You are on page 1of 8

J Neurosurg 137:1554–1561, 2022

Neurosurgical Forum
BROCA’S AREA

Complex cranial surgery and the Inpatient Sample (NIS) published in 2020 confirmed that
during the first 10 years following ISAT and ISUIA, in-
future of open cerebrovascular terventional procedures accounted for 56.3% of ruptured
training
aneurysm treatments overall and 65% of unruptured aneu-
rysms, with > 70% of all aneurysms undergoing primary
endovascular treatment in 2014, the last year of the study
sampling frame.2 Other recent analyses have demonstrated
Christopher S. Graffeo, MD, MS,1 Michael J. Link, MD,2 and an expanding role for flow diversion, Woven EndoBridge
Michael T. Lawton, MD1 (Microvention/Terumo) embolization, and a variety of
Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s
1 other devices that have resulted in a dramatic reduction
Hospital and Medical Center, Phoenix, Arizona; and 2Department of in the proportion of cerebrovascular cases preferentially
Neurosurgery, Mayo Clinic, Rochester, Minnesota treated with open neurosurgical techniques.6
Although endovascular therapies have positively in-
The Evolving Landscape of Cerebrovascular Treatment fluenced key aspects of patient care and the outcomes of
In less than a generation, the clinical practice and as- certain cerebrovascular diseases, including subarachnoid
sociated training opportunities in cerebrovascular neuro- hemorrhage and ischemic stroke, the full range of second-
surgery have evolved dramatically. Numerous factors have ary impacts that this shift has had on training and, there-
contributed to this profound transformation, including fore, on the care of future patients, is underappreciated.
trends in medical education, litigation, healthcare perfor- Correspondingly, we sought to describe the effect that
mance tracking, and shifting perspectives on the physi- changes in the culture and practice of cerebrovascular
cian-patient relationship. Notwithstanding these trends, neurosurgery have had on training pathways. As an al-
the single most important contributor to changes in cere- ternative to the dual vascular pathways, we describe the
brovascular training has been the widespread implementa- complex cranial model, which emphasizes microsurgical
tion of endovascular treatment. mastery in the treatment of both cerebrovascular and skull
Neurosurgical treatment of cerebrovascular diseas- base disorders while maintaining a focus on complemen-
es has been an area of rapid innovation for more than 3 tary operative techniques instead of a disease-specific
decades. During this time, microsurgery has been chal- educational approach.
lenged in all quarters. Most aneurysms that would have
previously undergone surgical clipping are now managed Clinical, Cultural, and Legislative Influences on
via endovascular intervention.1,2 Furthermore, although Neurosurgical Training
data have been equivocal regarding several key scenarios, In tandem with these clinical changes, the typical train-
an increase in the versatility and safety of the endovascu- ing experience for neurosurgery residents in the United
lar armamentarium has been noted, with initial trepida- States has also undergone a marked reduction in exposure
tion following the original description of detachable coils to open cerebrovascular operations. A study published by
by Guglielmi in 1991, ultimately giving way to more wide- Piazza et al. in 2017 using NIS data indicated that from
spread acceptance, particularly in the wake of the Interna- 2002 to 2011, in the United States, teaching opportuni-
tional Subarachnoid Aneurysm Trial (ISAT) in 1998 and ties for both ruptured and unruptured aneurysm clippings
the International Study of Unruptured Intracranial Aneu- decreased significantly.7 Their analysis demonstrated that
rysms (ISUIA) in 2003.3–5 the probability of a patient undergoing open treatment
A retrospective review of the National (Nationwide) decreased by 15.6% for those with ruptured aneurysms

ABBREVIATIONS ACGME = Accreditation Council for Graduate Medical Education; EEA = endoscopic endonasal approach; ISAT = International Subarachnoid Aneurysm
Trial; ISUIA = International Study of Unruptured Intracranial Aneurysms; NIS = National (Nationwide) Inpatient Sample; SRS = stereotactic radiosurgery.

1554 J Neurosurg Volume 137 • November 2022

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

and 9.8% for those with unruptured aneurysms during ation leaders in cranial neurosurgery practiced broadly,
each year of the study period. In contrast, endovascular often working in cerebrovascular, skull base, and neuro-
interventions increased by 18.7% and 10.8% per year, re- oncology.15 The list of neurosurgeon innovators practic-
spectively, over the same interval. Similar findings were ing in multiple subspecialties is extensive and includes
confirmed by Yaeger et al. in a study of resident case log Evandro de Oliveira, Vinko Dolenc, Raymond Donaghy,
data published by the Accreditation Council for Graduate Charles Drake, Takanori Fukushima, Roberto Heros,
Medical Education (ACGME) during the sampling frame Peter Janetta, Laligam Sekhar, Robert Spetzler, Bennett
of 2009 to 2019.8 Over that time, the fractional proportion Stein, Thoralf Sundt, John Tew Jr., and Charles Wilson,
of endovascular aneurysm treatments involving trainees among many others.
increased from 11.7% to 39.6%, while craniotomies for Evolution in medicine is often marked by an inverse dy-
aneurysm decreased from 88.3% to 60.4%. As of 2019, the namic, with individual practices narrowing and deepening
mean number of open aneurysm treatments completed by while the terrain of their parent specialty broadens. Within
graduating residents during their 7-year training was 32.5 neurosurgery, this pattern was observed as microsurgical
cases. These trends are anticipated to accelerate, a reality expertise proliferated and individual neurosurgeons fo-
that is now reflected by formal accreditation requirements, cused on narrower ranges of disease.16 Although this trend
which no longer include a case minimum requirement for benefited surgeons and patients alike, it also resulted in
open aneurysm treatments as of 2018.9 the prioritization of fellowship and practice structures that
Several other broad influences have affected the open were disease focused, the contemporary consequences of
vascular experience for neurosurgical trainees. Since 2003, which were not anticipated in the pre-endovascular ther-
all residents in ACGME-accredited programs have been apy era.
restricted to 80 hours of weekly clinical duties. Although Many neurosurgeons are drawn to innovation and have
studies interrogating the effect of these changes on neuro- a savvy understanding of novel tools or techniques that
surgery have been controversial, several observational and may influence practice. Similarly, many neurosurgeons
survey-based assessments have indicated that duty-hour are driven by the desire to provide safer and more effec-
restrictions could have reduced trainee case volume and tive treatments, ultimately motivating the development of
operative autonomy.10 Simultaneously, trends in malprac- novel therapies, such as endovascular devices or stereo-
tice litigation both within neurosurgery and throughout tactic radiosurgery (SRS). Correspondingly, as endovas-
medicine have demonstrated significant increases in case cular therapies have matured and their indications have
filings, settlements, and plaintiff decisions over the past 2 expanded over the past 2 decades, the dominant training
decades, further contributing to a decrease in trainee in- and practice model for cerebrovascular neurosurgeons
dependence during complex procedures.11 Although these has become the dual vascular approach oriented around
changes are not specific to cerebrovascular neurosurgery, fellowship-level training in both endovascular and open
when coupled with dwindling open case volumes, the net vascular surgery.17 Although several variations in the se-
effect has been markedly fewer open aneurysm, arterio- quencing of these fellowships are considered acceptable
venous malformation, or bypass operations per trainee, as entrées into the field, their end goal is shared: the genera-
well as less autonomy per case.9 tion of individual neurosurgeons who are disease-oriented
These forces have substantially increased the barriers specialists with competency in both disciplines.18
to developing advanced microsurgical skills during neu- The principal benefit of dual training is a theoretical
rosurgical residency, particularly for open cerebrovascular reduction in incentive-based bias toward either open or
operations. Encouragingly, the ongoing development of endovascular treatment, given that the same neurosurgeon
diverse and comprehensive simulation technologies could would be completing the procedure, regardless of the
eventually offset some of these educational disadvantag- recommended modality. In practice, whether combined
es, including those based on virtual or augmented real- training actually eliminates bias remains controversial.19,20
ity, animal or cadaveric tissue models, or 3D printing.12–14 More importantly, the assumption that consolidating de-
Current evidence suggests that these tools may shorten the cision-making in a single individual is desirable has not
learning curve for acquisition of basic skills among neu- been explicitly interrogated. Rather, mounting evidence
rosurgical trainees. However, they are not anticipated to suggests that a team of individuals with diverse skill sets
replace operative experience for advanced skill develop- and training would be better equipped to make difficult
ment. Consequently, fellowship-level training is expected decisions and execute complex treatment plans, as shown
to remain mandatory for all cerebrovascular neurosur- with multidisciplinary tumor boards.21,22
geons, although the common pathways into the field have The psychology literature supports these findings and
evolved in an unexpected fashion and are approaching an reports that teams consistently outperform isolated individ-
inflection point. uals in decision-making and are less vulnerable to bias, es-
pecially when team membership is intellectually diverse.23
Two Roads Diverged The putative benefits of investing in a single neurosurgeon
Apprenticeship has been a core aspect of neurosurgical with multiple skills may be negligible compared to the po-
training since its inception. Although the legacy of mod- tential advantages of a multidisciplinary team comprising
ern microsurgery can be traced through several lineages, members with complementary perspectives.
most of the leading modern neurosurgeons originate with
Gazi Yaşargil and his contemporaries or protégés. Follow- The Task at Hand
ing in Yaşargil’s tradition, many first- and second-gener- Although there is little evidence to support the emphasis

J Neurosurg Volume 137 • November 2022 1555

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

on consolidated decision-making in neurosurgery, numer- trolling final electrode advancement or collimator align-
ous studies have reinforced the concept that skill acqui- ment. Toward the center of the spectrum, neuro-oncology
sition benefits from frequent, deliberate repetition, espe- and epilepsy procedures frequently involve macroscopic
cially for precise execution of complex manual tasks.24,25 resections of large tumors or lobar domains, and the ex-
Within surgical pedagogy, a randomized study involving tent to which the microscope is used varies widely. Endo-
students demonstrated that baseline differences in ability vascular and endoscopic skull base procedures are unam-
or experience were readily overcome by focused practice biguously microscopic domains. However, by definition,
with robotic surgery during the study period.26 Another neither incorporates the operating microscope, and the
randomized study of general surgery residents observed physical skill sets of catheter- or endoscope-based opera-
significant differences in trainees who underwent distrib- tions are demanding but distinct from microneurosurgery.
uted skills acquisition programs rather than single mass Finally, at the extreme of working scale and micro-
sessions.27 Still, other studies from the general, orthope- scope integration, we encounter the overlapping domains
dic, and plastic surgery literature have reported similar of open cerebrovascular and skull base surgery. A cursory
findings among trainees who undergo serial skills training review of the diseases commonly treated within each sub-
exercises.28,29 Anecdotally, these results concur with ours specialty might suggest that the shared features between
regarding procedural competence and confidence across these disciplines are superficial. However, a more granular
a broad base of activities, ranging from medical students assessment demonstrates not only that the technical nu-
learning bedside procedures to cerebrovascular surgeons ances of aneurysm and arteriovenous malformation sur-
mastering the art of basilar apex aneurysm clipping.30,31 gery overlap substantially with skull base tumor resection
Applying these concepts to neurosurgical training, one and microvascular decompression but also that training
can plot the range of manual tasks common to each sub- and practice within each field have the potential to mark-
specialty alongside various axes. Two useful concepts are edly improve a surgeon’s abilities to perform complex cra-
the working scale of common procedures within a partic- nial operations across both domains.
ular domain and the extent to which those procedures are
dependent on skill with the operating microscope (Fig. 1). The Prodigal Trainee
Spine and trauma occupy the largest working scales. The potential benefits of a practice that incorporates
They infrequently require the operating microscope, with both cerebrovascular and skull base training are self-evi-
notable exceptions including microdiscectomy, cervical dent. Performing a higher volume of complicated or chal-
foraminotomy, and certain minimally invasive or onco- lenging cases using the operating microscope is more like-
logical spine procedures. Although the precision target- ly to advance the surgeon’s dexterity and manual skills.
ing of functional and stereotactic neurosurgery is at the This training is essential in the case of an intraoperative
microscopic level, the procedures are executed without the complication or anatomical variant that demands dynamic
need for magnification and with automated systems con- thinking, steady hands, and broad familiarity with tech-
niques for managing the unexpected. Furthermore, the
treatment landscape is such that maintaining a busy prac-
tice of predominantly open cerebrovascular operations is
essentially impossible for a junior surgeon, emphasizing
the pragmatic advantages of a second referral base.
Given the shared origin of these subspecialties and
their noted historical overlap among first- and second-gen-
eration neurosurgeons, many of the common skull base
techniques have an established utility for cerebrovascular
operations, such as the anterior clinoidectomy for access-
ing ophthalmic aneurysms, the orbitozygomatic cranioto-
my for high anterior communicating artery or basilar apex
aneurysms, or the far-lateral approach to vertebrobasilar
lesions, among others. Additionally, minimally invasive or
“keyhole” craniotomies, developed predominantly within
the realm of skull base surgery, have proven their versa-
tility in minimizing the morbidity associated with open
approaches to cerebrovascular lesions, such as the lateral
supraorbital and minipterional craniotomies for clipping
of unruptured anterior circulation aneurysms.32 These fa-
miliar examples provide a useful template for understand-
ing the rich opportunities for crosstalk between the train-
ing pathways.
Taking the approach discussion to the next level of so-
phistication, one appreciates that the craniotomies com-
FIG. 1. The neurosurgery microscopy matrix showing relative working monly used by neurosurgeons with skull base training
scales and microscopic dependence of major neurosurgical subspe- have the potential to permit more individualized treatment
cialty practices. MIS = minimally invasive surgery. across a range of challenging cerebrovascular diseases.

1556 J Neurosurg Volume 137 • November 2022

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

Skull base surgery is often conceptualized as a modular tise, particularly for lesions that come to the pial surface in
system for bone removal that attempts to optimize the an area that is difficult to access via traditional corridors
operative corridor while minimizing brain retraction.33 (Fig. 2A). For example, a ventral pontine lesion that comes
Although neuroanatomically defined, the skull base trian- to the surface laterally would require significant retraction
gles also provide an important heuristic for understanding and an unfavorable working angle if the standard retrosig-
disease and tailoring approaches to each patient and le- moid craniotomy were used (Fig. 2B). In contrast, the ex-
sion. This skull base framework has proven so valuable to tended retrosigmoid approach opens access to the petrous
cerebrovascular neurosurgery that it has, in turn, inspired fissure and transmiddle cerebellar peduncle approach, and
the conceptualization and development of several addi- the posterior petrosectomy offers a presigmoid corridor
tional sets of triangles, including those for tackling ante- that has both a shorter working distance and more lateral
rior communicating and vertebrobasilar aneurysms.34,35 angulation with respect to the ventral brainstem (Fig. 2C
Brainstem cavernomas are another key example of how and D).
cerebrovascular operations benefit from skull base exper- Similarly, basilar apex aneurysms demand a range of

FIG. 2. A: Overview of relative access provided by candidate approaches considered for posterior fossa access, such as for
resection of brainstem cavernous malformations, highlighting the value of a skull base skill set in treating cerebrovascular patholo-
gies. B–D: Craniotomy, dural opening, and intradural access are compared from the surgeon’s perspective for standard retrosig-
moid (B), extended retrosigmoid (C), and posterior petrosectomy (D) approaches. Panels A–C used with permission from Barrow
Neurological Institute, Phoenix, Arizona. Panel D upper reprinted from Operative Techniques in Neurosurgery, Vol 4, Issue 1,
Zubay G, Porter RW, Spetzler RF, Transpetrosal approaches, pp 24–29, Copyright 2001, with permission from Elsevier. Panel D
lower reproduced from Horgan MA, Delashaw JB, Schwartz MS, Kellogg JX, Spektor S, McMenomey S. Transcrusal approach to
the petroclival region with hearing preservation. J Neurosurg. 2001;94:660–666. ©AANS, published with permission.

J Neurosurg Volume 137 • November 2022 1557

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

treatment strategies, depending on their morphology and gain more exposure to an overlapping set of approaches
conformation to the skull base (Fig. 3A). Although early and techniques, as well as a deeper understanding of how
microsurgical treatments for basilar apex aneurysms that they can be technically adapted across a broader range of
could not be accessed via a pterional craniotomy and trans- diseases.
sylvian approach (Fig. 3B) relied on the subtemporal ap- In addition to approaching mastery, complication man-
proach (Fig. 3C), the exposure it affords is relatively lim- agement highlights another high-yield area of complex
ited. Skull base approaches markedly improve safe access cranial synergy. Although advanced approach training is
to basilar artery aneurysms, with high-riding aneurysms partially provided by isolated fellowship training in either
accessible via the orbitozygomatic craniotomy or transcav- field, certain techniques for complication management are
ernous approach (Fig. 3D) and low-lying aneurysms acces- substantially less represented across the disciplines.
sible via Kawase’s anterior petrosectomy (Fig. 3E).36 The most feared complication in skull base microneu-
These examples are representative of the many ways in rosurgery is a stroke from inadvertent vascular injury.
which the complex cranial model can markedly enhance Although stroke is uncommon when an experienced sur-
the depth and breadth of an individual’s training experi- geon performs the procedure, it is an unambiguous risk
ence. Rather than 2 discrete years focused on important but associated with certain skull base resections, particularly
discrete skill sets, a fellow who undertakes serial fellow- for large, deep-seated tumors that envelop critical struc-
ships in skull base and cerebrovascular neurosurgery may tures, such as petrous apex meningiomas. Although skull

FIG. 3. A: Overview of relative access provided by candidate approaches considered for basilar artery aneurysm access,
highlighting the value of a skull base skill set in treating cerebrovascular pathologies. B–D: Access to the basilar apex via the
pterional craniotomy and transsylvian approach is relatively limited, which historically prompted the development of the subtempo-
ral approach (C). Modern skull base approaches, including the orbitozygomatic craniotomy (D) and anterior petrosectomy (E, e.g.,
Kawase’s approach), have further empowered treatment of high- and low-riding basilar aneurysms. Used with permission from
Barrow Neurological Institute, Phoenix, Arizona.

1558 J Neurosurg Volume 137 • November 2022

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

base surgeons are well versed in techniques for controlling gagement does not require one to perform those interven-
bleeding, cerebrovascular bypass expertise is much rarer. tions personally.
Thus, experience and comfort with a wide range of cere- Finally, as has been shown with multidisciplinary team
brovascular bypasses equip the skull base surgeon with a dynamics, the potential for creativity appears to be en-
dramatically larger array of techniques for repairing ar- hanced by diverse surgeon experiences and backgrounds.
terial injuries and replacing blood flow following vessel Many innovations across medical practice have arisen by
injury. applying an outside perspective to established tools or
Similarly, although every neurosurgeon learns the fun- techniques. Famously, Andreas Raabe encountered the
damentals of CSF leakage management, skull base opera- technology that would become indocyanine green video-
tions are fraught with challenging CSF and wound care angiography while perusing the vendor hall at a general
issues. These challenges are partly attributable to the ex- trauma meeting, where he saw a tool for liver surgeons that
tensive skull base drilling most operations require. How- would ultimately revolutionize intraoperative cerebrovas-
ever, numerous other factors also contribute, including cular imaging.44 Particularly salient to the complex cranial
dependent wounds involving the posterior fossa or trans- model is “macrovascular decompression,” an innovative
sphenoidal regions, the frequent need for dural resection procedure at the intersection of skull base and cerebrovas-
and grafting, and commonplace indications for postop- cular practice. In these unusual operations, large dolicho-
erative irradiation or chemotherapy.37 Skull base training ectatic vertebrobasilar loops are elevated off the cranial
correspondingly provides deep familiarity with advanced nerves and retained in a noncompressive position via sling,
reconstructive techniques. Common tools are familiar to clip, or complete rerouting with cerebrovascular bypass.45
most neurosurgeons, such as the nasoseptal flap, or fron- These elegant and challenging operations highlight the
tal sinus cranialization and skull base reconstruction with power of intellectual and technical crossover between the
a pedicled pericranium.38 Others are more esoteric but disciplines, as their successful execution relies on mastery
highly effective mechanisms for preventing or resolving of skull base techniques, as well as comfort with poten-
CSF leakage, including the “yo-yo technique” for muscle tially unstable cerebrovascular abnormalities.
pledget occlusion of a communication into the sphenoid si-
nus after anterior clinoidectomy, the tack hole–based scalp The Complex Cranial Surgeon
flap suspension technique for far-lateral reconstruction, A survey of the current microneurosurgical landscape
and the full range of rotational and free flap options.39,40 invites an essential and fundamental question: What is the
Indirectly, skull base surgery has already provided best strategy to provide future generations of residents and
2 salient models for demonstrating how the relationship fellows with the resources needed to master and advance
between open and endovascular domains should evolve the increasingly rarified craft of cerebrovascular micro-
for cerebrovascular neurosurgeons. First, SRS has proven neurosurgery, ensuring that patients who require open
safety and efficacy across a wide variety of benign skull treatments continue to have excellent outcomes? The com-
base diseases such that it is almost universally accepted plex cranial route presents an important and compelling
as a core component of the treatment paradigms for ves- training model when considered in light of the growing
tibular schwannoma, meningioma, pituitary adenoma, list of endovascular tools, the influx of practitioners from
paraganglioma, and some cases of trigeminal neuralgia.41 radiology and neurology into the endovascular space, the
Almost all skull base surgeons recommend SRS for some advantages of diverse perspectives on the treatment team,
of their patients. Yet, a minority of surgeons participate and the benefits of frequent and focused repetition for
directly in radiation planning or delivery. Instead, these high-level manual skill development. Several pathways
surgeons focus predominantly on surgical cases and defer into complex cranial specialization are reasonable. All
SRS responsibilities to interested colleagues and radiation share the notion of fellowship-level education in operative
oncologists. management of both skull base and open cerebrovascu-
Second, the advent and refinement of the endoscopic lar diseases. As we have highlighted, this paired training
endonasal approach (EEA) within skull base surgery have experience reflects a strong tradition from neurosurgical
led to marked improvements in treating several important history, innovation enhancement, and technical synergy.
entities, including pituitary adenoma and craniopharyn- Without question, endovascular treatments will become
gioma.42 Although initially met with resistance by some safer and more dominant in the future, and patients will
skull base surgeons, EEA techniques have improved in benefit from the leadership of neurosurgeons with endo-
safety and efficacy, resulting in their emergence as a front- vascular expertise on their teams. However, for individuals
line treatment for many midline lesions.43 Nevertheless, who are motivated to take on the uncommon and techni-
larger tumors extending beyond the carotid arteries still cally challenging operations that will continue to mandate
require transcranial techniques, emphasizing another ex- open microsurgical treatment, the complex cranial train-
ample of critical synergy between contemporary and tra- ing pathway is more likely to provide a critical volume of
ditional schools of training. microsurgical cases and to empower the lifelong evolution
With these resonant examples in mind, our perspective of technical excellence.
is that all cerebrovascular neurosurgeons should be fully
committed to engagement with the academic and clinical Acknowledgments
dimensions of endovascular treatments, just as their skull We thank the staff of Neuroscience Publications at Barrow
base peers are with SRS or EEA. Simultaneously, we en- Neurological Institute for assistance with manuscript preparation.
courage more widespread recognition that intellectual en- Dr. Graffeo thanks his peers, Dr. Perry, Dr. Carlstrom, and Dr.

J Neurosurg Volume 137 • November 2022 1559

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

Srinivasan, for the spirited discussions that continue to inform his 17. Harbaugh RE, Agarwal A. Training residents in endovascular
perspective on complex cranial surgery. neurosurgery. Neurosurgery. 2006;59(5)(suppl 3):S277-S281,
S3-S13.
18. Todnem N, Ward A, Alleyne CH Jr. How hybrid/dual training
References influences cerebral aneurysm management. Contemp Neuro-
1. Lawton MT, Lang MJ. The future of open vascular neuro- surg. 2019;41(3):1-8.
surgery: perspectives on cavernous malformations, AVMs, 19. Jiang B, Bender MT, Hasjim B, et al. Aneurysm treatment
and bypasses for complex aneurysms. J Neurosurg. 2019;​ practice patterns for newly appointed dual-trained cerebro-
130(5):1409-1425. vascular/endovascular neurosurgeons: Comparison of open
2. Luther E, McCarthy DJ, Brunet MC, et al. Treatment and di- surgical to neuroendovascular procedures in the first 2 years
agnosis of cerebral aneurysms in the post-International Sub- of academic practice. Surg Neurol Int. 2017;8:154.
arachnoid Aneurysm Trial (ISAT) era: trends and outcomes. 20. Volovici V, Verploegh ISC, Vos JC, et al. Can young vascu-
J Neurointerv Surg. 2020;12(7):682-687. lar neurosurgeons become proficient in microsurgical clip
3. Wiebers DO, Whisnant JP, Huston J III, et al. Unruptured reconstruction in the endovascular era? A Rotterdam cohort
intracranial aneurysms: natural history, clinical outcome, spanning 2 decades with propensity score matching for com-
and risks of surgical and endovascular treatment. Lancet. plexity. World Neurosurg. 2020;144:e780-e788.
2003;362(9378):103-110. 21. Carlson ER. Collective wisdom and multidisciplinary tumor
4. Lindgren A, Vergouwen MDI, van der Schaaf I, et al. Endo- boards. J Oral Maxillofac Surg. 2014;72(2):235-236.
vascular coiling versus neurosurgical clipping for people with 22. Lamb BW, Brown KF, Nagpal K, Vincent C, Green JS,
aneurysmal subarachnoid haemorrhage. Cochrane Database Sevdalis N. Quality of care management decisions by mul-
Syst Rev. 2018;8:CD003085. tidisciplinary cancer teams: a systematic review. Ann Surg
5. Molyneux A, Kerr R, Stratton I, et al. International Sub- Oncol. 2011;18(8):2116-2125.
arachnoid Aneurysm Trial (ISAT) of neurosurgical clipping 23. Brodbeck FC, Kerschreiter R, Mojzisch A, Schulz-Hardt
versus endovascular coiling in 2143 patients with ruptured S. Group decision making under conditions of distributed
intracranial aneurysms: a randomised trial. Lancet. 2002;​ knowledge: the information asymmetries model. AMRO.
360(9342):1267-1274. 2007;32(2):459-479.
6. Walcott BP, Stapleton CJ, Choudhri O, Patel AB. Flow diver- 24. Friedrich MJ. Practice makes perfect: risk-free medical train-
sion for the treatment of intracranial aneurysms. JAMA Neu- ing with patient simulators. JAMA. 2002;288(22):2808-2812.
rol. 2016;73(8):1002-1008. 25. Jonides J. How does practice makes perfect? Nat Neurosci.
7. Piazza M, Nayak N, Ali Z, et al. Trends in resident operative 2004;7(1):10-11.
teaching opportunities for treatment of intracranial aneu- 26. Shee K, Ghali FM, Hyams ES. Practice makes perfect: cor-
rysms. World Neurosurg. 2017;103:194-200. relations between prior experience in high-level athletics and
8. Yaeger KA, Munich SA, Byrne RW, Germano IM. Trends in robotic surgical performance do not persist after task repeti-
United States neurosurgery residency education and training tion. J Surg Educ. 2017;74(4):630-637.
over the last decade (2009-2019). Neurosurg Focus. 2020;​ 27. Moulton CAE, Dubrowski A, Macrae H, Graham B, Grober
48(3):E6. E, Reznick R. Teaching surgical skills: what kind of practice
9. ACGME Program Requirements for Graduate Medical makes perfect? A randomized, controlled trial. Ann Surg.
Education in Neurological Surgery. Neurological Surgery 2006;244(3):400-409.
Program Requirements and FAQs. Accreditation Council 28. Applebaum MA, Doren EL, Ghanem AM, Myers SR, Har-
for Graduate Medical Education. Accessed March 11, 2022. rington M, Smith DJ. Microsurgery competency during
https://www.acgme.org/Specialties/Program-Requirements- plastic surgery residency: an objective skills assessment of an
and-FAQs-and-Applications/pfcatid/10/Neurological%20 integrated residency training program. Eplasty. 2018;18:e25.
Surgery 29. Dammerer D, Putzer D, Wurm A, Liebensteiner M, Nogler
10. Bina RW, Lemole GM Jr, Dumont TM. On resident duty hour M, Krismer M. Progress in knee arthroscopy skills of resi-
restrictions and neurosurgical training: review of the litera- dents and medical students: a prospective assessment of
ture. J Neurosurg. 2016;124(3):842-848. simulator exercises and analysis of learning curves. J Surg
11. Mukherjee S, Pringle C, Crocker M. A nine-year review of Educ. 2018;75(6):1643-1649.
medicolegal claims in neurosurgery. Ann R Coll Surg Engl. 30. Barr J, Graffeo CS. Procedural experience and confidence
2014;96(4):266-270. among graduating medical students. J Surg Educ. 2016;​73(3):​
12. Graffeo CS, Perry A, Carlstrom LP, et al. 3D printing for 466-473.
complex cranial surgery education: Technical overview and 31. Lawton MT. Basilar apex aneurysms: surgical results and
preliminary validation study. J Neurol Surg B Skull Base. perspectives from an initial experience. Neurosurgery.
Published online February 22, 2021. doi:10.1055/​s-0040- 2002;50(1):1-10.
1722719 32. Esposito G, Dias SF, Burkhardt JK, et al. Selection strategy
13. Perry A, Graffeo CS, Carlstrom LP, Anding WJ, Link MJ, for optimal keyhole approaches for middle cerebral artery
Rangel-Castilla L. Novel rodent model for simulation of syl- aneurysms: lateral supraorbital versus minipterional crani-
vian fissure dissection and cerebrovascular bypass under sub- otomy. World Neurosurg. 2019;122:e349-e357.
arachnoid hemorrhage conditions: technical note and timing 33. Jean WC. Skull Base Surgery: Strategies. Thieme; 2019.
study. Neurosurg Focus. 2019;46(2):E17. 34. Ivan ME, Safaee MM, Martirosyan NL, et al. Anatomical tri-
14. Belykh E, Giovani A, Abramov I, et al. Novel system of angles defining routes to anterior communicating artery an-
simulation models for aneurysm clipping training: descrip- eurysms: the junctional and precommunicating triangles and
tion of models and assessment of face, content, and construct the role of dome projection. J Neurosurg. 2019;132(5):1517-
validity. Oper Neurosurg (Hagerstown). 2021;21(6):558-569. 1528.
15. Flamm ES, Professor M. Professor M. Gazi Yaşargil: an ap- 35. Tayebi Meybodi A, Borba Moreira L, Zhao X, Preul MC,
preciation by a former apprentice. Neurosurgery. 1999;​45(5):​ Lawton MT. Anatomical analysis of the vagoaccessory tri-
1015-1018. angle and the triangles within: the suprahypoglossal, infra-
16. Gottfried ON, Rovit RL, Popp AJ, Kraus KL, Simon AS, hypoglossal, and hypoglossal–hypoglossal triangles. World
Couldwell WT. Neurosurgical workforce trends in the United Neurosurg. 2019;126:e463-e472.
States. J Neurosurg. 2005;102(2):202-208. 36. Tayebi Meybodi A, Benet A, Rodriguez Rubio R, et al.

1560 J Neurosurg Volume 137 • November 2022

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC


Neurosurgical forum

Comparative analysis of orbitozygomatic and subtemporal 44. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V.
approaches to the basilar apex: a cadaveric study. World Neu- Near-infrared indocyanine green video angiography: a new
rosurg. 2018;119:e607-e616. method for intraoperative assessment of vascular flow. Neu-
37. Fraser S, Gardner PA, Koutourousiou M, et al. Risk factors rosurgery. 2003;52(1):132-139.
associated with postoperative cerebrospinal fluid leak after 45. Srinivasan VM, Labib MA, Furey CG, Catapano JS, Lawton
endoscopic endonasal skull base surgery. J Neurosurg. 2018;​ MT. The “binder ring” bypass: transection, rerouting, and
128(4):1066-1071. reanastomosis as an alternative to macrovascular decom-
38. Gagliardi F, Boari N, Mortini P. Reconstruction techniques in pression of a dolichoectatic vertebral artery. Oper Neuro-
skull base surgery. J Craniofac Surg. 2011;22(3):1015-1020. surg (Hagerstown). Published online February 11, 2022.
39. Ali MS, Magill ST, McDermott MW. Far lateral craniotomy doi:10.1227/ONS.0000000000000099
closure technique for preservation of suboccipital muscula-
ture. J Neurol Surg B Skull Base. 2021;82(5):562-566. Disclosures
40. Chi JH, Sughrue M, Kunwar S, Lawton MT. The “yo-yo” The authors report no conflict of interest.
technique to prevent cerebrospinal fluid rhinorrhea after
anterior clinoidectomy for proximal internal carotid artery Correspondence
aneurysms. Neurosurgery. 2006;59(1)(suppl 1):ONS101-
ONS107. Michael T. Lawton: neuropub@barrowneuro.org.
41. Kondziolka D. Current and novel practice of stereotactic ra-
INCLUDE WHEN CITING
diosurgery. J Neurosurg. 2019;130(6):1789-1798.
Published online April 29, 2022; DOI: 10.3171/2022.3.JNS212939.
42. Gardner PA, Prevedello DM, Kassam AB, Snyderman CH,
Carrau RL, Mintz AH. The evolution of the endonasal ap-
proach for craniopharyngiomas. J Neurosurg. 2008;108(5):​
1043-1047.
43. Cavallo LM, Somma T, Solari D, et al. Endoscopic endonasal
transsphenoidal surgery: history and evolution. World Neuro-
surg. 2019;127:686-694.

J Neurosurg Volume 137 • November 2022 1561

Unauthenticated | Downloaded 03/28/24 03:51 PM UTC

You might also like