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doi: 10.1227/NEU.0000000000000222
Training in Vascular Neurosurgery

Cerebrovascular Neurosurgery in Evolution: The Endovascular Paradigm

Sorkin, Grant C. MD*,‡; Dumont, Travis M. MD*,‡; Eller, Jorge L. MD*,‡; Mokin, Maxim MD, PhD*,‡; Snyder, Kenneth V. MD, PhD*,‡,§,¶,‖; Levy, Elad I. MD*,‡,§,‖; Siddiqui, Adnan H. MD, PhD*,‡,§,‖,#; Hopkins, L. Nelson MD*,‡,§,‖,#

Section Editor(s): Bendok, Bernard R. MD; Levy, Elad I. MD

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Author Information

Departments of *Neurosurgery,

§Radiology, and

Neurology, School of Medicine and Biomedical Sciences, and

Toshiba Stroke and Vascular Research Center, University at Buffalo, State University of New York;

Department of Neurosurgery, Gates Vascular Institute, Kaleida Health Buffalo, New York;

#Jacobs Institute, Buffalo, New York

Correspondence: L. Nelson Hopkins, MD, Jacobs Institute, 875 Ellicott St, 5th Floor, Buffalo NY 14203. E-mail:

Received June 17, 2013

Accepted October 11, 2013

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Endovascular technique represents an important, minimally invasive approach to treating cerebrovascular disease. In this article, we discuss the origins of endovascular neurosurgery as a discipline in the context of important technical milestones, evidence-based medicine, and future cerebrovascular neurosurgical training. Cerebrovascular neurosurgery has seen a steady, convergent evolution toward the surgeon capable of seamless incorporation of open and endovascular approaches to any complex vascular disease affecting the central nervous system. Neurosurgery must assume the leadership role in the multidisciplinary neurovascular team.

ABBREVIATIONS: AVM, arteriovenous malformation

CCF, carotid-cavernous fistula

SAMMPRIS, Stenting vs Aggressive Medical Therapy for Intracranial Arterial Stenosis

All surgical disciplines are subject to a paradox in needing to maximize exposure to safely address disease while minimizing disruption of vulnerable surrounding structures. Surgery within the central nervous system epitomizes this conflict because the disruption of nonpathological tissue is unforgiving. Within this paradox, we find the impetus for the refinement and progression of surgical technique. Herein lies the appeal of minimally invasive surgery. In this article, we describe milestones of endovascular technique with hopes of illustrating the convergent, rather than divergent, evolution between open and endovascular neurosurgery in training the hybrid vascular neurosurgeon of today’s generation.

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The earliest attempts at “endovascular” treatment consisted of procedures involving open surgical approaches to the carotid system combined with intravascular treatment of pathological conditions. The hybrid nature of endovascular technique revealed itself from its origins as a discipline (Figure). This evolution can be traced back to the early 1900s, when an open approach to the external carotid artery allowed embolization of malignant tumors of the head and neck with paraffin and Vaseline.1,2 In the 1930s, combined approaches were used to treat carotid-cavernous fistulas (CCFs) by surgical trapping of the internal carotid artery followed by use of muscle for embolization.3-5 This important decade included the earliest successful extravascular treatment of cerebral aneurysms by clip ligation and wrapping via craniotomy6,7 and remains a milestone in the history of cerebrovascular neurosurgery. It was also during this time that the earliest endovascular embolization of aneurysms was attempted via direct surgical exposure by craniotomy.8 These hybrid procedures continued into the 1970s, at which time Parkinson described CCF treatment with internal carotid artery preservation by direct packing through the infratrochlear cavernous triangle, later known as the Parkinson triangle.9,10

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With the complexity of the hybrid procedures described above came the desire to reduce morbidity and mortality. In 1953, Seldinger’s technique for catheter replacement of a needle for percutaneous arterial access was pivotal to the technique of cerebral angiography pioneered by Moniz in the 1920s (Figure).11-13 This technique also served as an impetus for the development of angiography catheters.12,13 These catheters allowed selective vessel injection for angiography and for intervention. Early attempts of arteriovenous malformation (AVM) embolization described by Luessenhop et al14 in the 1960s, in which embolizate was blindly introduced into the surgically exposed carotid system (Figure), were supplanted by percutaneous, catheter-based embolization of blood vessels that were located with increasing selectivity within the vascular tree.2,15,16 This approach prompted the use of a variety of embolic materials in the search for a material that was soft enough to mold to vascular lesions, had low viscosity and controlled polymerization for delivery and penetration, and was radiopaque for visibility. Such materials included Silastic pellets,14 silicone,17 steel and porcelain pellets,18 Gelfoam (Pharmacia & Upjohn, New York, New York),16 blood clots,19 isobutyl-2-cynoacrylate,20 and dural fragments.2 These precursors helped to refine favorable embolizate attributes, leading to the agents used today, including n-butyl-cyanoacrylate, Onyx (Covidien, Mansfield, Massachusetts), and polyvinyl alcohol particles.

As catheter and percutaneous technique matured, an important endovascular milestone occurred in the 1970s (Figure). Serbinenko21 performed the first successful embolization of a direct CCF with internal carotid artery preservation via an endovascular approach by delivering detachable balloons through a carotid wall defect. Although more successful for CCFs than AVMs or aneurysms, the introduction of detachable balloons was important because the detachable balloon represented the first widely accepted tool developed specifically within the emerging field of endovascular neurosurgery in addressing intracranial vascular pathology.5,22-24 Use of these balloons continued until the 2000s, supplanted by newer embolization technologies that are discussed below.

The context of this milestone deserves further elaboration. Before the introduction of balloons, advancement of endovascular technique relied on hybrid procedures that required open and endovascular approaches to complex vascular disease like CCFs and AVMs. Detachable balloons provided the potential to treat these conditions completely by endovascular means. As a consequence, the field of endovascular neurosurgery became independent and self-sustainable from open vascular neurosurgery, and future advances occurred in isolation. The dichotomy between open vs endovascular neurosurgery was established.

The next major advancement in endovascular technology occurred in the mid-1980s with the introduction of guidewire-supported microcatheters for cerebral use (Figure).2 Previously, navigation of microcatheters was contingent on preferential bulk flow, making selective catheterization of sidewall vessels difficult. Guidewire support allowed improved navigation to sidewall vessels and served as a more stable platform for aneurysm catheterization. This development also introduced a new stimulus for microcatheter and microwire technological advancement, from which came microcatheters and microwires with progressive segmental softness, nickel-titanium alloy (nitinol) construction, hydrophilic coatings, improved torquability, and improved radiopacity.2 These attributes are important in contemporary microcatheters and microwires.

As March 23, 1937, was important to cerebrovascular neurosurgery in marking the first clip ligation of a brain aneurysm, March 6, 1990, was equally important in marking the first detachable coil embolization of a brain aneurysm (Figure).25-27 Before the development of Guglielmi detachable coils, “free coils” could be delivered through a catheter with a “pusher” wire that did not allow adjustment in the event of suboptimal positioning. This characteristic made them more appropriate for large AVMs or parent vessel sacrifice rather than for delicate aneurysm interventions.2 With the advent of detachable coils, neurointerventionists had a stable platform for calculated delivery and the ability to adjust or change coils if malpositioned. This breakthrough served not only as the impetus for the advancement of coiling technique and technology but also as a stimulus for coiling adjunct technologies. The emergence of aneurysm neck remodeling with compliant intracranial balloons or intracranial stents has expanded the technical feasibility for endovascular treatment of aneurysms beyond the favorable dome-to-neck ratio to which first-generation coil technology was limited.28-33 Furthermore, as this adjunct technology matured, stenting and balloon angioplasty became a means to treat other vascular disease independently of coiling, including intracranial atherosclerotic disease and stroke. This effectively expanded the spectrum of disease amenable to endovascular intervention.34-39 Perhaps the most important contribution of Guglielmi detachable coils within the context of the field is the eventual acceptance of coil embolization as an alternative to clip ligation in the management of intracranial aneurysms.40 This effectively brought endovascular technology to the forefront of the cerebrovascular neurosurgical community and marked the modern era of endovascular neurosurgery.

With interest in endovascular technique primed, the 1990s became a time when stroke gained recognition as a surgical entity (Figure). Local intra-arterial thrombolytic therapy showed promising recanalization rates for intracranial large-vessel occlusions.41,42 Interest in intra-arterial therapy for acute ischemic stroke culminated in the development of the Merci Retriever (Stryker, Kalamazoo, Michigan), a first-generation mechanical embolectomy device designed for large-vessel intracranial thrombectomy.43 This device represented the precursor to the “stent retrievers” currently used for acute ischemic stroke revascularization. Within the context of the field, the Merci Retriever represented a “surgical” treatment to a disease traditionally viewed as a medical entity that accounted for a major cause of death in the United States.44 This emergence of acute stroke revascularization as a surgical entity in the cerebrovascular neurosurgical community implied the need for a broader familiarity of intracranial and extracranial vascular pathology that traditionally fell within the purview of neurology rather than neurosurgery. The ramifications of such overlap between disciplines must be reflected in the training of future cerebrovascular neurosurgeons.

The most recent endovascular milestone came in the mid-2000s in the form of endoluminal reconstruction via flow diversion (Figure). Stents designed with higher metal coverage (30%-50%) and lower porosity preferentially effected bulk flow away from an aneurysm, thereby effectively excluding an aneurysm from the intracranial circulation with preservation of parent vessels.45-47 Flow diversion revolutionized our management of giant aneurysms, which were traditionally treated with surgical ligation or bypass that consisted of complex skull base exposures with lengthy operative times, increased morbidity and mortality rates, long hospitalizations, or need for parent vessel sacrifice.48-50 We now had the option of endoluminal reconstruction with flow diversion and parent vessel preservation performed under conscious sedation confined within a 2- to 3-day hospitalization. The above milestones represent the application of progressive thinking and technological advancement to challenging cerebrovascular disease.

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With rapidly evolving technology and > 20 years since the advent of detachable coils, much experience has been gained with modern neurological endovascular technique. The management of intracranial aneurysms is arguably the biggest contribution of endovascular technique to modern cerebrovascular neurosurgery. The International Subarachnoid Aneurysm Trial demonstrated a 7.4% absolute risk reduction in death and dependency at 1 year in patients treated with endovascular coil embolization vs clip ligation for patients with a ruptured aneurysm.40 This landmark study gave validity to coil embolization as a first-line treatment for ruptured aneurysms and, in doing so, strengthened the role of coil embolization in cerebrovascular neurosurgery. The management of giant aneurysms has also been revolutionized with endovascular technique in the form of flow diversion. We now have promising prospective series that show 6-month occlusion rates as high as 73.6% to 95%, with major complication rates ranging from 0% to 6.5%.51-54 For untreated giant aneurysms with 5-year rupture rates of 40% in the anterior circulation and 50% in the posterior circulation,55 as well as surgical morbidity and mortality rates as high as 30% and 10%, respectively,49,56-58 we have compelling literature supporting this treatment option for this formidable disease entity.

Current literature supporting the use of endovascular revascularization for extracranial and intracranial atherosclerotic disease has less accord. Data from the Carotid Revascularization Endarterectomy vs Stenting Trial demonstrated no difference in the composite 4-year primary end point of stroke/myocardial infarction/death between stented and endarterectomy groups.59 However, within the periprocedural period, more minor strokes were noted in the stented group, whereas more myocardial infarctions were noted in the endarterectomy group. Although these opposing risks demonstrate the importance of patient selection for carotid revascularization and highlight a degree of equipoise between carotid stenting and carotid endarterectomy, superiority of stenting has not been shown. Therefore, carotid stenting remains complementary to, rather than a substitute for, open carotid revascularization.

We have gained valuable experience for the role of endovascular intervention for intracranial atherosclerotic disease. Before the Stenting vs Aggressive Medical Therapy for Intracranial Arterial Stenosis trial (SAMMPRIS),35 intracranial percutaneous transluminal angioplasty and stenting was used with promising results for the management of symptomatic intracranial atherosclerosis.34,37,39 Enrollment in this trial was stopped early because of a 30-day stroke or death rate of 14.7% in the angioplasty and stenting arm compared with 5.8% in the medical arm, with 1-year stroke or death rates of 20% and 12.2%, respectively.35 These results greatly influenced our endovascular approach to secondary stroke prevention related to intracranial atherosclerotic disease. We are currently evaluating the use of submaximal angioplasty without stenting in the cohort of patients who remain symptomatic despite the aggressive medical therapy described in SAMMPRIS.60 The SAMMPRIS study illustrates the importance of understanding the natural history of this disease and medical alternatives for optimized stroke prevention.

The endovascular management of acute ischemic stroke is also a source of great debate within current literature. Three trials were recently reported that force us to examine the role of endovascular revascularization compared with medical therapy for acute ischemic stroke.61-63 The Interventional Management of Stroke III trial compared intravenous tissue-type plasminogen activator therapy alone vs combined intravenous tissue-type plasminogen activator and intra-arterial therapies.61 This study was prematurely stopped owing to prespecified definitions of futility and lack of effect in improving functional outcomes in the treatment arm. Importantly, safety profiles in both arms were similar. Furthermore, when a prespecified subset evaluation was performed (Van Elteren analysis) in patients who had confirmed large-vessel occlusion, an improvement in 3-month functional outcome was appreciated in favor of endovascular intervention (P = .001).61 In the Mechanical Retrieval and Recanalization of Stroke Clots Using Embolectomy trial, patients were randomized to intravenous thrombolytics vs endovascular thrombectomy with inclusion criteria specifying large-vessel occlusion and perfusion imaging.63 The investigators found no difference in functional outcomes between 64 patients who underwent thrombectomy and 54 patients who received systemic tissue-type plasminogen activator despite penumbral pattern. However, despite a low revascularization rate of 67% owing to first-generation thrombectomy devices (Merci Retriever or Penumbra System [Penumbra, Inc, Alameda, California]), improvement in the 3-month modified Rankin Scale score (3.2 [2.6-3.8] vs 4.1 [3.7-4.5]; P = .04) and median absolute infarct growth (9.0 vs 72.5 mL; P < .001) was shown for patients in whom reperfusion and revascularization were achieved. Lastly, in Synthesis Expansion: A Randomized Controlled Trial on Intra-Arterial vs Intravenous Thrombolysis in Acute Ischemic Stroke, investigators found no improvement in 3-month modified Rankin Scale score in the endovascular group vs the thrombolytic therapy group.62 However, noninvasive imaging demonstrating target vessel occlusion was not performed, and among 181 patients assigned to the endovascular group, only 165 actually received intra-arterial therapy, which consisted of wire manipulation and intra-arterial thrombolytics, rather than modern thrombectomy devices (n = 56). Although scientifically sound, these studies epitomize the difficulties of producing and applying randomized clinical trials in such a rapidly evolving field. At first glance, the evidence does not support endovascular therapy for acute ischemic stroke, but below the surface, one realizes that imaging, technology, and technique have advanced generations beyond that used in these studies. Furthermore, subsequent registries and trials have shown improved safety and efficacy of modern revascularization techniques.64-66 Lastly, these studies do not address the stroke population who presents outside the thrombolytic window, for whom endovascular intervention remains the sole option for revascularization.

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As evident by its moniker given by the Accreditation Council for Graduate Medical Education, “endovascular surgical neuroradiology” spans the disciplines of neurosurgery, neurology, and neuroradiology.67,68 Therefore, beyond adequate technical training, practitioners need to understand the breadth of natural histories, treatment alternatives, and imaging modalities that are necessary for the various vascular diseases encountered.

Multiple performance standards by medical societies have been developed for catheter-based cervicocerebral diagnostic and therapeutic interventions.69-74 These standards reiterate the fundamental need for an understanding of neurological pathophysiology, anatomy, critical care, and diagnostic modalities in those who perform the interventions and recognize the unforgiving nature of complications within the central nervous system. Thus, existing standards require a dedicated year of formal neurodiagnostic or vascular neurology training beyond radiology or neurology residency before entering into training in endovascular surgical neuroradiology.69 Furthermore, a minimum of 100 appropriately supervised cervicocerebral angiograms is needed for credentialing before interventional training.69-71,75,76 Lastly, because the interpretation of an angiogram is as important as the technique, operators are required to recognize and, if needed, to address all possible neurovascular processes, thereby precluding a limited form of credentialing.69 Acknowledging the importance and permanence of the endovascular paradigm to cerebrovascular neurosurgery, neurosurgical residency programs are now required to incorporate endovascular training into their curriculum.68,70,71

These standards provide the pathways necessary to produce clinicians with the acumen to perform endovascular interventions, but they do not tell us the requirements of today’s generation of cerebrovascular neurosurgeons. With the knowledge we have and will continue to acquire, it becomes apparent that endovascular technique can be first-line treatment, as in the case of ruptured or giant aneurysms; complementary to open technique, as in the case of carotid disease; or second to medical therapy, as in the case of intracranial atherosclerosis. Furthermore, the combined use of endovascular technique with open surgery, as in the case of tumor or AVM resection, reaffirms its longevity and adjunctive nature as a tool for preoperative planning. As technology progresses, so will the applications of endovascular technique, and the lines between neurology, neurosurgery, and radiology will continue to blur. For these reasons, neurosurgery remains the ideal discipline to understand when and how to use endovascular tools to treat all vascular disease that affects the nervous system. Today’s generation of cerebrovascular neurosurgeons must incorporate these tools into their armamentarium because their use will continue to serve as minimally invasive alternatives in treating cerebrovascular disease.

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Cerebrovascular neurosurgery has seen a steady, convergent evolution toward the surgeon capable of seamless incorporation of open and endovascular approach to any complex vascular disease affecting the central nervous system. Neurosurgery must assume the leadership role in the multidisciplinary neurovascular team.

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Dr Hopkins receives grant/research support from Toshiba; serves as a consultant to Abbott, Boston Scientific, Cordis, Micrus, and Silk Road; holds financial interests in Access Closure, Augmenix, Boston Scientific, Claret Medical, Endomation, Micrus, and Valor Medical; holds a board/trustee/officer position with Access Closure and Claret Medical; serves on Abbott Vascular’s speakers’ bureau; and has received honoraria from Bard, Boston Scientific, Cleveland Clinic, Complete Conference Management, Cordis, Memorial Health Care System, and the Society for Cardiovascular Angiography and Interventions. Dr Levy receives research grant support, other research support (devices), and honoraria from Boston Scientific and research support from Codman & Shurtleff, Inc and ev3/Covidien Vascular Therapies; has ownership interests in Intratech Medical Ltd and Mynx/Access Closure; serves as a consultant on the board of Scientific Advisors to Codman & Shurtleff, Inc; serves as a consultant per project and/or per hour for Codman & Shurtleff, Inc, ev3/Covidien Vascular Therapies, and TheraSyn Sensors, Inc; and receives fees for carotid stent training from Abbott Vascular and ev3/Covidien Vascular Therapies. Dr Levy receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr Mokin has received an educational grant from Toshiba. Dr Siddiqui has received research grants from the National Institutes of Health (coinvestigator: NINDS 1R01NS064592-01A1, Hemodynamic Induction of Pathological Remodeling Leading to Intracranial Aneurysms) and the University at Buffalo (Research Development Award) (neither is related to this report); holds financial interests in Hotspur, Intratech Medical, StimSox, Valor Medical, and Blockade Medical; serves as a consultant to Codman & Shurtleff, Inc, Concentric Medical, Covidien Vascular Therapies, GuidePoint Global Consulting, Penumbra, Inc, Stryker Neurovascular, and Pulsar Vascular; belongs to the speakers’ bureaus of Codman & Shurtleff, Inc and Genentech; serves on National Steering Committees for the Penumbra, Inc 3D Separator Trial and Covidien SWIFT PRIME Trial; serves on an advisory board for Codman & Shurtleff and Covidien Vascular Therapies; and has received honoraria from American Association of Neurological Surgeons’ courses, Annual Peripheral Angioplasty and All That Jazz Course, Penumbra, Inc, and from Abbott Vascular and Codman & Shurtleff, Inc for training other neurointerventionists in carotid stenting and for training physicians in endovascular stenting for aneurysms. Dr Siddiqui receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr Snyder serves as a consultant and a member of the speakers’ bureau for Toshiba and has received honoraria from Toshiba. He serves as a member of the speakers’ bureau for and has received honoraria from ev3 and The Stroke Group. Drs Dumont, Eller, and Sorkin report no financial relationships.

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We thank Paul H. Dressel, BFA, for preparation of the figure and Debra J. Zimmer for editorial assistance.

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Advances; Endovascular neurosurgery; Technique; Technology; Training

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