TECHNIQUE APPLICATIONS

IN SITU BYPASS IN THE MANAGEMENT OF COMPLEX

INTRACRANIAL ANEURYSMS: TECHNIQUE APPLICATION
IN 13 PATIENTS
Alfredo QuionesHinojosa, M.D.
Department of Neurological
Surgery, Center for Stroke and
Cerebrovascular Disease,
University of California,
San Francisco,
San Francisco, California

Michael T. Lawton, M.D.

Department of Neurological
Surgery, Center for Stroke and
Cerebrovascular Disease,
University of California,
San Francisco,
San Francisco, California
Reprint requests:
Michael T. Lawton, M.D.,
Department of Neurological
Surgery, University of California,
San Francisco,
505 Parnassus Avenue,
Moffitt Hospital,
Room M779, Box 0112,
San Francisco, CA 94143-0112.
Email:
lawtonm@neurosurg.ucsf.edu
Received, December 6, 2004.
Accepted, February 7, 2005.

OBJECTIVE: Cerebral revascularization is an important part of the treatment of complex intracranial aneurysms that require deliberate occlusion of a parent artery. In situ
bypass brings together intracranial donor and recipient arteries that lie parallel and in
close proximity to one another rather than using an extracranial donor artery. An
experience with in situ bypasses was retrospectively reviewed.
METHODS: Thirteen aneurysms were treated with in situ bypasses between 1997 and
2004. During this time, 1071 aneurysms were treated microsurgically and 46 bypasses
were performed as part of the aneurysm treatment.
RESULTS: Treated aneurysms were located at the middle cerebral artery (MCA) in five
patients, posteroinferior cerebellar artery (PICA) in three patients, vertebral artery in
three patients, and anterior communicating artery in two patients. Seven aneurysms
were fusiform or dolichoectatic, and six aneurysms were saccular. Microsurgical
revascularization techniques included side-to-side anastomosis of intracranial arteries
in eight patients and aneurysm excision with end-to-end reanastomosis of the parent
artery in five patients. In situ bypasses included A3A3 anterior cerebral artery bypass
in two patients, anterior temporal artery-MCA bypass in one patient, MCAMCA
bypass in one patient, and PICAPICA bypass in four patients. Aneurysm excision with
arterial reanastomosis included three MCA aneurysms and two PICA aneurysms. On
angiography, all aneurysms were completely obliterated and 12 bypasses were patent.
CONCLUSION: In situ bypass is a safe and effective alternative to extracranialintracranial bypasses and high-flow bypasses using saphenous vein or radial artery
grafts. Although in situ bypasses are more demanding technically, they do not require
harvesting a donor artery, can be accomplished with one anastomosis, and are less
vulnerable to injury or occlusion.
KEY WORDS: Intracranial aneurysm, Microsurgery, Revascularization, Subarachnoid hemorrhage
Neurosurgery 57[ONS Suppl 1]:ONS-140ONS-145, 2005

ost intracranial aneurysms can be managed with microsurgical clipping or endovascular coiling, but a subset of
aneurysms with complex anatomy or fusiform/
dolichoectatic morphology may require an alternative approach
using revascularization. Despite disappointing results from national
trials examining the therapeutic efficacy of extracranial-tointracranial (ECIC) bypass surgery for ischemic stroke, this technique remains a critical part of the neurosurgeons armamentarium
for treating complex and giant intracranial aneurysms, particularly
when the treatment involves the deliberate sacrifice or occlusion of
a parent artery that supplies the aneurysm (4, 8, 10). ECIC bypass
surgery typically involves the anastomosis of the superficial temporal artery (STA) or occipital artery (OA) (9) to an intracranial recip-

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DOI: 10.1227/01.NEU.0000163599.78896.F4

ient artery but may also use saphenous vein or radial artery grafts
connected to donor arteries more proximally (i.e., to the internal,
external, or common carotid artery), which delivers increased blood
flow. These two types of bypasses constitute the majority of procedures used in the management of complex intracranial aneurysms,
but an important and elegant third type is the in situ or intracranialto-intracranial (ICIC) bypass.
In situ bypass requires that donor and recipient arteries lie parallel and in close proximity to one another. Anatomically, there are
at least four sites where this requirement is met: the anterior cerebral
arteries (ACAs) as they course over the genu and rostrum of the
corpus callosum (A2 and A3 segments); the middle cerebral artery
(MCA) branches, including the anterior temporal artery, as they

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course through the sylvian fissure; the posterior cerebral artery

(PCA) and superior cerebellar artery (SCA) as they course around
the midbrain through the ambient cistern; and the posteroinferior
cerebellar arteries (PICAs) as they course around the posterior medulla and tonsils in the cisterna magna. These in situ bypasses are
appealing because they are entirely intracranial, are less vulnerable
to injury or occlusion, do not require harvesting an extracranial
artery or graft, use donor and recipient arteries with diameters that
are well matched, and require just one anastomosis (1, 3, 5, 7). We
reviewed our experience with in situ bypasses to evaluate their
utility and to share our technical lessons learned.

PATIENTS AND METHODS

Patients with aneurysms treated at the University of California, San Francisco, by the senior author (MTL) were identified from the cerebrovascular diseases database. Between
August 1997 and August 2004, 1071 aneurysms were treated
microsurgically in 864 patients. Among the cohort, 46 patients
underwent bypass surgery as part of the management of their
aneurysm. High-flow bypasses with saphenous vein or radial
artery grafts were performed in 21 patients, and low-flow
ECIC bypasses with STA or OA grafts were performed in 12
patients. In situ bypasses were performed in the remaining 13
patients. Included in these in situ bypasses were aneurysms

FOR

ANEURYSMS

that were excised with primary end-to-end reanastomosis of

the parent artery. Medical records, neurological examinations,
angiograms, operative reports, and postoperative courses for
these patients were retrospectively reviewed.
There were six women and seven men, with a mean age of
42.5 years (range, 1677 yr). Aneurysm rupture was the most
common presentation (eight patients). The other five patients
presented with headache or other neurological complaints,
and unruptured aneurysms were detected during diagnostic
evaluation (Table 1).
During surgery, brain relaxation was achieved with mannitol and cerebrospinal fluid drainage through a ventriculostomy or through a window created in the lamina terminalis.
Mild hypothermia and barbiturates titrated to achieve electroencephalographic burst suppression were used to increase
tolerance to cerebral ischemia during the time when the anastomosis was performed and the parent arteries were temporarily occluded. Blood pressure was increased with pressor
agents during this time if changes in somatosensory evoked
potentials or the electroencephalogram were observed.

RESULTS
Aneurysms treated with in situ bypass were located at the
MCA in five patients, PICA in three patients, vertebral artery

TABLE 1. Summary of in situ bypass casesa

Patient
no.

Sex/age
(yr)

SAH

F/78

F/48

Aneurysm
location

Morphology

Bypass location

Arterial occlusion

Radiographic outcome

L ACA

Saccular

A3A3

Endovascular

Patent bypass, obliteration of aneurysm

A ComA

Saccular

A3A3

Endovascular

Patent bypass, obliteration of aneurysm

F/16

L MCA

Saccular

ATAMCA

Surgical

Patent bypass, obliteration of aneurysm

M/19

R MCA

F/D

MCA E/R

Surgical

Patent bypass, obliteration of aneurysm

F/40

L MCA

Saccularb

MCA E/R

Surgical

Patent bypass, obliteration of aneurysm

F/23

L MCA

Saccularb

MCAMCA

Surgical

Patent bypass, obliteration of aneurysm

M/36

R MCA

F/D

MCASTAMCA

Surgical

Obstructed bypass, obliteration of aneurysm

M/44

R PICA

F/D

PICA E/R

Surgical

Patent bypass, obliteration of aneurysm

M/52

L PICA

F/D

PICA E/R

Surgical

Patent bypass, obliteration of aneurysm

10

F/51

R VA

F/D

PICAPICA

Endovascular

Patent bypass, obliteration of aneurysm

11

M/77

R PICA

Saccular

PICAPICA

Endovascular

Patent bypass, obliteration of aneurysm

12

F/47

L VA

F/D

PICAPICA

None

Patent bypass, obliteration of aneurysm

13

M/30

R VA

F/D

PICAPICA

Endovascular

Patent bypass, obliteration of aneurysm

a
SAH, subarachnoid hemorrhage; N, no; L, left; ACA, anterior cerebral artery; Y, yes; A ComA, anterior communicating artery; MCA, middle cerebral artery; ATA,
anterior temporal artery; F/D, fusiform/dolichoectatic; E/R, excision-reanastomosis; STA, superficial temporal artery; PICA, posteroinferior cerebellar artery; VA,
vertebral artery.
b
Mycotic.

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12 bypasses were patent. The occluded bypass was the MCA

STAMCA reconstruction performed after aneurysm excision
because of inability to reapproximate the arterial ends without
the interposition graft. No adverse ischemic complications
were observed clinically or radiographically in this patient or
in any of the other patients.

in three patients, and anterior communicating artery in two

patients (Table 1). Seven aneurysms were fusiform or dolichoectatic, and six aneurysms were saccular. Two aneurysms
were mycotic or infectious.
Microsurgical revascularization techniques included side-toside anastomosis of intracranial arteries in eight patients and
aneurysm excision with end-to-end reanastomosis of the parent
artery in five patients. ICIC bypasses included A3A3 ACA
bypass in two patients (Fig. 1), anterior temporal artery-MCA
bypass in one patient, MCAMCA bypass in one patient, and
PICAPICA bypass in four patients (Fig. 2). Aneurysm excision
with arterial reanastomosis included three MCA aneurysms and
two PICA aneurysms (Fig. 3). Reanastomosis of one of the MCAs
required an interposition graft from the STA. No additional or
unexpected difficulties were encountered in the eight patients
who presented with ruptured aneurysms compared with the five
patients who presented with unruptured aneurysms.
Seven aneurysms were surgically trapped after performing
the bypass during a single surgical stage. Five aneurysms
were occluded endovascularly in a second stage. By means of
angiography, all aneurysms were completely obliterated and

The requirement for in situ bypass that donor and recipient

arteries lie parallel and in close proximity makes at least four
bypasses possible to perform. On the basis of this clinical
experience, only three were applicable to aneurysms located at
the anterior communicating artery, MCA, and PICA. On the
basis of the anatomy of these arteries, the PCASCA bypass is
possible, but we did not need this bypass in this experience.
The PCASCA bypass might have utility in the management
of a basilar apex aneurysm when clipping cannot preserve
flow in the ipsilateral P1 PCA, the posterior communicating
artery is diminutive or occluded, and the STA is also diminutive or unavailable. In this case, a PCASCA bypass per-

FIGURE 1. Scans and intraoperative photographs showing an A3A3

bypass in Patient 1. This 78-year-old woman presented with aphasia and
headaches. A, head computed tomographic scan demonstrating a giant and
partially thrombosed anterior communicating artery aneurysm and
obstructive hydrocephalus attributable to compression of the foramen of
Monro by the aneurysm. B, left internal carotid artery angiogram (anteroposterior view) revealing a superiorly projecting aneurysm without a clippable neck. The left A1 and A2 ACA segments were separated by the base
of the aneurysm, indicating fusiform/dolichoectatic morphology. A multimodality strategy was planned, with a bypass to the distal ACA as the
first stage and endovascular coil occlusion of the aneurysm and left A1
ACA as the second stage. She underwent a bifrontal craniotomy via an

interhemispheric approach and A3A3 ACA side-to-side anastomosis to

revascularize the ACA territory distal to the aneurysm. The back walls of
the anastomosis were sutured from within the arterial lumen first (C);
then, the front walls were sutured (D). E, depth of this surgical corridor
is shown. F, postoperative left carotid artery angiography demonstrating a
patent bypass with good distal flow in bilateral ACA territories. G and
H, patient then underwent coil occlusion of the aneurysm and the proximal left A1 ACA, with right carotid artery angiography demonstrating
obliteration of the aneurysm and blood flow in bilateral ACA territories
originating from the right A2 ACA and crossing to the left hemisphere
through the bypass. The anastomosis site is indicated by the large black
arrow in H.

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DISCUSSION

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FOR

ANEURYSMS

FIGURE 2. Scans and intraoperative photographs showing a PICA

PICA bypass in Patient 13. A 30-year-old man presented with subarachnoid hemorrhage (A) and a right vertebral artery dissecting aneurysm
(B). The patient was taken to the operating room for a suboccipital craniotomy, where the PICAs were brought together between the tonsils (C)
with a side-to-side anastomosis to allow the contralateral PICA to supply
the ipsilateral PICA in a retrograde fashion (D). E, arteries maintained

good flow after the release of the temporary clips. F, aneurysm could be
appreciated through the craniotomy. G, on postoperative Day 2, the
patient underwent a postoperative angiogram revealing the bypass to be
fully patent (site of the anastomosis illustrated by arrow). H, endovascular occlusion of the vertebral artery with coils was performed, and the
final angiogram revealed a fully patent bypass and obliteration of the
aneurysm.

formed before clipping the aneurysm might enable the patient

to tolerate an occlusion of the P1 PCA after aneurysm clipping.
In addition to these ICIC bypasses, aneurysm excision with
arterial reanastomosis is another variant of in situ bypass that
can be performed with aneurysms at any location, provided
that there is enough redundancy in the arterial ends to reapproximate them without tension. Excision-reanastomosis is
particularly applicable to infectious and fusiform aneurysms
that are small in size and often distally located (2).
In situ bypasses are appealing because they eliminate the need
to harvest a donor artery extracranially, saving the neurosurgeon
time and effort and also sparing the patient a second or third
incision when saphenous vein or radial artery grafts are used.
Bypasses that use the STA or OA as a donor artery do not spare
the patient an additional incision, but these arteries can sometimes be so diminutive in caliber that the adequacy of the bypass
can be uncertain. In other cases, particularly after prior surgery
or trauma, these arteries may be occluded and unavailable. In
situ bypass has conceptual advantages as well, with no length to
the bypass and therefore a reduced risk of delayed occlusion. Its
intracranial location protects it from exogenous occlusion or injury. With ACA bypass, the STA is not long enough to reach the
A3 segment, necessitating more complex ECIC bypasses like the
bonnet bypass, with a long saphenous vein graft from the

cervical carotid artery or STA (11). In these cases, the A3A3

ACA bypass is more elegant and less invasive.
All in situ bypasses in this experience were part of a
planned surgical strategy that reflected the availability and
size of extracranial donor arteries, aneurysm location, and
neurosurgeon preferences. A small or previously occluded
STA necessitates an alternative approach for MCA aneurysms
and increases the appeal of in situ bypasses. The deep midline
location of ACA aneurysms renders the STA insufficient. The
OA is more cumbersome to dissect and seems to be more
prone to postoperative occlusion than the STA. Consequently,
with PICA aneurysms, surgeon preference for using the adjacent PICA over the OA accounted for the PICAPICA bypass
being the most common one in this patient series.
In situ bypass requires temporary occlusion of two major
intracranial arteries to perform the side-to-side anastomosis instead of just temporarily occluding one recipient artery with a
traditional ECIC bypass. Furthermore, any complication with
the anastomosis that compromises the flow or patency of the
donor and recipient arteries is potentially more dangerous because of the extra artery involved. However, this concern did not
materialize in this clinical experience. There were no occlusions
in the side-to-side anastomoses. We attributed this to a long
arteriotomy, with a length that is typically three times the diam-

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FIGURE 3. Scans and intraoperative photographs showing a PICA aneurysm excision and arterial reanastomosis in Patient 8, a 44-year-old
man. A, patient presented with a giant thrombotic right PICA aneurysm
(with symptoms related to mass effect
on his medulla) and a left PICA aneurysm. The patient underwent a
right far lateral craniotomy; for
trapping/debulking of the giant
thrombotic right PICA aneurysm, reanastomosis of the right PICA (B and C), and clip reconstruction of the left PICA aneurysm (D and E) (arrow in C illustrates the temporary clip application). F and
G, postoperative angiogram demonstrating excellent obliteration of the aneurysm, and a patent bypass as shown by arrows.

eter of the arteries. The one occlusion that did occur (Patient 7)
was attributed to an interposition graft in an end-to-end reanastomosis, emphasizing the diminished patency rate associated
with two serial anastomoses and the need to mobilize the arterial
ends aggressively to avoid the need for an interposition graft.
If this one atypical case is excluded, the overall patency rate
with in situ bypasses compares favorably with that of conventional ECIC bypasses using STA donor artery or saphenous
vein grafts. In the senior authors revascularization experience
with 101 bypass procedures for aneurysms, ischemic diseases,
and cranial base tumors, the patency rate for STA bypasses
was 98.4% (61 of 62 bypasses) and that for saphenous vein
bypasses was 92.3% (24 of 26 bypasses).
Mobilization of donor and recipient arteries is equally important with the side-to-side anastomosis. These arteries should be
touching, or nearly touching, before sutures are placed. If sutures
are required to pull the arteries together, there is a risk of the
sutures breaking or tearing through the arterial wall as they are
tightened and a risk of kinking the afferent and/or efferent
arteries, which can compromise their blood flow. Arteries that
approximate without tension on the sutures remain in a parallel
course that optimizes the flow through the bypass.
The side-to-side anastomosis is not as familiar to neurosurgeons as the end-to-end anastomosis. It requires suturing the
back wall of the anastomosis from inside the lumen (Fig. 1). The
first bite after approximating the two arteries passes the needle
from outside the lumen to inside the lumen. The next sutures are
then placed in a continuous fashion to the opposite end of the
arteriotomies, where the needle is again passed from inside the
lumen to outside the lumen. These two reversing passes must be

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remembered. Once these sutures are loosely placed along the

entire line, they are tightened and tied to a second suture at the
other end of the arteriotomy. The front wall of the anastomosis is
performed with a simple continuous suture from outside the
lumen. This anastomosis is often performed in a deep surgical
corridor, making it essential to position a continuous suction
drain at the depths of the field to keep it clear of blood.
Half of the patients in this series were managed with a
multidisciplinary approach combining microsurgical and endovascular techniques. The advantages of this strategy include minimizing the invasiveness of surgery, sometimes
eliminating a second craniotomy, and delaying the aneurysm
occlusion until the patients hemodynamics and general medical condition have been optimized (6).
In summary, the ability to revascularize an intracranial artery creates options in aneurysm management beyond direct
clipping or coiling, allowing deliberate arterial occlusion without the risk of ischemic stroke and neurological morbidity that
would have occurred without a bypass. These strategies
should be considered in the management of complex aneurysms, and these techniques should be part of the armamentarium of vascular neurosurgeons.

REFERENCES
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Current multimodality management of infectious intracranial aneurysms.
Neurosurgery 48:12031214, 2001.

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3. Evans JJ, Sekhar LN, Rak R, Stimac D: Bypass grafting and revascularization in the
management of posterior circulation aneurysms. Neurosurgery 55:10361049, 2004.
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aneurysm surgery: Current techniques, indications, and outcome. Neurosurgery 38:8394, 1996.
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7. Lemole GM Jr, Henn J, Javedan S, Deshmukh V, Spetzler RF: Cerebral
revascularization performed using posterior inferior cerebellar arteryposterior inferior cerebellar artery bypass: Report of four cases and literature
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9. Roski RA, Spetzler RF, Hopkins LN: Occipital artery to posterior inferior cerebellar
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Acknowledgment
Neither of the authors of this study has any financial interest in any of the
instruments or methodologies used in this study.

ANEURYSMS

unavailable or when the need for bypass arises unexpectedly during

surgery, this strategy for revascularization provides a useful and
elegant option.
Sepideh Amin-Hanjani
Robert F. Spetzler
Phoenix, Arizona

uiones-Hinojosa and Lawton describe their experience using in

situ bypasses for the management of complex intracranial aneurysms in 13 patients. This technique is essential and needs to be
mastered by any microvascular surgeon who is currently treating
complex intracranial aneurysms. There is no question that deconstructive procedures associated with bypass procedures are becoming
more essential in the treatment of giant and complex intracranial
aneurysms. Endosaccular occlusion certainly has a role; however,
many aneurysms that cannot be treated by using endosaccular techniques also are unable to be treated by using standard microsurgical
techniques and, therefore, require much more refined and sophisticated procedures. As the authors have alluded, the in situ bypass is an
extremely attractive option, particularly for middle cerebral artery,
anterior cerebral artery and PICA-to-PICA bypasses. The authors are
to be congratulated on an impressive series. There is no question that
this particular information should be kept in the file of every active
operating microvascular surgeon.

COMMENTS

Robert H. Rosenwasser
Philadelphia, Pennsylvania

n this article, Quiones-Hinojosa and Lawton present a series of

patients to illustrate the value of local or in situ anastasmosis in the
management of intracranial aneurysms that cannot be coiled or
clipped without revascularization. Based on my experience with cerebral revascularization in 73 patients with aneurysms and 10 in situ
bypasses, I concur with the authors recommendations. In some patients, the flow provided by this type of anastamosis may be inadequate for the need; for instance, in basilar artery occlusion. In some
patients, an extracranial to intracranial bypass may allow the aneurysm treatment to be provided in the same stage as the bypass
operation. For instance, in the authors case 11, a posteroinferior
cerebellar artery (PICA) aneurysm, a PICA-PICA anastamosis was
performed, followed by endovascular obliteration in a second stage.
An occipital to PICA anastamosis, followed by aneurysm clipping,
could have been performed in a single operation, avoiding the need
for a second procedure. This series and others demonstrate the need
for either close collaboration or a single surgeon when performing
endovascular and microsurgical aneurysm bypass procedures.
Laligam N. Sekhar
Seattle, Washington

FOR

n this article, the authors nicely illustrate the strategy of intracranialintracranial bypass for distal revascularization in the treatment of
complex intracranial aneurysms. Based on cardiac bypass experience,
the long-term patency rates of in situ vessels may well be higher.
However, with both donor and recipient territories at risk in the event
of even rare bypass occlusion or extended cross-clamping, we would
not consider intracranial-intracranial bypass as the first line of treatment. When suitable extracranial vessels or interposition grafts are

he number of intracranial aneurysms treated by using endovascular coil embolization has been growing very quickly in the past
few years. Nowadays, in some neurosurgical centers, most small and
simple aneurysms are being treated by using the endovascular approach. The fast and great development of new technologies of endovascular materials will probably permit the use of the endovascular
route to treat most intracranial aneurysms in the coming years. Thus,
in the near future, it is likely that open surgery will deal only with
giant and complex aneurysms that cannot be treated by using the
endovascular route and with cases for which endovascular treatment
results in complications. Young neurosurgeons who want to work
with vascular neurosurgery must learn interventionist neuroradiology and the techniques of cerebral revascularization.
The authors have done a very good job with the technique of in situ
bypass for aneurysm surgery. I fully agree with them: the in situ
bypass is an excellent alternative to revascularize the brain when
dealing with complex aneurysms. Another important remark is the
multidisciplinary management of half of the cases. As stressed by the
authors, this strategy minimizes the invasiveness of the surgery and
delays the aneurysm occlusion until the patients hemodynamics and
general conditions have optimized. They present an important series
of cases with very good results. The only postoperative thrombosis
was in the end-to-end reanastomosis of the middle cerebral artery
with interposition of a graft. In my personal experience of in situ
bypass, I had a similar case in which I interposed a saphenous vein
graft that occluded in the postoperative period.
Atos Alves de Sousa
Belo Horizonte, Brazil