography illustrates the le- along the reconstructed M2 segment and the clip construct used.
sion. He was taken to the operating room for vessel reconstruction with

pat ien ts p resen t ing w ith a delay after th eir in it ial ru pt u re bu t st roph ic r u pt u re (or reru pt u re). Th e su ccess of t reat m en t , eith er
w h o are in a state of vasospasm to receive in t ra-ar terial th erapy via coil or clip can be m easu red by th e degree of an eur ysm oblit-
at th e t im e of an eu r ysm obliterat ion . Ret rospect ive evalu at ion of erat ion , p aten cy of p aren t an d perforat ing vascu lat u re, an d th e
th is tech n iqu e h as iden t ified sim ilar ou tcom es to su rgical series durabilit y of their nat ure. Recan alizat ion an d recurrence are com -
in h igh -grad e p at ien t s.22,23 Alt h ough con t roversial, t h e In ter- plicat ion s kn ow n to occu r in frequ en tly follow ing any an eu r ysm
n at ion al Subarach n oid An eur ysm Trial (ISAT) dem on st rates a t reat m en t , an d th eir in ciden ce m ay be related to th e t reat m en t
su r vival advan tage in p at ien t s t reated w ith en dovascu lar coiling m odalit y itself.26–30 This phenom enon is of particular im portance
com p ared w it h t h e op en su rgical grou p .5,6 Also, t h e Bar row w h en evaluat ing young, h ealthy pat ien t s w ith m any decades left
Ru pt u red An eu r ysm Trial (BRAT) provides n ew p rosp ect ive evi- of life. Th e durabilit y of t reat m en t , th erefore, becom es of in -
den ce for th is fin ding, w ith st at ist ically sign ifican t p oorer ou t- creasing im por t an ce in th is specific populat ion . ISAT an d oth er
com es at t ribu ted to th eir surgical clip arm .24 Som e pract it ion ers st u dies h ave dem on st rated th e su periorit y of clipp ing, com p ared
h ave ext rapolated th ese fin dings to h igh -grade r upt ures, w h ere w ith coiling, in providing long-term protect ion from reh em or-
th ey p rim arily favor en dovascu lar th erapy on th e p rem ise th at rh age.5,6,31,32 In fact , t w o p at ien t s in ISAT w h o h ad docu m en ted
en dovascular therapy m ay have a low er procedural risk in a group com p lete angiograp h ic occlu sion of t h eir an eu r ysm follow in g
th at is already at a ver y h igh risk of overall m or talit y. Despite th e coilin g su ffered reh em or rh age even t s. Th erefore, regard less of
qu est ion of du rabilit y in th e long term , coiling can p rovide ade- any sm all poten t ial ben efit th at m ay be con ferred by coil em bo-
qu ate p rotect ion from reru pt u re in th e acu te p eriod .25 It sh ou ld lizat ion in this young popu lat ion w ith regard to in it ial su rgical
be n oted th at h igh -grade r upt ures w ith space-occupying h em a- risk, th ose p at ien t s u n der 40 years of age are likely to h ave bet ter
tom as require em ergent surger y for clot evacuation; t ypically an- long-term protection from rehem orrhage by clip placem ent, given
eur ysm obliterat ion is accom p lish ed at th at t im e as w ell. Regard- th eir long life expect an cy.27
less of t reat m en t , th e ou tcom e of h igh -grade r u pt u res rem ain s Regardless of th e in it ial t reat m en t m odalit y, vigilan ce in an -
guarded. In th e absen ce of h ead-to-h ead com parison s bet w een giographic follow -up is m andatory. Even aneur ysm s that are oblit-
th ese t w o t reat m en t algorith m s, pat ien t care m u st be cu stom - erated (or perceived obliterated) can dem on st rate recu rren ce in
ized to individual clinical scenarios, in the con text of in st it ut ional both th e sh or t an d long term . In th e case of clipping, in t raopera-
experien ce an d available resources. t ive or postop erat ive angiograp hy m ay be u sefu l to determ in e
th e exact clip p lacem en t an d p aren t vessel arch itect u re. Postop -
erat ive follow -u p of clip ped an eu r ysm s w ith digit al su bt ract ion
angiograp hy, n on invasive com pu ted tom ography angiography,
or m agn et ic reson an ce angiography is com m on , alth ough prac-
■ Recurrence t ice pat tern s regarding t im ing an d frequ en cy differ con siderably
Th e goal of all an eu r ysm su rger y is to elim in ate blood flow in to am ong in st it ut ion s. Coiled an eur ysm s are of par t icu lar im por-
th e an eu r ysm , p rotect ing t h e p at ien t from a p oten t ially cat a- tance for close-in ter val follow -up given th e ph en om en on of coil

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65 Cerebral Aneurysms: To Clip or Coil? 781

a b

Fig . 65.4a,b Aneurysm coiling after previous clipping. A 47-year-old m unicating artery aneurysm m easuring 6.5 m m in greatest dim ension. The
wom an present s 15 years following m icrosurgical clip obliteration of previously placed aneurysm clip was observed to be anterolateral, whereas
a posterior com m unicating artery aneurysm at a referring hospital. Over the aneurysm segment was posteromedial directed. (b) Coil em bolization
the course of 2 days, she developed a com plete third cranial nerve palsy. was perform ed successfully, with obliteration of the aneurysm sac and
(a) Three-dimensional angiogram demonstrated a recurrent posterior com - preservation of the posterior com m unicating artery flow.

com p act ion t h at can resu lt in an eu r ysm regrow t h an d su bse- th rough th e sam e cran iotom y, th ey sh ou ld be t reated at th e sam e
qu en t h em or rh age.33 Lon g-ter m follow -u p (beyon d 2 years) for t im e. Th e h igh er-r isk an eu r ysm sh ou ld be id en t ified based on
coiled an eu r ysm s is also in dicated given rep or t s of recu rren ce size an d con figu rat ion , as t h is h elp s to d eter m in e t h e in it ial
after com plete coil obliterat ion beyon d th is t im e poin t .34,35 t reat m en t—obliterat ing th e an eu r ysm th at h as th e h igh est risk
If recu rren ce does occur, presen t ing eith er on angiograph ic of rupt ure. If th e pat ien t presen ts in th e set t ing of a su barach -
follow -up or reh em orrh age, t reat m en t opt ion s in clude eith er n oid h em orrh age, th e an eur ysm predicted to h ave bled sh ould
clipping or coiling. An eu r ysm s can be clip ped after coiling 36–38 be t reated first , com m on ly iden t ified by its irregular con tour an d
an d vice versa (Fig. 65.4).10 Specific t reat m en t is h igh ly in dividu- su barach n oid h em orrh age pat tern .42 Coiling of on e an eur ysm
alized an d reflects an eu r ysm an d p at ien t ch aracterist ics, sim ilar is n ot a con t rain dicat ion to clipp ing of an oth er an eu r ysm in th e
to prim arily t reated an eur ysm s. Previou sly t reated lesion s are sam e p at ien t if th ese are determ in ed to be th e opt im al t reat-
part icu larly ch allenging en tit ies an d requ ire con siderat ion of th e m en t m eth ods for each on e. Both m eth ods sh ould be evaluated
com p lete n eu rovascu lar arm am en tariu m . Th ese in clu de, bu t are in all pat ien ts w ith m u lt iple lesion s; in dividual an eur ysm ch ar-
n ot lim ited to, re-clipping, re-coiling, coiling follow ing prim ar y acterist ics sh ould be th e prim ar y con siderat ion in t reat m en t
clipp ing, clipp ing follow ing prim ar y coiling, an d ext racran ial-to– plan n ing togeth er w ith th e ch aracterist ics of con com itan t an eu-
in t racran ial bypass w ith coil or clip occlu sion of an eu r ysm an d r ysm s already (or readily) exposed in th e surgical field.
paren t vessel.39,40 Addit ion al adjuvan t s, such as balloon -assisted
coil m ass rem odeling and stent-assisted coiling, can be considered
in sp ecific sit u at ion s. Th ere h as even been th e develop m en t of a
n ovel an eur ysm clip w ith blades design ed to accom m odate pre-
viously coiled aneurysm s.41 Factors that favor endovascular treat-
■ Mycotic Aneurysms
m ent are posterior circulation location, aneur ysm size larger than Mycot ic an eur ysm s, bet ter defin ed as in fect iou s an eur ysm s, t yp -
10 m m , an d fusiform m orphology because of th e h igh er surgical ically occur in th e dist al cerebral vascu lat u re an d often in th e
risk associated w ith th ese factors.39 Oth er con dit ion s gen erally set t ing of bacterial en docardit is. For un ru pt ured an eur ysm s, th e
su p por t t reat ing recu rren t an eu r ysm s w ith clip p ing, secon dar y m ain st ay of th erapy is an t ibiot ic t reat m en t an d follow -up cere-
to th e sup erior long-term du rabilit y of rep air it can provide. bral angiography.43 Operative or endovascular treatm ent should be
pu rsu ed for th ose experien cing an eu r ysm al r u pt u re or en large-
m en t desp ite an t ibiot ic th erapy. Th ese pat ien t s are ten uous an d
entail high risk from both an anesthesia and a surger y standpoint.
Specifically from a n eu rosurgical perspect ive, th e in t raop erat ive
■ Multiple Aneurysms rupt ure risk is h igh given th e path ologically fragile w all of th ese
Many p at ien t s diagn osed w ith an in t racran ial an eu r ysm act u ally lesions. Microsurgical intervention, either via clip reconstruction
h arbor m u lt ip le an eu r ysm s. Th ey sh ou ld be evalu ated for clip or cerebrovascular bypass, is indicated w hen distal vasculature is
or coil an eur ysm obliterat ion both in isolat ion an d in th e con text expected to supply eloquent territory and has been perform ed w ith
of each oth er. For exam ple, if n earby an eur ysm s are accessible relat ively low m orbidit y an d m or talit y at specialized cen ters.44

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782 V Cerebral and Spinal Aneurysms

In th e m ajor it y of cases, en d ovascu lar in ter ven t ion is t h e n er ve palsy com pared w ith en dovascularly t reated pat ien t s.49 In
first - lin e t reat m en t of d ist al in fect iou s an eu r ysm s. Typ ically, th e absen ce of class I dat a, th e best available eviden ce su p p ort s
p aren t -vessel sacr ifice is u sed to exclu d e t h e an eu r ysm from th e idea th at clip obliterat ion yields bet ter ch an ces for recover y
t h e circulat ion ; th is can be accom plish ed w ith liqu id em bolic from a th ird n er ve palsy.
agents or w ith endovascular coils. However, retrograde filling and
rupture of the lesion m ay still occur after proxim al coil occlusion.
Th erefore, th e u se of liqu id em bolic agen t s su ch as Onyx (ev3
Neu rovascu lar, Ir vin e, CA) w ith p aren t-vessel sacrifice is com - ■ Socioeconomic Considerations
m on ly requ ired to ach ieve a du rable t reat m en t resp on se.45
Th e cost s to t reat an eu r ysm s via m icrosu rgical clip or en dovas-
cular coil obliterat ion m ay differ substan t ially, alth ough prelim i-
n ar y dat a are con flict ing. From a con cept ual fram ew ork, on e can
■ Posterior Communicating Artery hypoth esize th at a surgical procedure results in a longer h ospit al
st ay secon dar y to th e n at u re of h aving a m ajor cran ial op erat ion ,
w ith Third Nerve Palsy lead ing to in creased cost s. Th e cou n terp oin t w ou ld be th at coil
Poster ior com m u n icat in g ar ter y an eu r ysm s h ave a p rop en sit y obliterat ion m igh t n ot be as durable a t reat m en t as clipping an d
to com press cran ial n er ve III. Progn osis for recover y m ay differ m ight require m ore frequent surveillance angiography and poten-
d ep en d ing on t reat m en t m odalit y an d sh ou ld be con sid ered tially fu rth er t reat m en t . Addit ion ally, coil em bolizat ion m aterial
carefu lly alon g w it h ot h er st an dard factors. A grow in g body of m ay be su bst an t ially m ore expen sive th an a m icrosu rgical clip .
eviden ce suppor ts th e hypoth esis th at th e th ird n er ve palsy as- Th ese hypotheses h ave been investigated for the inpatient set-
sociated w ith th ese lesion s is m ore likely to recover w h en t reated t ing u sing a single large h ospit al system an d n at ionw id e h ealth
early an d w ith m icrosurgical clip obliterat ion , rath er th an w ith care dat abases. No st u dy h as yet an alyzed th e long-term longit u -
en d ovascu lar coiling.46,47 Som e st u dies also suggest th at com - din al costs of an eu r ysm t reat m en t related to m odalit y. In a st udy
plete recover y from th ird n er ve p alsy is p ossible w ith en dovas- in th e Un ited States of un ru pt u red an eu r ysm s t reated by eith er
cu lar t h erapy, alt h ough in ter p ret at ion of t h ese dat a is lim ited en d ovascu lar coiling or m icrosu rgical clipp ing, th e overall in -
by th e lack of h ead-to-h ead com parison an d by th e sm all coh or t creased ch arges related to t reat m en t w ere sign ifican tly at t ribu t-
size.48 A system at ic review of m ore th an 200 pat ien ts w ith pos- able to coiling.50 Th is ph en om en on w as also seen in a differen t
terior com m u n icat ing ar ter y an eu r ysm s an d t h ird n er ve p alsy an alysis of th e sam e database; h ow ever, it is possible th at th ose
con cludes th at su rgical t reat m en t w as associated w ith a sign ifi- differen ces w ere secon dar y to th e p resen t ing diagn osis an d site-
can tly h igh er rate of recover y from a com plete or p ar t ial th ird of-ser vice variat ion s.4 In a h igh -volum e h ospit al system , coiling

Fig. 65.5 Factors influencing the decision to clip or coil. Many factors strongly favor one treatment modalit y over the other. These generalizations
m ust be considered when evaluating a treatm ent m odalit y for intracranial m ust be considered in the context of all patient-specific and aneurysm -
aneurysm s. In the center of the balance are factors that can influence the specific characteristics, in addition to those shown here.
decision to clip or coil either way. Farther from the center are factors that

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65 Cerebral Aneurysms: To Clip or Coil? 783

w as also associated w ith h igh er inp at ien t costs for both ru pt u red
an d u n rupt ured an eur ysm s.51 Con t radictor y fin dings h ave also
■ Conclusion
been repor ted w h ere en dovascular t reat m en t w as associated “To clip or to coil” is at th e fulcrum of an eur ysm t reat m en t plan -
w ith low er h osp ital ch arges com p ared w ith su rger y.52 Given th e n in g (Fig. 65.5). Pat ien t s are best ser ved by a m u lt im odalit y
recen t scru t iny surrou n ding h ealth care expen dit ure an d cost- p rovider w h o can accurately w eigh th e risks an d ben efits of
effectiveness research, further studies are indicated. Ongoing ad- t reat m en t based on an eu r ysm ch aracterist ics, clin ical scen ario,
van ces in pat ien t care, su ch as elect ive an eur ysm coiling un der best available evid en ce, an d p rovid er skill level. Th is ongoing
procedu ral sedat ion , are effect ive an d m ay h elp to reduce h ealth d ialogu e en rich es th e field of n eu rovascular surger y. Pat ien t care
care cost s an d im prove efficien cy.53 an d clin ical outcom es w ill con t in u e to ben efit as a resu lt .

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for com plex basilar an d ver tebrobasilar jun ct ion an eur ysm s. Neurosur- 28. Hayakaw a M, Murayam a Y, Duckw iler GR, Gobin YP, Guglielm i G, Vi-
ger y 2013;72:763–775, discussion 775–776 ñ u ela F. Nat u ral h istor y of th e n eck rem n an t of a cerebral an eu r ysm
13. Kalan i MY, Zabram ski JM, Hu YC, Spet zler RF. Ext racran ial-in t racran ial t reated w ith th e Guglielm i det ach able coil system . J Neurosurg 2000;93:
bypass an d vessel occlusion for th e t reat m en t of un clippable gian t m iddle 561–568
cerebral ar ter y aneu r ysm s. Neu rosurger y 2013;72:428–435, discu ssion 29. Drake CG, Allcock JM. Postoperat ive angiography an d th e “slipped” clip.
435–436 J Neu rosu rg 1973;39:683–689
14. Pon ce FA, Spet zler RF, Han PP, et al. Cardiac st an dst ill for cerebral an eu- 30. el-Belt agy M, Muroi C, Roth P, Fan din o J, Im h of HG, Yon ekaw a Y. Recu rren t
r ysm s in 103 pat ien t s: an update on th e experien ce at th e Barrow Neu ro- in t racran ial an eur ysm s after successful neck clipping. World Neurosurg
logical In st it ute. Clin ical art icle. J Neurosu rg 2011;114:877–884 2010;74:472–477
15. Ogilvy CS, Carter BS. A proposed com preh ensive grading system to pre- 31. David CA, Vish teh AG, Spet zler RF, Lem ole M, Law ton MT, Par tovi S. Late
dict ou tcom e for su rgical m an agem en t of in t racran ial an eu r ysm s. Neu ro- angiograph ic follow -up review of surgically t reated an eur ysm s. J Neu ro-
surger y 1998;42:959–968, discu ssion 968–970 surg 1999;91:396–401

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32. Murayam a Y, Nien YL, Duckw iler G, et al. Guglielm i det ach able coil em bo- 44. Nussbaum ES, Madison MT, Goddard JK, Lassig JP, Nu ssbaum LA. Periph -
lizat ion of cerebral an eu r ysm s: 11 years’ experience. J Neurosurg 2003; eral in t racran ial an eur ysm s: m an agem ent ch allenges in 60 con secut ive
98:959–966 cases. J Neurosurg 2009;110:7–13
33. Slu zew ski M, van Rooij W J, Slob MJ, Bescós JO, Slu m p CH, W ijn alda D. 45. La Barge DV III, Ng PP, Steven s EA, Friedlin e NK, Kestle JR, Sch m idt RH.
Relat ion bet w een an eu r ysm volu m e, p acking, an d com p act ion in 145 Exten ded in t racran ial applicat ion s for ethylen e vinyl alcoh ol copolym er
cerebral an eu r ysm s t reated w it h coils. Rad iology 2004;231:653–658 (Onyx): m ycot ic an d d issect ing an eu r ysm s. Tech n ical n ote. J Neu rosu rg
34. Mericle RA, Wakh loo AK, Lopes DK, Lan zin o G, Guterm an LR, Hopkin s LN. 2009;111:114–118
Delayed an eu r ysm regrow th an d recan alizat ion after Guglielm i det ach - 46. Leivo S, Hern esn iem i J, Luukkon en M, Vapalah t i M. Early su rger y im -
able coil t reat m en t . Case repor t . J Neu rosu rg 1998;89:142–145 proves th e cure of an eur ysm -in du ced ocu lom otor palsy. Surg Neurol
35. Cogn ard C, Weill A, Spelle L, et al. Long-term angiograph ic follow -up of 1996;45:430–434
169 in t racranial berr y an eur ysm s occluded w ith det ach able coils. Radiol- 47. Chen PR, Am in -Hanjan i S, Albuqu erque FC, McDougall C, Zabram ski JM,
ogy 1999;212:348–356 Spet zler RF. Outcom e of ocu lom otor n er ve palsy from posterior com m u-
36. Lejeu n e JP, Th in es L, Tasch n er C, Bourgeois P, Hen on H, Leclerc X. Neuro- n icat ing ar ter y an eur ysm s: com parison of clipping and coiling. Neu rosur-
surgical t reat m en t for an eur ysm rem n an t s or recurren ces after coil occlu- ger y 2006;58:1040–1046, discussion 1040–1046
sion . Neurosurger y 2008;63:684–691, discussion 691–692 48. Zh ang SH, Pei W, Cai XS, Ch eng G. En dovascular m an agem en t an d recov-
37. Vezn edaroglu E, Benitez RP, Rosenw asser RH. Surgically t reated an eu- er y from ocu lom otor n er ve palsy associated w ith an eur ysm s of th e pos-
r ysm s previously coiled: lesson s learn ed. Neurosurger y 2004;54:300–303, terior com m unicating arter y. World Neurosurg 2010;74:316–319
discu ssion 303–305 49. Gü resir E, Sch uss P, Set zer M, Plat z J, Seifer t V, Vat ter H. Posterior com -
38. Zh ang YJ, Barrow DL, Caw ley CM, Dion JE. Neu rosurgical m an agem en t m un icat ing ar ter y an eur ysm -related ocu lom otor n er ve palsy: in fluen ce
of int racran ial an eur ysm s previously t reated w ith en dovascu lar th erapy. of surgical an d endovascular t reat m en t on recover y: single-cen ter series
Neurosu rger y 2003;52:283–293, discussion 293–295 an d system at ic review. Neu rosu rger y 2011;68:1527–1533, d iscu ssion
39. Hoh BL, Car ter BS, Put m an CM, Ogilvy CS. Im por t an t factors for a com - 1533–1534
bined n eurovascular team to con sider in select ing a t reat m en t m odalit y 50. Huang MC, Baaj AA, Dow n es K, et al. Paradoxical t ren ds in th e m an age-
for pat ien t s w ith previously clipped residu al an d recurren t in t racran ial m en t of un r upt ured cerebral an eur ysm s in th e Un ited St ates: an alysis of
aneur ysm s. Neurosurgery 2003;52:732–738, discussion 738–739 n at ionw ide dat abase over a 10-year period. St roke 2011;42:1730–1735
40. Pon ce FA, Albuquerqu e FC, McDougall CG, Han PP, Zabram ski JM, Spet zler 51. Hoh BL, Chi YY, Derm ot t MA, Lipori PJ, Lew is SB. Th e effect of coiling ver-
RF. Com bin ed en d ovascular an d m icrosu rgical m an agem en t of gian t an d sus clipping of rupt ured an d un rupt ured cerebral an eur ysm s on length of
com plex un ru pt ured an eur ysm s. Neu rosurg Focus 2004;17:E11 st ay, h ospit al cost , h ospit al reim bursem en t , an d surgeon reim bursem en t
41. Nussbaum ES, Nussbau m LA. A n ovel an eur ysm clip design for ath erom a- at th e un iversit y of Florida. Neu rosurger y 2009;64:614–619, discussion
tou s, th rom bot ic, or previou sly coiled lesion s: p relim in ar y experien ce 619–621
w ith th e “com pression clip” in 6 cases. Neurosurger y 2010;67(2, Su ppl 52. Higash ida RT, Lah ue BJ, Torbey MT, Hopkin s LN, Leip E, Hanley DF. Treat-
Op erat ive):333–341 m en t of un r upt ured in t racran ial an eur ysm s: a n at ionw ide assessm en t of
42. Nehls DG, Flom RA, Carter LP, Spetzler RF. Multiple intracranial aneur ysm s: effect iven ess. AJNR Am J Neuroradiol 2007;28:146–151
determ ining the site of rupt ure. J Neurosurg 1985;63:342–348 53. Ogilvy CS, Yang X, Jam il OA, et al. Neu roin ter ven t ion al procedures for u n -
43. Ph u ong LK, Lin k M, W ijdicks E. Man agem en t of in t racran ial in fect iou s rupt ured in t racran ial an eur ysm s u n der procedural sedat ion and local
an eur ysm s: a series of 16 cases. Neurosu rger y 2002;51:1145–1151, dis- an esth esia: a large-volu m e, single-cen ter exp erien ce. J Neu rosu rg 2011;
cussion 1151–1152 114:120–128

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VI Cerebral and Spinal Arteriovenous
Fistulas and Malformations

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66 Cerebral Arteriovenous Malformations
Moham ed Sam y Elham m ady, Seth Hayes, and Roberto C. Heros

An ar terioven ou s m alform at ion (AVM) is an abn orm al collect ion Oth er vascular lesion s, su ch as cavern ous m alform at ion s, du ral
of blood vessels con sist ing of direct fist ulous con n ect ion s be- AVMs an d fist ulas, an d vein of Galen m alform at ion s are covered
t w een ar teries an d vein s w ith ou t a n orm al in ter ven ing cap illar y in oth er ch apters.
bed or fun ct ion al n eu ral t issue. In h is w rit ings abou t th e t reat-
m ent of cerebrovascular m alform ation s, Har vey Cushing 1 in 1928
w rote,
■ Epidemiology and Relationships to
It w ould be n oth ing less th an foolh ardy to at tack on e of th e
deep -seated racem ose lesion s. . . . Th e su rgical h istor y of Other Vascular Malformations and
m ost of th e reported cases sh ow s n ot on ly th e fut ilit y of an Congenital Syndromes
operat ive at t ack upon on e of th ese angiom as but th e ex-
In t racran ial AVMs are u n com m on lesion s w it h an ill-d efin ed
t rem e risk of seriou s cor t ical dam age w h ich it en t ails. . . .
in cid en ce an d p revalen ce. Ou r kn ow ledge of t h e ep idem iology
How m any less su ccessfu l at tem pt s, m ad e by su rgeon s
of cerebral AVMs is largely based on dat a from autopsy series
less fam iliar w ith in t racran ial procedures, h ave gon e un re-
an d populat ion -based st udies. Autopsy dat a suggest th at th e fre-
corded m ay be left to th e im agin at ion .
qu en cy of AVM detect ion is 4.3%.3,4 In p op u lat ion -based st u dies
Sin ce th e discou raging early su rgical exp erien ce of Cu sh ing an d th e repor ted in ciden ce rates w ere 1.1 per 100,000 p erson s in
h is con tem poraries, w e h ave m ade t rem en dous advan ces in our Olm sted Cou n t y, Min n esota,5 1.34 p er 100,000 p erson -years in
u n d erst an d in g of t h e p at h ogen esis, clin ical p resen t at ion , an d th e New York Islan ds AVM st u dy (covering Man h at t an Islan d,
n at u ral h istor y of cerebral AVMs. Fu r t h er m ore, m ajor develop - St aten Islan d, an d Long Islan d),6 1.12 per 100,000 adu lt s p er year
m en t s h ave been m ade in m icrosu rgical, en dovascular, an d ra- in th e Scot t ish In t racran ial Vascu lar Malform at ion St u dy,7 an d
diosu rgical t reat m en t of th ese lesion s. Th is ch apter review s th e 0.89 per 100,000 person -years in w estern Au st ralia.8–10 Preva-
epidem iology, clin ical feat u res, an d n at u ral h istor y of cerebral len ce data in th e literat u re range from 18 per 100,000 peop le
AVMs; discusses th e in dicat ion s an d outcom es of th e various (0.02%) in a ret rospect ive an alysis in Scotlan d to 0.2%in an an aly-
t reat m en t m odalit ies; an d describes th e su rgical tech n iqu e an d sis of 2,500 asym ptom at ic Ger m an m ales.7,11 Alt h ough t h ese
n uan ces of AVM resect ion in par t icular locat ion s. lesion s are 10 t im es less com m on th an in t racran ial an eur ysm s,
th ey accou n t for 2% of all st rokes an d 38% of in t racerebral h em -
orrh ages in pat ien ts bet w een 15 an d 45 years of age.12–14
Th e p ath ogen esis of AVMs rem ain s con t roversial. Th ey are
■ Classification of Cerebrovascular gen erally believed to be developm en tal lesion s, alth ough th ere is
eviden ce th at th ey m ay be acquired. It h as been suggested th at
Malformations reten t ion of th e p rim ordial arterioven ou s con n ect ion s from th e
Cerebrovascular m alform at ion is a gen eral term en com p assing fet al in t racran ial vasculat ure,15 or failu re of developm en t of an
several dist in ct en t it ies, each w ith a differen t m icroscop ic st ru c- in ter ven ing capillar y n et w ork,16 cou ld resu lt in th e d evelop m en t
t u re, physiology, an d clin ical beh avior. Th e m ost w idely accepted of AVMs. Altern at ively, it h as been p ost ulated th at th e prim ar y
classificat ion of cerebrovascu lar m alform at ion s w as t h at p ro- abn orm alit y in AVM path ogen esis lies w ith in a dist urbed ven ous
posed by McCorm ick.2 In th is sch em e vascular m alform at ion s d rain age system .17,18 Ven ou s hyp er ten sion h as been p rop osed
are divided in to th e follow ing four m ajor t ypes based on th e n a- to in crease in t ralum in al pressure, redu ce t issu e perfusion , an d
t ure of th e com pon en t vessels an d th e com posit ion of th e in ter- result in diapedet ic h em orrh age, all of w h ich can lead to local
vening neural tissue: (1) arteriovenous m alform ations, (2) venous increases in angiogenic factors.19 Venous outflow restriction m ay
m alform at ion s, (3) cavern ous m alform at ion s, an d (4) capillar y open preexist ing ar terioven ou s con n ect ion s, result ing in ar terio-
telangiect asia. Th e u sefu ln ess of t h is classificat ion system is ven ou s sh u n t s t h at can en large over t im e.19 Th e occasion al co-
d em on st rated by t h e fact t h at each t yp e of lesion h as d ist in ct existen ce of m ore th at on e t yp e of vascu lar m alform at ion , also
clin ical an d rad iograp h ic feat u res. kn ow n as “m ixed cerebrovascular m alform at ion s,” h as been w ell
Th is ch apter focu ses on p aren chym al ar terioven ou s m alfor- recogn ized .20 Sim ilarly, n um erous repor t s h ave n oted abn orm al
m at ion s, th at is, lesion s w ith in th e brain substan ce con sist ing of pat tern s of ven ou s drain age in associat ion w ith AVMs, telangiec-
direct fist u lous con n ection s bet w een ar teries an d vein s w ith out tasias, an d cavern ous angiom as; n ever th eless, it rem ain s un clear
a n orm al in ter ven ing capillar y bed or fun ct ion al n eural t issue. w h eth er th is associat ion represen ts a t r ue cause-an d-effect rela-

787

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788 VI Cerebral and Spinal Arteriovenous Fistulas and Malform ations

t ion sh ip or sim p ly a coin cid en t al expression of in ap prop riately Seizures


form ed cerebral vascu lat u re.18
Seizu res represen t th e secon d m ost com m on t yp e of p resen t a-
Cerebral AVMs are m ost com m on ly d iscovered in th e t h ird
t ion in p at ien t s w ith su p raten torial AVMs, occu rring in alm ost
or four th decade of life; h ow ever, th ey can presen t at any age.
70% of pat ien ts. Seizures w ith out obvious h em orrh age are seen
St udies h ave n ot revealed con sisten t gen der predom in an ce.
in 25 to 50% of cases; 18 to 35% of pat ien t s w ith an AVM are di-
AVMs can be located in a w ide variet y of an atom ic locat ion s,
agn osed du ring evalu at ion for a seizu re.28–33 Th e average age of
w ith th e supraten torial com par t m en t being th e m ost com m on .
on set is 25 years. Sim ple an d com plex par t ial seizures are th e
Th e cerebellu m is t h e m ost com m on locat ion in th e posterior
m ost com m on t ypes recogn ized. Th e path ophysiology of seizure
fossa, w h ereas brain stem an d ven t ricular locat ion s are less com -
d evelop m en t m ay be secon dar y to m ass effect an d cor t ical ir-
m on .21–23 Th ese m alform at ion s are u su ally solitar y, but m ult iple
r it at ion , h em odyn am ic alterat ion s leading to isch em ia, or gliosis.
lesion s h ave been repor ted in 1 to 9% of pat ien ts.12,24
Seizu res h ave been fou n d to occu r m ore frequ en tly w ith AVMs
Cerebral vascu lar m alfor m at ion s can occu r in associat ion
h aving on e or m ore of th e follow ing feat ures: large size, m iddle
w ith w ell-d efin ed gen et ic d isord ers. St u rge-Weber syn d rom e,
cerebral ar ter y (MCA) dist ribut ion , cor t ical locat ion of th e n idus
also kn ow n as en ceph alot rigem in al angiom atosis, is a n eurocu-
or ar terial feeders, an d th e presen ce of ven ous varices.37,38
taneous syn drom e w ith n o obvious m ode of gen et ic t ran sm is-
sion . It is ch aracterized by cu tan eou s angiom as (por t-w in e st ain )
involving th e face in th e dist ribu t ion of th e t rigem in al n er ve an d Progressive Neurologic Deficit
an ipsilateral leptom en ingeal vascular m alform at ion . Th e vascu -
lar lesion t ypically involves an atroph ic parieto-occipital lobe and Approxim ately 3 to 10% of pat ien ts h arboring a cerebral AVM
con sist s of th in -w alled su barach n oid an d p ial vessels resem bling p resen t w it h a p rogressive n eu rologic d eficit in t h e absen ce of
capillar y an d ven ou s ch an n els. Associated dyst rop h ic calcifica- h em or rh age.39 Th e u n d erlying p at h op hysiology is secon dar y
t ion s in th e m iddle layers of th e gray m at ter cen tered on th e ce- to m ass effect or due to isch em ic steal. Mass effect m ay occur as
rebral m icrovessels produce the classic curvilinear double parallel a resu lt of d irect p ressu re by t h e AVM or cerebral edem a in
lin es or t ram t racks seen on p lain rad iograp h s or com p uted to- th e su rrou n ding p aren chym a. Isch em ic steal is th ough t to resu lt
m ography (CT) scan s. Pat ien t s suffer severe in t ractable epilepsy from th e h igh -flow, low -resist an ce p ath w ay created by th e AVM.
early in life and m ay be m entally challenged. Rendu-Osler-Weber Cerebral blood flow (CBF) from th e adjacen t t issu e is th ough t to
syn d rom e, also kn ow n as h ered it ar y h em or rh agic telangiect a- be lost to th e path ological m alform at ion . Th is m ay lead to vari-
sia, is an autosom al dom in an t gen et ic disorder due to m utat ion ous sym ptom s, depen ding on th e an atom ic locat ion of th e isch -
in th e t ran sform ing grow th factor-β (TGF-β) receptor gen e. It is em ia. Larger AVMs an d cer t ain sh u n t ch aracter ist ics are m ore
ch aracterized by vascu lar m alform at ion s involving cu t an eou s, likely to lead to sym ptom at ic isch em ic steal. Tran scu t an eou s
m ucosal, an d visceral t issues. Cerebral vascular lesion s in clude Dop p ler evalu at ion h as d isp layed h igh er velocit ies an d greater
telangiectasias or m ult iple AVMs. Wyburn -Mason syn drom e is flow volu m es in th is p at ien t pop ulat ion .40
ch aracterized by u n ilateral cu t an eou s n evi an d AVMs involving
th e ret in a, opt ic n er ve, an d dien cep h alon .25 Headache
Approxim ately 6 to 14% of pat ien t s w ith cerebral AVMs presen t
w ith chronic headaches w ithout hem orrhage. The pattern of head-
■ Clinical Presentation and ach e is t ypically h em icran ial (ipsilateral or con t ralateral to th e
m alform at ion ) an d sim ilar to m igrain es; h ow ever, th e in ciden ce
Pathophysiology of m igrain e h eadach es in pat ien t s w ith AVMs does n ot exceed
Th e clin ical presen t at ion or discover y of AVMs can be classified that of the general populat ion.41 Patients w ith occipital AVMs m ay
into five basic categories: intracerebral hem orrhage, seizures, neu- be m ore pron e to h eadach e presen t at ion . W h en th e h eadach es
rologic deficit , h eadach es, an d in ciden tal or asym ptom at ic are m igrain ous in ch aracter in pat ien t s w ith occipital AVMs, th ey
lesion s. characteristically occur on th e side of the AVM. Visual phenom -
ena, w hen they occur, are alw ays on the contralateral visual field.41
Th is con sisten cy in th e lateralizat ion of th e m igrain e d ifferen t i-
Intracerebral Hemorrhage ates pat ien ts w ith occip ital AVMs from pat ien ts w ith classic m i-
In t racerebral h em orrh age rem ain s th e m ost com m on an d dan - grain e in w h ich th e h eadach es t ypically ch ange sides. Th erefore,
gerou s p resen tat ion . Historically, AVM ru pt ure w as respon sible w h en a pat ien t w ith m igrain es con sisten tly repor ts th at th e
for th e in it ial presen t at ion of greater th an 70% of pat ien ts.26,27 h eadach e an d visual ph en om en a occur on th e sam e side, an im -
More recent review s of large m odern series found that 45 to 72% aging st u dy is in dicated to ru le ou t an organ ic lesion su ch as an
of p at ien ts presen t w ith h em orrh age.28–33 Accordingly, AVMs are AVM. Th e path ophysiology is hypoth esized to be caused by th e
respon sible for on e-th ird of h em orrh agic stokes in you ng adults,34 recruit m en t of m en ingeal ar teries an d in creased blood flow.
secon d on ly to r u pt u re of an ar terial an eu r ysm . In t raparen chy-
m al h em orrh age is th e m ost com m on t ype of bleed, follow ed by
in t raven t ricu lar an d subarach n oid h em orrh ages. Most p at ien t s
Asymptomatic
experience their first hem orrhage w hen th ey are 20 to 40 years of As d escr ibed , m ost p at ien t s are d iagn osed w it h AVMs follow -
age.32 Est im ated m or t alit y an d perm an en t m orbidit y w ith each in g p resen t at ion w it h h em or rh age or seizu re; h ow ever, w ith
hem orrhage are 10 to 30%and 20 to 30%, respectively.21,26,27,30,35,36 t h e in creased u t ilizat ion of n on invasive im aging, in ciden tal dis-

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66 Cerebral Arteriovenous Malformations 789

cover y in p at ien t s evalu ated for a variet y of reason s is n ot u n - rebral AVMs, 94 pat ien t s (36%) un der w en t t reat m en t . Eigh t cases
com m on. This proportion has increased to 10% in m odern series, from th e rem ain ing 168 (64%) u n t reated pat ien ts w ere exclu ded
com p ared w ith a h istorical rate of less th an 2%.39 In terest ingly, in from the study because of death, subsequent inter vention, or loss
a single populat ion -based st udy of in tracerebral vascular m al- of follow -u p . Th e rem ain ing 160 u n t reated pat ien t s com p rised
form at ion s, 40% w ere asym ptom at ic.42 th e “n at ural h istor y coh ort .” Clin ical presen t at ion in cluded h em -
orrh age in 71%an d seizu res in 25%. Th e rem ain ing pat ien t s w ere
asym ptom at ic or p resen ted w ith h eadach e or vagu e sym ptom s.
Th e m ean follow -up period w as 23.7 years an d w as rem arkably
available in 98% of pat ien ts. Du ring th e follow -u p p eriod, 64 p a-
■ Natural History t ien t s suffered at least on e h em orrh age (range 1–12 even ts). A
Th e m an agem en t of pat ien t s w ith cerebral AVMs is based on an tot al of 147 n ew h em or rh ages w ere obser ved , resu lt in g in an
understanding of the natural history and the risk of intervention. an n u al bleed rate of 4%. Th e m ean in ter val bet w een presen tat ion
Several series h ave evalu ated t h e n at u ral h istor y of AVMs an d su bsequ en t h em orrh age w as 7.7 years. Th e yearly m orbidit y
w it h regard to t h e r isk of h em orrh age (Table 66.1). In a ser ies rate w as 1.7%, an d th e m or talit y rate w as 1%. In terest ingly, th e
of 168 p at ien t s w it h ou t a h istor y of p reviou s h em or rh age, 18% yearly rate of h em orrh age for th ose AVMs th at h ad n ever bled in
of pat ien t s h ad subsequen t h em orrh age at a m ean follow -u p of pat ien t s w h o p resen ted w ith seizures or w ith vague sym ptom s
8.2 years.42 Th e an n u al r isk of h em or rh age w as 2.2%. In a st u dy w as ver y sim ilar: 4.3% per year for seizu res an d 3.9% p er year for
of 191 p at ien t s rep or ted by Graf et al,35 102 h ad a single bleed, vagu e sym ptom s. Alth ough th e st u dy provided valu able in for-
32 h ad a recurren t h em orrh age, an d 57 n ever bled. Th e m ean m at ion regard in g th e n at u ral h istor y of cerebral AVMs, it h ad
follow -up period for pat ien ts w ith unr upt ured an d rupt ured several w eakn esses. First , th e st udy su ffered a select ion bias, as
AVMs w as 4.8 an d 2 years, resp ect ively. Th e an n u al risk for h em - 97 pat ien t s from th e origin al 262 p at ien t s u lt im ately u n der w en t
orrh age in pat ien t s w ith n o h istor y of a previous bleed w as 2 to in ter ven t ion . Secon d, th e diagn osis of h em orrh age w as m ade
3%. Am ong th e pat ien t s follow ed after th eir AVM r upt ured, th e prior to th e availabilit y of CT an d w as based on clin ical su spicion ,
risk of rebleeding w as 6%in t h e first year, after w h ich th e average a posit ive lu m bar pu n ct u re, or eviden ce of brain sh ift on radio-
rebleeding rate fell to a con st an t level of 2% per year for 20 grap h s. Fin ally, t h e an n u al h em or rh age rate w as calcu lated by
years.35 Craw ford et al27 rep or ted a ret rosp ect ive st u dy of 217 dividing all even t s by t h e years of follow -u p . Pat ien t s w it h sev-
pat ien ts w ith AVMs m an aged w ith ou t su rger y. Most (64%) pa- eral h em orrh agic even ts w ere in cluded, an d th u s th e an n u al
t ien ts in it ially p resen ted w ith h em orrh age. Th e m ean follow -u p bleed rate m ay h ave been falsely exaggerated.
of 10.4 years yielded an an n u al h em orrh age rate of 3.4%. Sur vival Som e invest igators h ave expressed con cern s over th e use of
an alyses sh ow ed a 42% risk of h em orrh age, a 29% risk of death , dat a from th e classic n at ural h istor y st udies by On dra et al 26 an d
an 18% risk of epilep sy, an d a 27% risk of a n eu rologic h an dicap Craw ford et al27 to ju st ify t reat m en t of pat ien t s h arboring u n -
by 20 years after diagn osis in u n op erated pat ien ts. rupt u red AVMs.43 Th ey poin t ou t th at th e m ajorit y of pat ien ts in
An im por tan t st udy on th e n at ural h istor y of cerebral AVMs th ese st u dies in it ially p resen ted w ith h em orrh age, an d th at th e
from th e Un iversit y of Helsin ki w as repor ted by On dra et al26 in rep orted an n ual bleed rates represen t a blen d of th e n at ural h is-
1990. Am ong 262 pat ien t s w ith angiograph ically diagn osed ce- tor y of both previously ru pt ured an d un r upt ured AVMs. Th ese

Table 66.1 Natural History Studies for Arteriovenous Malformations (AVMs)

Average Follow -Up


Author (Year) Type of Study No. of Patients (Years) Annual Hemorrhage Rate

Graf et al (1983)35 Retrospective 191 4.8 2–3% in patients without hem orrhage; 6% the
first year after hemorrhage, then 2% in
patients with hemorrhage
Crawford et al Retrospective 217 10.4 2%; 36% cumulative risk at 10-year follow-up in
(1986)27 patients with hemorrhage; 17% in patients
without hemorrhage
Brown et al (1988)21 Retrospective 168 (all unruptured) 8.2 2.2% m ean risk of hemorrhage per year

Ondra et al (1990)26 Retrospective 160 23.7 4% overall; 3.9% in patients with hemorrhage;
4.3% with seizure; 3.9% with other symptoms
Mast et al (1997)32 Prospective 281 1.0 2.2% in patients without hemorrhage; 17.8% in
patients with hemorrhage
Halim et al (2004)31 Retrospective 790 4.0 7% the first year after presentation with hem or-
rhage compared to 3% after presentation with-
out hemorrhage, then 3% for both over time
Stapf et al (2006)28 Prospective database 622 102 days 1.3% for unruptured AVMs and 5.9% for patients
with AVMs who presented with hemorrhage
Hernesniemi et al Retrospective 238 13.5 years 2.4% overall; three times higher in the first 5
(2008)44 years (4.6%) than in subsequent years (1.6%)

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investigators hypothesize that the classic data likely overestim ate w ere st at ist ically sign ifican t r isk factors for rebleed . Mu lt ivar i-
th e h em orrh age rate am ong u n ru pt u red AVMs an d u n derest i- ate an alysis dem on st rated th at size, deep locat ion , deep ven ou s
m ate th e rebleed rate am ong rupt ured AVMs. Th e n ot ion th at th e drain age, an d th e p resen ce of an ar terial an eu r ysm w ere risk fac-
an n ual hem orrh age rate is sim ilar for rupt ured an d un r upt ured tors. Upon evaluat ing th e risk of h em orrh age during follow -up,
AVMs h as recen tly been ch allenged based on n ew dat a glean ed univariate and m ultivariate analysis dem onstrated that older age,
from t w o large p rosp ect ive AVM dat abases at th e Un iversit y of hem orrhagic presen tation, deep location, and deep venous drain -
Helsin ki an d Colum bia Un iversit y. age w ere in dep en d en t risk factors for rebleed. Th e at t ribu table
In 2008 Hern esn iem i et al44 reported a follow -u p st udy to th e risk of AVM h em orrh age at follow -u p w as 47.7%for p at ien t s w ith
origin al Un iversit y of Helsin ki st u dy. A total of 631 AVMs w ere h em orrh age at presen tat ion , 9.4% w ith deep brain locat ion , an d
evalu ated from 1942 to 2005; 393 pat ien ts w h o rebled or w ere 13.9% w ith deep ven ous drain age. Overall, 6% (39 pat ien t s) bled
t reated w ith in 30 days of diagn osis w ere exclu ded. Th e rem ain - du ring follow -u p , for an average an n u al rate of h em orrh age of
ing 238 pat ien t s w ere in cluded in th e grou p of un t reated p a- 2.8%. Th e est im ates for an n ual rate of h em orrh age w ere 1.3% for
t ien ts. Th is w as in addit ion to th e 160 u n t reated pat ien ts in th e u n ru pt u red AVMs an d 5.9%for AVMs in p at ien t s presen t ing w ith
origin al st udy. Rath er th an d ividing all even ts by years of follow - hem orrhage. In terestingly, average ann ual hem orrhage rates w ere
up , th e auth ors perform ed a Kaplan -Meier an alysis from presen - an alyzed for four differen t subgroups based on th e discovered
tation until first rebleed. Furtherm ore, unlike in the original study, in depen den t risk factors. In AVMs w ith ou t deep ven ous drain age
th e diagn osis of h em orrh age w as based on ly on CT eviden ce. Of an d located su perficially, th e an n u al rate of h em orrh age w as
n ote, th ere w ere pat ien ts presen t ing w ith a h eadach e w h o did 0.9% w ith out a prior bleed an d 4.5% in pat ien ts w h o presen ted
n ot h ave a h em orrh age. Th e average follow -up w as 13.5 years. w ith a bleed. In pat ien t s w ith deep ven ous drain age but w ith a
Th e overall an n u al ru pt u re rate w as 2.4%. Th e rate w as th ree su p erficial locat ion , th e an n u al risk w as 2.4%in p at ien ts w ith ou t
t im es h igh er in th e first 5 years (4.6%) th an in su bsequ en t years a p rior bleed an d 11.4% in th ose w ith a prior h em orrh age. In pa-
(1.6%). Th is in terest ing obser vat ion im p lies th at a h em odyn am ic t ien t s w it h ou t d eep ven ou s d rain age bu t a d eep locat ion , t h e
ch ange m ay alter th e risk of rupt u re. Several factors w ere asso- an n ual rupt ure risk w ith out a bleed w as 3.1%an d th e rate w ith a
ciated w ith a greater risk of r upt ure. A previous rupt u re, deep prior bleed w as 14.8%. Th e last grou p w as com p rom ised of AVMs
or in fraten torial locat ion , younger age, an d deep ven ou s drain age w ith deep ven ous drain age an d a deep an atom ic locat ion . In th is
(on ly in th e first 5 years) w ere risk factors in u n ivariate an alysis. grou p th e an n ual risk of h em orrh age w ith out a p rior bleed w as
Mu lt ivariate an alysis revealed th at , du ring th e first 5 years, a 8% an d th e risk w ith a prior h em orrh age w as 34.3%. Th is reveals
previou s h em orrh age or a deep locat ion w ere risk factors. After a risk ranging from 0.9% to 34.3%, based on previously defin ed
5 years, risk factors in cluded previous h em orrh age, deep or in - risk factors.
fraten torial locat ion , an d large size. Th e h em orrh age risk varied Th e recen t eviden ce th at u n ru pt u red AVMs m ay carr y a m ore
from 12% for in fraten torial AVMs in th e first 5 years to 1% for ben ign n at ural h istor y th an rupt u red AVMs led to th e in it iat ion
su praten torial AVMs after 5 years. In th is st u dy, deep locat ion of th e ARUBA t r ial (A Ran d om ized t r ial of Un r u pt u red Brain
an d previou s rupt ure in creased th e relat ive risk of r upt ure 4 fold. Ar terioven ous m alform at ion s).45 Th is w as an NIH-fu n ded m u lt i-
Large size w as foun d to be a risk factor for h em orrh age on ly in cen ter ran dom ized st u dy d esign ed to d eter m in e w h et h er p ro -
m ult ivariate an alysis. Because pat ien ts w ith sm all AVMs presen t p hylact ic in ter ven t ion (en d ovascu lar, su rgical, an d rad iat ion
w ith hem orrhage m ore frequently, it is likely that univariate anal- th erapy, alon e or in com bin at ion ) for u n r upt ured AVMs or defer-
ysis falsely raises their bleed rate to equal that of patients w ith ral of in ter ven t ion u n less h em or rh age occu r red w ou ld p rove
large AVMs. How ever, in m ultivariate an alysis it is only w h en th e su perior. Th e prim ar y en dpoin t w as th e com posite m easure of
in flu en ce of previou s h em orrh age is rem oved an d th e t w o sizes any st roke or death an d th e secondar y an alysis w as overall fun c-
are separated th at large size sh ow s up as an in creased predictor t ion al st at u s an d qu alit y of life at a m in im u m of 5 years from
of bleeding. Th us, pat ien ts w ith sm all AVMs are m ore likely to ran d om izat ion . In it ially t h e st u dy w as d esign ed to ran d om ize
present w ith hem orrhage because they do not present w ith sym p - 800 pat ien ts w ith un r upt ured cerebral AVMs, but due to difficul-
tom s secon dar y to m ass effect or seizu res; h ow ever, sm all AVMs t ies w ith pat ien t en rollm en t an d after an in terim an alysis th e
are less likely to rebleed th an are large AVMs. Large size h as n ot n um ber of pat ien ts in ten ded for ran dom izat ion w as revised to
been foun d to be a risk factor in oth er st udies. But n on e of th e 400. Even before en rollm en t began in April 2007 th e st udy de-
st u d ies u sing Kap lan -Meier an alysis an d Cox m od els h ave sh ow n sign of th e ARUBA t r ial h ad been h eavily cr it icized for several
t h at sm all size p red ict s AVM r u pt u re. Th erefore, h em or rh age reason s, w h ich w e w ill d iscu ss below . Perh ap s t h e greatest cr it -
an d large size ad d to t h e r isk of reh em or rh age. Differen ces in icism w as th e p rop osed 5-year follow -u p period, w h ich m any
resu lt s, com pared w ith th ose of On dra et al,26 in clu de a low er thought w ould detect all procedure-related com plicat ions but
an n ual risk of rupt u re (2.4% vs 4%) an d a variable risk of rupt ure w ould be too short to detect the potential long-term benefit of
bet w een rupt ured an d u n rupt ured AVMs. Th ese fin dings can be intervention w ith regards to hem orrhage prevention. It was th ere-
explain ed by differen ces in stat ist ical m eth odology. fore n ot surprising th at th e st u dy w as prem at urely stopped by
Ut ilizing th e Colu m bia prosp ect ive AVM dat abase th at w as th e dat a safet y m on itoring board du e to excessive m orbidit y in
in it iated in 1989, St ap f et al28 review ed th e d em ograph ic, clin i- th e t reat m en t arm as com p ared w ith th e con ser vat ively t reated
cal, an d m orp h ological feat u res of 622 pat ien t s diagn osed w ith coh or t . A tot al of 223 p at ien t s h ad been en rolled in th e t rial w ith
an AVM. In total, 282 (45%) presen ted w ith a bleed. Th e m ean a m ean follow -u p of approxim ately 33 m on th s. Baselin e pat ien t
pret reat m en t follow -u p w as 829 days; 438 pat ien ts (70%) w ere dem ograp h ics w ere sim ilar bet w een th ose ran d om ized to m edi-
t reated w ith in 12 m on th s. In pat ien ts p resen t ing w ith a bleed, cal therapy (n = 109) and those assign ed to in ter vent ion (n = 114).
un ivariate an alysis fou n d th at in creased age, in fraten torial an d Th e prim ar y ou tcom e of death an d st roke w as seen in 11 pa-
d eep locat ion , d eep ven ou s d rain age, an d an ar ter ial an eu r ysm t ien ts (10%) in th e m edical group an d 33 p at ien ts (29%) in th e

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66 Cerebral Arteriovenous Malformations 791

in ter ven t ion grou p . Mort alit y w as sim ilar in both grou ps. Ou t- brain . An AVM t ypically appears as a t igh tly packed “h on eycom b”
com es based on Sp et zler-Mar t in grading w ere sim ilar for grad e I of flow voids on T1- an d T2-w eigh ted im ages. Secon dar y ch anges
an d II lesion s, bu t w ere sign ifican tly w orse for t reated grade III in t h e adjacen t brain t issu e su ch as m ass effect , ed em a, an d
an d IV AVMs. isch em ic ch anges can also be seen . MRI in conju n ct ion w ith an -
Th e ARUBA st u dy su ffers several m eth odological lim it at ion s giography provides com plem en tar y in form at ion th at facilit ates
com m on to m ost p rosp ect ive, ran dom ized, con t rolled t rials. An understanding the three-dim ensional structure of the nidus, feed-
in h eren t select ion bias clearly lim its th e gen eral app licabilit y of ing arteries, an d drain ing vein s. How ever, m agn et ic reson an ce
th e resu lt s. Fu r th erm ore, it is p ossible th at su ch a bias skew ed angiography (MRA) curren tly can n ot replace conven t ion al cere-
th e st u dy tow ard n o ben efit from in ter ven t ion becau se it is rea- bral angiography. Although MRI is sensitive in revealing subacute
son able to p resu m e th at p at ien t s w ith favorable risk to ben efit h em orrh age, in th e set t ing of acute h em orrh age it is vir t ually
rat ios w ere likely t reated ou t side th e t rial an d on ly th ose p a- u seless because th e h em atom a obscu res all det ails of th e AVM.
t ien ts in w h o clin ician s w ere really n ot su re w ou ld ben efit from We recom m en d obtain ing a form al cerebral angiogram if th e
in ter ven t ion w ere referred for ran dom izat ion . An oth er w eak- clin ical h istor y an d th e im aging ch aracterist ics of th e h em atom a
n ess of th e st udy w as th at th e in clusion criteria w ere too gen eral. suggest th e presen ce of an AVM.
A young pat ien t w ith a Spet zler-Mar t in grade I fron to-polar AVM
an d an elderly pat ien t w ith a grade IV lesion w ere both eligible
for ran dom izat ion , alth ough th e risk of surgical in ter ven t ion is
Angiography
ext rem ely low in th e form er case an d yet su bst an t ial in th e lat ter. Cerebral d igit al su bst ract ion angiograp hy (DSA) is st ill con sid -
An oth er lim itat ion of ARUBA is th e lack of st rat ificat ion of in ter- ered t h e gold st an dard to est ablish t h e d iagn osis an d to p re-
ven t ion al th erapies. Th ere is a diversit y of AVM risk feat ures an d operat ively assess a pat ien t w ith an AVM. Th is st u dy can provide
variou s m u lt im odal t reat m en t pat tern s; h ow ever, th e st u dy w as valuable in form at ion regarding size, locat ion , an d con figurat ion
n ot pow ered to evaluate th e t reat m en t effect by in dividual m o- (com pact versus diffuse) of th e AVM n idus as w ell as th e pat tern
dalit y. Fu r th erm ore, oth er sh or t-term ben efits of AVM t reat m en t an d locat ion of feeding ar teries an d drain ing vein s. In addit ion ,
su ch as alleviat ion of h eadach es, con t rol of seizu res, an d redu c- DSA m ay detect th e presen ce of angioarch itect ural feat ures as-
t ion of ven ou s hyper ten sion or ar terial steal w ere n ot addressed sociated w ith an in creased risk of h em orrh age, su ch as feeding
by t h e p r im ar y en d p oin t . Fin ally, as w e m en t ion ed above, on e ar ter y or in t ran idal an eur ysm s,48–52 d eep ven ou s drain age,29 ve-
of t h e greatest w eakn ess of t h e ARUBA t r ial is t h e sh or t -ter m n ou s an eu r ysm or ou t flow com p rom ise,53 p er forat in g feed in g
follow -up. Alth ough , th e ARUBA st udy plan s to follow th e cur- vessels,54 an d deep or periven t ricular locat ion . Extern al carot id
ren t coh ort of p at ien t s for an addit ion al 5 years, it is un clear if inject ion s sh ou ld be p erform ed in large convexit y AVMs, par t ic-
th is w ill be su fficien t to determ in e w h eth er or n ot in ter ven t ion u larly in p at ien t s w it h a h istor y of p reviou s su rger y, em boliza-
offers a ben efit over th e n at u ral h istor y w ith regard to h em or- tion, or h em orrhage, as these lesions m ay recruit external carotid
rh age p reven t ion d u r ing t h is sh or t in ter val of follow -u p . Be- ar terial sup ply. Th e t im ing of DSA follow ing a h em orrh age is also
cau se p at ien t s h arbor in g cerebral AVMs are t yp ically you n g at crit ical. Vessels that were not visualized on an early angiogram
t h e t im e of diagn osis an d exp osed to a lifelong cu m u lat ive risk of secondar y to com p ression from a h em orrh age m ay ap pear on a
fu t u re h em orrh age, w e su sp ect th at th e plan n ed 5-year addi- follow -up DSA several w eeks later. Fur th erm ore, it is im por t an t
t ion al follow -u p w ill also n ot su ffice. For a th orough discu ssion th at an angiogram be p erform ed close to th e t im e of su rger y, as
on oth er sh or tcom ings of th is t rial, th e reader is referred to sev- AVMs can ch ange in size an d con figurat ion over t im e.
eral excellen t editorials.46,47

Functional Evaluation
Measu ring th e fu n ct ion alit y of cor t ical st ru ct u res adjacen t to
■ Imaging AVMs is crit ical w h en assessing th e risk of in ter ven t ion . Several
tech n iques are available, in cluding posit ron em ission tom ogra-
Computed Tomography phy (PET), fu n ct ion al MRI (fMRI), an d m agn etoen cep h alograp hy
A CT scan is th e prim ar y n euroradiograph ic screen ing tool for (MEG). In form at ion glean ed from th ese st udies en ables th e sur-
pat ien ts presen ting w ith acu te n eu rologic sym ptom s related to geon to tailor t reat m en t m odalit ies.
u n rupt u red or ru pt ured AVMs. A n on con t rast CT m ay dem on - Positron em ission tom ography en ables clin icians to accurately
st rate th e p resen ce of acu te h em orrh age, hydroceph alu s, calcifi- qu an t it ate both local cerebral fu n ct ion an d blood flow u sing ra-
cat ion , or areas of en cep h alom alacia related to p reviou s su rger y dioact ively labeled flu orodeoxyglucose an d w ater, resp ect ively.
or rupt u re. On th e oth er h an d, a con t rast CT can provide in for- Region al m etabolic act ivit y is determ in ed in directly by m easu r-
m at ion regarding th e AVM locat ion , n idus, feeding arteries, an d ing th e u t ilizat ion of glucose an d CBF on a relat ive scale as fun c-
d rain ing vein s, an d it is p ar t icu larly valu able as a qu ick st u dy t ion al t asks geared tow ard st im u lat ing th e cor tex in qu est ion are
in t h e set t ing of a life-t h reat in g h em or rh age p r ior to su rgical u n dertaken by th e pat ien t . PET im ages can th en be m app ed on to
evacuat ion . m agn et ic reson an ce (MR) im ages to est im ate th e proxim it y of
fun ct ion ally act ive cort ical t issu e to AVM locat ion .
Fu n ct ion al MRI u ses t h e ch ange in m agn et izat ion bet w een
Magnetic Resonance Imaging oxygen -rich an d oxygen -poor blood as it s basic m easu re. Local
Magn et ic reson an ce im aging (MRI) is su p erior to CT im aging in in creases in CBF during t ask act ivat ion result in greater oxygen -
delin eat ing th e m acro-arch itect u ral details of th e AVM, as w ell ated blood levels, w h ich are seen as in creased sign al ch ange on
as in defin ing it s exact an atom ic relat ion to th e surroun ding MRI. Th ese MR sequen ces are run repet it ively during th e on an d

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off states of th e task. Su bsequ en tly, act ivat ion m aps can be con - Th e p resen ce of d eep ven ou s d rain age is an in d irect in d ica-
st r u cted w ith carefu l cor rect ion of m ot ion ar t ifact . Alt h ough tor of th e fact th at th e AVM involves th e ven t ricular w all or is
p rom ising, rou t in e u se of fMRI as th e sole m et h od of n eu ral located or exten ds to th e deeper region s of th e brain . Th ese fea-
fun ct ion al localizat ion h as n ot been defin it ively establish ed. t ures ren der surgical resect ion m ore tech n ically ch allenging as
Magn etoen cep h alography is a tech n iqu e for m app ing brain th ey are difficu lt to access an d are invariably su p p lied by deep
act ivit y by record in g t h e m agn et ic field s p rod u ced by ch anges pen et rat ing ar teries even if th ey are n ot visu alized angiograph i-
in t h e elect r ical cu r ren t of act ivated cor t ical n eu ron s. Th e est i- cally. Fu r th erm ore, involvem en t of th e ven t ricular w all is asso-
m ated sou rce locat ion s obt ain ed from MEG can be com bin ed ciated w it h t h e p resen ce of ar ter ialized su bep en dym al vein s,
w ith MRI to create a m agn et ic source im age. Th is m eth od offers w h ich are fragile, resist coagulat ion , an d ten d to ret ract in to th e
th e p oten t ial for ext rem ely fin e tem poral resolu t ion as com p ared ven t ricles. How ever, deep ven ou s drain age m ay act ually be an
w ith fMRI th at depen ds on ch anges in CBF. Lim it at ion s in clude advantage intraoperatively as the draining veins are hidden aw ay
th e relat ively sm all field of view an d t h e n ecessit y for a sh ielded from the surgeon until the last m om ents of the AVM resect ion .
room given th e low sign al-to-n oise rat io. Th e h igh er th e AVM grade, th e greater th e difficu lt y an d risk
associated w it h su rgical resect ion . Low -grad e AVMs (grad e I
an d II) h ave low m orbid it y rates (0–5%) associated w it h t h eir
resect ion an d are th u s t ypically t reated surgically.57,58 High -
■ Arteriovenous Malformation Grading grade AVMs (grade IV an d V) h ave h igh m orbidit y rates (12–38%)
associated w it h t h eir resect ion an d are frequ en t ly m an aged
Several classificat ion system s h ave been p rop osed to grad e ce-
con ser vat ively. In con t rast , grade III AVMs represen t a h eteroge-
rebral AVMs.55–57 Th ey en com p ass th e variou s an atom ic an d
n eous group of lesion s w ith variable surgical risk. In a surgical
physiological feat ures of an AVM th at in flu en ce t reat m en t . Th ey
ser ies of 74 p at ien t s w it h grad e III AVMs, Law ton 58 fou n d by
est im ate th e risk associated w ith variou s th erapeu t ic tech n iqu es.
size (S), ven ous drain age (V), an d eloquen ce (E), th at sm all AVMs
Th e Spet zler-Mar t in grading system h as becom e on e of th e m ost
(S1V1E1), m edium /deep AVMs (S2V1E0), an d m edium / eloquen t
usefu l an d w idely accepted classificat ion system s for both com -
AVMs (S2V0E1) carried a surgical risk (n ew deficit or death ) of
m un icat ion of in form at ion regarding cerebral AVMs an d predic-
2.9%, 7.1%, an d 14.8% resp ect ively. In terest ingly, th ere w ere n o
t ion of th e tech n ical difficu lt y an d risks associated w ith su rgical
large grade III AVMs (S3V0E0) in th is series, eith er du e to selec-
resect ion .56 In th is system , AVMs receive a grade from I th rough
t ion bias or th e rarit y of th e lesion . Th ese resu lts led Law ton to
V, w h ich correspon ds to a poin t scale depen ding on th e size of
suggest su bdividing Sp et zler-Mar t in grade III AVMs by su rgical
th e AVM, its p roxim it y to eloqu en t n eu ral t issu e, an d w h eth er
risk as follow s: grade III– AVMs (S1V1E1), w ith risk sim ilar to
th e AVM drain s in to th e deep ven ou s system .
th at of low -grade AVMs, can be safely t reated w ith m icrosu rgical
resect ion ; grade III+ AVMs (S2V0E1), w ith risk sim ilar to th at of
Arteriovenous Malformation Size h igh -grade AVMs, sh ould be m an aged con ser vat ively; an d grade
III AVMs (S2V1E0), w ith in term ediate risk, require pruden t se-
Size is scored by m easu ring th e greatest diam eter of th e AVM lect ion for su rger y. A sim ilar m odificat ion w as proposed by de
n idus on DSA, CT, or MRI. Th e AVM n idu s is subsequen tly rated Oliveira an d colleagues.59 Grade III AVMs w ere subdivided in to
as sm all (less th at 3 cm ), m edium (3 to 6 cm ), or large (m ore th an IIIA if th ey w ere large an d IIIB if th ey w ere sm all but h ad deep
6 cm ). Th e size of th e AVM ser ves as a surrogate for th e n um ber ven ou s d rain age or w ere located in eloqu en t areas. d e Oliveira
of feeding ar teries, th e am oun t of flow th rough th e AVM, an d th e an d colleagu es gen erally recom m en ded em bolizat ion follow ed
degree of h em odyn am ic effect on th e adjacen t brain . by su rgical resect ion for grad e IIIA AVMs an d rad iosu rger y for
grades IIIB.
Alth ough m any experien ced su rgeon s h ave con firm ed th e va-
Eloquence of Adjacent Brain lid it y of th e Sp et zler-Mar tin grading system in predict ing su rgi-
Eloquen t n eu ral t issue is defin ed as region s of th e brain th at h ar- cal m orbidit y an d m or talit y, th e classificat ion fails to directly
bor easily iden t ifiable n eurologic fun ct ion an d can result in a address several im por t an t factors, su ch as th e pat tern of ar terial
disabling n eu rologic d eficit if inju red . Th ese region s in clu de th e su p ply (su p er ficial versu s deep p erforat ing), th e con figu rat ion of
sen sor y, m otor, language, an d visu al cor tex; th e hypoth alam u s th e n id u s (com p act versu s diffu se), an d th e presen ce of feeding
an d th alam us; th e in tern al capsu le; th e brain stem ; th e cerebel- ar ter y an eur ysm s. Fur th erm ore, it is im por t an t for surgeon s to
lar p edu n cles; an d th e deep cerebellar n u clei. How ever, region s recogn ize th at th e grading system does n ot t ake in to con sider-
of th e brain w ith fun ct ion th at can be easily com pen sated for at ion th eir ow n person al experien ce. How ever, th e classificat ion
that result in subtle non disabling neurologic deficits, such as the is ext rem ely h elpful in com m u n icat ing in form at ion regarding a
fron top olar or cerebellar cor tex, are con sidered n on eloqu en t . cerebral AVM, an alysis of an in dividu al surgeon’s series of cases,
an d com parison w ith th e results of oth er surgical series or t reat-
m en t m odalit ies. Fu r t h erm ore, i

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