Endovascular Treatment of Ruptured Vertebrobasilar Dissecting Aneurysms Using Flow Diversion Embolization Devices: Single-Institution Experience

Endovascular Treatment of Ruptured Vertebrobasilar Dissecting Aneurysms Using Flow Diversion Embolization Devices: Single-Institution Experience

Original Article Endovascular Treatment of Ruptured Vertebrobasilar Dissecting Aneurysms Using Flow Diversion Embolization Devices: Single-Institutio...

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Original Article

Endovascular Treatment of Ruptured Vertebrobasilar Dissecting Aneurysms Using Flow Diversion Embolization Devices: Single-Institution Experience Waldo R. Guerrero1, Santiago Ortega-Gutierrez1, Minako Hayakawa2, Colin P. Derdeyn2, James D. Rossen3, David Hasan4, Edgar A. Samaniego1

OBJECTIVE: Treatment of ruptured posterior circulation dissecting aneurysms is technically challenging with potentially high morbidity and mortality. We sought to assess the safety and feasibility of using a flow-diversion device (FDD) and a specific acute antiplatelet aggregation protocol in the management of ruptured dissecting aneurysms.

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METHODS: Subjects with ruptured dissecting aneurysms treated during a 3-year period were retrospectively identified from a prospective registry. Intraoperative complications, morbidity, and mortality were recorded. Tirofiban maintenance infusion without bolus was administered intravenously immediately after deployment of the FDD, and almost all patients were loaded with dual antiplatelet (aspirin and clopidogrel) post procedure. Clinical follow-up evaluation and modified Rankin Scale were assessed.

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RESULTS: Nine subjects with ruptured posterior circulation dissecting aneurysms were treated with an FDD: 5 vertebral artery, 2 basilar artery, and 2 posterior inferior cerebellar artery aneurysms. Average World Federation of Neurosurgical Societies score was 2 (range 1e5). Seven patients had external ventricular drain placed acutely for hydrocephalus. Eight patients received tirofiban infusion without bolus after FDD. No intraoperative complications occurred. Two subjects developed asymptomatic intraparenchymal hemorrhage found on surveillance noncontrast

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computed tomography. One subject suffered a major intraparenchymal hemorrhage and died a few days post intervention after additional anticoagulation was started for a left ventricular assist device. Follow-up modified Rankin Scale within 12 months was 0 in 3 subjects, 1 in 3 subjects, 2 in 1 subject, and 4 in 1. CONCLUSIONS: Treatment of dissecting posterior circulation aneurysms with FDDs is feasible and a potential alternative to deconstructive techniques.

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INTRODUCTION

D

issecting aneurysms of the vertebrobasilar system are an uncommon etiology of nontraumatic subarachnoid hemorrhage (SAH). Ruptured vertebrobasilar dissecting aneurysms have a high rate of early rehemorrhage of approximately 70%.1 Furthermore, they are associated with poor clinical outcome and a high mortality.2 Early endovascular treatment is favored over surgical clipping due to the significant risk of cranial nerve and brainstem injury associated with open surgical approaches.3 Endovascular treatment options include parent vessel sacrifice or proximal occlusion (flow reversal in the disease segment) with a success rate of 62%e73%.4,5 Madaelil et al6 reported 12 patients with good collateral circulation who underwent endovascular sacrifice. They suggested that this technique could be the preferred treatment for acutely ruptured

Key words Antiplatelet - Dissecting aneurysms - Flow-diversion device - Intraparenchymal hemorrhage

From the 1Departments of Neurology, and 2Radiology, University of Iowa Hospital and Clinics, Iowa City; 3Division of Cardiovascular Medicine, Department of Internal Medicine, University of Iowa Hospital and Clinics, Iowa City; and 4Department of Neurosurgery, University of Iowa Hospital and Clinics, Iowa City, Iowa, USA

Abbreviations and Acronyms FDD: Flow-diversion device mRS: modified Rankin Scale PICA: Posterior inferior cerebellar artery SAC: Stent-assisted coiling SAH: Subarachnoid hemorrhage VA: Vertebral artery VP: Ventriculoperitoneal

Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.09.125

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To whom correspondence should be addressed: Edgar A. Samaniego, M.D. [E-mail: [email protected]]

Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.

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ORIGINAL ARTICLE WALDO R. GUERRERO ET AL.

TREATMENT OF RUPTURED VERTEBROBASILAR DISSECTING ANEURYSMS WITH FLOW DIVERSION

Endovascular Treatment All procedures were performed under general anesthesia. An access guide catheter was used to selectively catheterize the V3 segment of the VA under fluoroscopic guidance. A Marksman microcatheter (Medtronic, Minneapolis, MN) was then advanced distal to the ruptured aneurysm using a Synchro-2 microwire (Stryker, Kalamazoo, MI) under roadmap. One or 2 FDDs (Pipeline embolization device, Medtronic) were deployed through the Marksman microcatheter using a coaxial guide-catheter system. No coils were used in the treatment of the aneurysms. Timing of the FDD placement (post-SAH treatment day), number of FDDs used, dose of antiplatelet agents, perioperative management, and clinical and angiographic follow-ups were analyzed.

dissecting aneurysms involving the distal vertebral artery (VA) in the presence of good collateral circulation. In their series of 12 patients, 2 patients had an ischemic infarct and 1 patient died.6 However, parent vessel sacrifice is not an option if the dissecting aneurysm extends into the basilar artery and posterior inferior cerebellar artery (PICA). Reconstructive techniques with stent-assisted coiling (SAC) have also been described.7 Reconstruction of the parent artery with a flow-diversion device (FDD) may provide a feasible and safe treatment alternative in managing these complex and challenging aneurysms. Few investigators have reported their experience in treating ruptured aneurysms with FDD.7-9 Only 1 case series has described its use in the treatment of ruptured dissecting aneurysms.10 FDDs may be effective in these lesions due to flow modification, elimination of shear stress, and reconstruction of the parent artery with subsequent aneurysmal thrombosis. Nevertheless, the need for antiplatelet therapy during and after deployment of FDDs has restricted their use mainly to unruptured saccular aneurysms. We report our single-center experience in treating ruptured dissecting aneurysms with FDDs and describe our antiplatelet regimen.

Antiplatelet Regimen Tirofiban (Medicure, Winnepeg, Canada) was administered immediately following deployment of the FDD: no bolus was given and an infusion of 0.1 mcg/kg/min was maintained for 2e6 hours after the procedure. All patients were also loaded with dual antiplatelets (aspirin 325 mg and clopidogrel 600 mg) immediately post procedure (Table 1). Aspirin and clopidogrel response testing was not performed. RESULTS

METHODS Demographic, Clinical, and Aneurysm Characteristics Nine patients (6 men) between 31 and 72 years old were identified and included in the analysis. The SAH World Federation of Neurological Surgeons scores ranged from 1e5 and Fisher score ranged from 1e4. Mean aneurysm diameter was 5 mm (2e8 mm) (see Table 1). Seven aneurysms had a dissecting-fusiform morphology and were located at the V4 segment of the VA. Two aneurysms were located at the basilar tip. Seven of 9 patients had an external ventricular drain (EVD) due to hydrocephalus before FDD treatment (see Table 1). Two patients eventually underwent ventriculoperitoneal (VP) shunt placement. The procedure was

Study Population We performed a retrospective analysis of our prospectively acquired SAH database that has been maintained since 2009. All consecutive cases of SAH secondary to ruptured posterior circulation dissecting aneurysms treated with FDD between November 2014 and April 2017 at our institution were included in the analysis. All patients were admitted to a surgical neurological intensive care unit after FDD placement. Patient data collection was approved by the Institutional Review Board.

Table 1. Demographic and Angiographic Characteristics Gender

Location

Aneurysm Pre-SAH WFNS Fisher Post Tirofiban Number of Periprocedural Size (mm) mRS Admission Admission SAH Day EVD Aspirin Plavix Infusion FDDs Complications* mRS/Mo

M

Distal Vertebral

5

0

4

3

0

Yes

Yes

Yes

Yes

1

ATH

1/6

F

Distal Vertebral

4

0

5

3

0

Yes

Yes

Yes

Yes

M

Distal Vertebral

8

0

1

3

1

Yes

No

Yes

No

2

ATH

1/2

1

None

0/4

M

Distal Basilar

2

0

1

2

1

No

Yes

Yes

Yes

1

None

0/6

M

Distal Vertebral

8

3

1

2

1

Yes

Yes

M

PICA

3

0

1

3

0

Yes

Yes

Yes

Yes

1

IPH

6/1

Yes

Yes

1

None

1/4

F

PICA

5

0

4

4

0

Yes

Yes

Yes

Yes

1

None

4/3

F

Distal Basilar

7

0

1

1

1

No

Yes

Yes

Yes

1

None

0/3

M

Distal Vertebral

4

0

4

4

1

Yes

Yes

Yes

Yes

1

None

2/11

SAH, subarachnoid hemorrhage; mRS, modified Rankin Scale; WFNS, World Federation of Neurological Surgeons; EVD, extraventricular drain; FDD, flow-diversion device; M, male; ATH, asymptomatic track hemorrhage; IPH, intraparenchymal hemorrhage; F, female; PICA, posterior inferior cerebellar artery; Mo, months. *30-day periprocedural complications.

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ORIGINAL ARTICLE WALDO R. GUERRERO ET AL.

TREATMENT OF RUPTURED VERTEBROBASILAR DISSECTING ANEURYSMS WITH FLOW DIVERSION

done while patients were on aspirin and clopidogrel given the high risk of FDD thrombosis if antiplatelets stopped. At the time of EVD removal we did not change the antiplatelet regimen, and no patients required platelet transfusions. Endovascular Procedure and Adverse Events In all 9 patients, FDD deployment was technically successful. One patient had 2 FDDs placed; otherwise, the remainder underwent treatment with 1 FDD. No intraoperative events (dissection, vasospasm, femoral artery damage and/or hematoma, thrombosis, and contrast extravasation) occurred. None of the aneurysms rebled after the implantation of the FDD. One patient (Case 5) died a few days after endovascular treatment because of complications of an intraparenchymal hemorrhage. This patient initially presented with SAH and underwent emergent EVD placement. Endovascular treatment of a right VA aneurysm with an FDD was uneventful. This patient’s pre-SAH modified Rankin Scale (mRS) score was 3. In addition to dual antiplatelets the patient required full anticoagulation due to severe cardiomyopathy and the need for a left ventricular assist device. Five days after admission and treatment of his aneurysm, the patient deteriorated and a noncontrast computed tomography demonstrated a massive right frontal intraparenchymal hemorrhage with midline shift and herniation. The patient’s family decided to pursue comfort measures and palliative care. Two subjects (Cases 1 and 2) had asymptomatic IPHs along the EVD tract (Figure 1). Both subjects had follow-up mRS of 1. No delayed (up to 12 months after the procedure) morbidity was observed. FOLLOW-UP EVALUATIONS A clinical evaluation was conducted within 1e12 months after the endovascular treatment: mRS 0 ¼ 3, mRS1 ¼ 3, mRS 2 ¼ 1, mRS 4 ¼ 1, and mRS 6 ¼ 1 (see Table 1). A follow-up diagnostic cerebral angiogram (DSA) was available in 5 of the 8 surviving patients (cases 3, 4, 6, 7, and 9). Angiographic follow-up in these patients demonstrated no residual aneurysm, recurrence, or in-stent stenosis (Figure 2). One patient (case 6) who was treated with an FDD deployed in the PICA had an asymptomatic occlusion of the VA just distal to the FDD and the treated PICA was patent (Figure 3). DISCUSSION This small single-center case series describes the treatment of ruptured vertebrobasilar dissecting aneurysms with FDDs. The treatment of these aneurysms was feasible and may be a promising alternative to arterial sacrifice or complex reconstructive endovascular techniques. Furthermore, our series suggests that using our acute antiplatelet protocol might be feasible in the setting of acute SAH and in patients with recently placed EVDs. Dissecting-fusiform aneurysms are associated with a high risk of rebleeding and are challenging to treat.11 Open surgical approaches carry a high risk of morbidity and mortality, mainly due to the friability and fragility of the parent vessel wall, which increases the risk of intraoperative rupture. Moreover, the fusiform morphology and lack of a defined neck renders surgical clipping difficult.12,13 The endovascular treatment of

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dissecting aneurysms involving the vertebrobasilar circulation has been mainly limited to deconstructive techniques such as proximal VA occlusion and parent vessel sacrifice.6 However, the primary disadvantage of endovascular trapping is the risk of ischemic stroke when the aneurysm involves a dominant VA, especially if the contralateral VA is hypoplastic or the posterior communicating arteries are absent.14 Patients are also at risk for brainstem and spinal cord infarcts secondary to occlusion of lateral medullary perforating arteries.15 Thus preservation of the parent vessel is of utmost importance. Dabus et al7 described reconstructive techniques in the treatment of fusiform intracranial VA aneurysms. Two of the 9 patient included in the analysis presented with SAH. Although the reported technical outcome was excellent, 6 of the 9 patients required more than 1 stent to achieve some degree of flow diversion and vessel wall remodeling. FDDs could represent a potential alternative in treating ruptured fusiformedissecting aneurysms of the posterior circulation. However, it is not clear if FDDs are the best option for these aneurysms given the high rate of early rehemorrhage that has been described with this type of aneurysm. FDDs cause gradual aneurysm thrombosis and delayed remodeling of the diseased parent artery and may not “secure” the aneurysm immediately after deployment. Furthermore, the use of FDDs in the posterior circulation is questioned by reports of early rupture and occlusion of perforators.16,17 Finally, the need for acute administration of antiplatelet agents could increase the rate of complications such as EVD tract hemorrhage and aneurysmal rebleeding. Several case series have described the use of FDD in the treatment of acute aneurysmal SAH; however, the experience in treating ruptured vertebrobasilar dissecting aneurysms is limited.8,10,18 Lin et al9 reported 4 patients with ruptured vertebrobasilar aneurysms treated with FDDs. FDD deployment was successful in all cases. However, 1 of these 4 patients developed diffuse brainstem ischemia on the same day of uneventful FDD placement for treatment of a fusiform basilar trunk aneurysm. In our series there were no intraoperative complications directly related to the FDD implant and no patient rebled. In addition, 7 of the 9 patients achieved mRS of 0e2 on follow-up. One patient achieved an mRS of 4, and only 1 patient died due to the concomitant use of full anticoagulation and dual antiplatelets. However, our series did not include large fusiform aneurysms involving the basilar artery, which usually have a “malignant” behavior after flow diversion. The optimal antiplatelet regimen for FDDs in the acute phase of SAH has yet to be determined. The use of dual antiplatelet regimens in patients with acute SAH is cumbersome due to the risk of aneurysmal rebleeding and the need for other neurosurgical procedures such as placement of EVDs and VP shunts. Moreover, these patients often require procedures such as gastrostomy, tracheostomy, and decompressive craniectomy during their acute hospitalization. Chan et al10 published a series of 8 patients with ruptured vertebrobasilar dissecting aneurysms treated with FDDs who received intraprocedural systemic heparinization and a loading dose of aspirin 320 mg and clopidogrel 300 mg via nasogastric tube just before deployment of FDD. Interestingly, in this study patients received only 1 antiplatelet agent

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ORIGINAL ARTICLE WALDO R. GUERRERO ET AL.

TREATMENT OF RUPTURED VERTEBROBASILAR DISSECTING ANEURYSMS WITH FLOW DIVERSION

Figure 1. Noncontrast head computed tomography demonstrating asymptomatic intraparenchymal

(aspirin or clopidogrel) for 3e6 months after treatment. The effectiveness of aspirin or clopidogrel was measured with the VerifyNow test (Accumetrics). Two patients experienced symptomatic complications. There were no procedure-related thrombotic or rebleeding events.10

Figure 2. A 66-year-old man presented with a subarachnoid hemorrhage Fisher IV. (A) Digital subtraction angiography (DSA) demonstrated a dissecting fusiform left vertebral artery aneurysm (arrow) next to the posterior inferior cerebellar artery origin. (B) Follow-up DSA 10 days after placement of

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hemorrhages (arrows) along the extraventricular drain tract in cases 1 (A) and 2 (B).

In our case series, we used our recently published protocol for anticoagulation with tirofiban during flow diversion.19 Eight of the 9 patients were maintained on a tirofiban infusion for 2e6 hours after the procedure. Furthermore, patients were loaded with aspirin 325 mg and clopidogrel 600 mg immediately after FDD

the flow-diversion device demonstrates early vessel-wall remodeling (arrow). (C) 14-month follow-up DSA demonstrating reconstruction of the diseased vertebral artery with no evidence of aneurysmal remnant.

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2017.09.125

ORIGINAL ARTICLE WALDO R. GUERRERO ET AL.

TREATMENT OF RUPTURED VERTEBROBASILAR DISSECTING ANEURYSMS WITH FLOW DIVERSION

Figure 3. (A) Digital subtraction angiography (DSA) demonstrating a dissecting-fusiform aneurysm (arrow) at the proximal left posterior inferior cerebellar artery (PICA). (B) Unsubtracted digital angiography demonstrating placement of a flow-diversion device in

placement. Two subjects developed asymptomatic IPHs along the EVD track (see Figure 1). The mRS score for both patients at follow-up was 1. In another case series of 12 patients who underwent VP shunting after SAC of ruptured aneurysms, 4 patients who were on dual antiplatelets suffered an intracranial hemorrhage related to the VP shunt procedure.20 Three hemorrhages were asymptomatic and occurred along the tract of the ventricular catheter. Only 1 hemorrhage was clinically significant requiring shunt revision. DSA follow-up evaluation was performed in 5 of the 8 survivors. Long-term angiographic follow-up demonstrated no residual aneurysm, recurrence, or in-stent stenosis (see Figure 2). Only 1 patient had an asymptomatic parent artery occlusion of the VA just distal to the PICA due to protrusion of the proximal end of the FDD into the VA (see Figure 1). In our series, 2 patients had a repeat DSA within the first 10 days of initial FDD treatment. In 1 case the aneurysm decreased in size, and in the other case the aneurysm was occluded. Given the early rebleeding rate of ruptured dissecting aneurysms, we recommend a follow-up angiogram within the first few days post the initial FDD treatment to ensure that the dissecting aneurysm is stable and has not changed in morphology.

REFERENCES 1. Mizutani T, Aruga T, Kirino T, Miki Y, Saito I, Tsuchida T. Recurrent subarachnoid hemorrhage from untreated ruptured vertebrobasilar dissecting aneurysms. Neurosurgery. 1995;36:905-911.

2. Ramgren B, Cronqvist M, Romner B, Brandt L, Holtas S, Larsson EM. Vertebrobasilar dissection with subarachnoid hemorrhage: a retrospective study of 29 patients. Neuroradiology. 2005;47: 97-104.

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the left PICA (arrow). (C) Follow-up DSA after 8 months shows interval thrombosis of the left PICA aneurysm with patent FDD. Note distal occlusion (arrow) of the vertebral artery.

This small case series reflects our experience in treating posterior circulation dissecting aneurysms with FDDs. Despite the high periprocedural hemorrhagic risk (3/9 IPHs: 2 asymptomatic) of patients on dual antiplatelets with EVD placement, these patients still achieved an excellent clinical outcome. This is in line with our previous experience with the placement of VP shunts in patients who underwent SAC of ruptured aneurysms. Asymptomatic hemorrhagic complications occurred in 33% of SAH patients.20 This is a small and self-reported case series with only 9 patients. These limitations may affect the low rate of procedural complications. Moreover, the antiplatelet regimen after FDD placement was not standardized in the first cases. CONCLUSION An FDD is an alternative in treating ruptured and dissectingfusiform aneurysm of the posterior circulation not amenable to primary coiling, balloon-assisted coiling, and deconstructive techniques. The FDD may be used to “secure” the aneurysm and reconstruct the disease vessel segment. This approach may be even safer in patients who do not require EVD placement and/or other open neurosurgical procedures.

3. Al-khayat H, Al-Khayat H, Beshay J, Manner D, White J. Vertebral artery-posteroinferior cerebellar artery aneurysms: clinical and lower cranial nerve outcomes in 52 patients. Neurosurgery. 2005;56: 2-10. 4. Rabinov JD, Hellinger FR, Morris PP, Ogilvy CS, Putman CM. Endovascular management of vertebrobasilar dissecting aneurysms. AJNR Am J Neuroradiol. 2003;24:1421-1428. 5. Steinberg GK, Drake CG, Peerless SJ. Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms. Immediate

results and long-term outcome in 201 patients. J Neurosurg. 1993;79:161-173. 6. Madaelil TP, Wallace AN, Chatterjee AN, Zipfel GJ, Dacey RG Jr, DT Cross 3rd, et al. Endovascular parent vessel sacrifice in ruptured dissecting vertebral and posterior inferior cerebellar artery aneurysms: clinical outcomes and review of the literature. J Neurointerv Surg. 2016;8: 796-801. 7. Dabus G, Lin E, Linfante I. Endovascular treatment of fusiform intracranial vertebral artery

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14. Sugiu K, Tokunaga K, Watanabe K, Sasahara W, Ono S, Tamiya T, et al. Emergent endovascular treatment of ruptured vertebral artery dissecting aneurysms. Neuroradiology. 2005;47:158-164. 15. Martin PJ. Vertebrobasilar ischaemia. QJM. 1998; 91:799-811. 16. Fox B, Humphries WE, Doss VT, Hoit D, Elijovich L, Arthur AS. Rupture of giant vertebrobasilar aneurysm following flow diversion: mechanical stretch as a potential mechanism for early aneurysm rupture. BMJ Case Reports. 2014; 2014. 17. McTaggart RA, Santarelli JG, Marcellus ML, Steinberg GK, Dodd RL, Do HM, et al. Delayed retraction of the pipeline embolization device and corking failure: pitfalls of pipeline embolization device placement in the setting of a ruptured aneurysm. Oper Neurosurg. 2013;72(suppl 2): onsE245-onsE251.

12. Le Feuvre DE, Taylor AG. The management of very small/blister internal carotid artery aneurysms. Interv Neuroradiol. 2011;17:431-434.

18. Yoon JW, Siddiqui AH, Dumont TM, Levy EI, Hopkins LN, Lanzino G, et al. Feasibility and safety of pipeline embolization device in patients with ruptured carotid blister aneurysms. Neurosurgery. 2014;75:419-429.

13. McLaughlin N, Laroche M, Bojanowski MW. Surgical management of blood blister-like aneurysms of the internal carotid artery. World Neurosurg. 2010; 74:483-493.

19. Chalouhi N, Jabbour P, Daou B, Starke RM, Shields B, Hasan DM. A new protocol for anticoagulation with tirofiban during flow diversion. Neurosurgery. 2016;78:670-674.

20. Mahaney KB, Chalouhi N, Viljoen S, Smietana J, Kung DK, Jabbour P, et al. Risk of hemorrhagic complication associated with ventriculoperitoneal shunt placement in aneurysmal subarachnoid hemorrhage patients on dual antiplatelet therapy. J Neurosurg. 2013;119: 937-942.

Conflict of interest statement: We confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. We have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. We have followed the regulations of our institutions concerning intellectual property. Received 26 June 2017; accepted 19 September 2017 Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.09.125 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com

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1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2017.09.125