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Michael M. McDowell and Andrew F. Ducruet

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Alfred P. See, Bruno C. Flores, Karam Moon, Andrew F. Ducruet, Robert F. Spetzler and Felipe C. Albuquerque

Supratentorial arteriovenous malformations in eloquent territories can be difficult to resect. This video presents the treatment of a patient with a symptomatic 3-cm arteriovenous malformation in the left motor strip. At the authors’ institution, per the surgeon’s discretion, preoperative angiography is performed to evaluate the need for preoperative embolization. Multimodality treatment reduced the microsurgical risk by allowing early occlusion of a draining vein, by decreasing overall intraoperative hemorrhage, and by allowing minimal pial dissection in the deep aspect of the arteriovenous malformation that abutted the corticospinal tract. The choice of embolysate was an additional nuance of the embolization.

The video can be found here: https://youtu.be/HWZ0RjgPEXg.

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Xiaoran Zhang, William J. Ares, Philipp Taussky, Andrew F. Ducruet and Ramesh Grandhi

Intracranial aneurysms (IAs) are a result of complex interactions between biochemical and mechanical forces and can lead to significant morbidity if they rupture and cause subarachnoid hemorrhage. This review explores the role of matrix metalloproteinases (MMPs) in the pathogenesis and progression of IAs. In addition to providing a review of the normal function of MMPs, it is intended to explore the interaction between inflammation and abnormal blood flow and the resultant pathological vascular remodeling processes seen in the development and rupture of IAs. Also reviewed is the potential for the use of MMPs as a diagnostic tool for assessment of aneurysm development and progression.

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Karam Moon, Felipe C. Albuquerque, Andrew F. Ducruet, R. Webster Crowley and Cameron G. McDougall

Object

Intracranial aneurysms, especially those of the cavernous segment of the internal carotid artery (ICA), can present with cranial nerve (CN) palsies. The Pipeline Embolization Device (PED) has demonstrated safety and efficacy in the treatment of cerebral aneurysms by flow diversion, but little data exist reporting the outcomes of cranial neuropathies following treatment with the device.

Methods

The prospectively maintained Barrow Neurological Institute's endovascular database was reviewed for all patients treated with the PED after presenting with one or more CN palsies secondary to a cerebral aneurysm since May 2011. Patient charts and digital subtraction angiograms were reviewed to report clinical and angiographic outcomes. Only patients with clinical follow-up were included in the analysis.

Results

A total of 127 patients were treated with the PED at the authors' institution after FDA approval. Twentytwo patients presented with cranial neuropathies, for initial inclusion in this study. Of these, 20 had sufficient followup for analysis. Cranial neuropathies included those of CN II, III, V, and VI, with presenting symptoms of diplopia, decreased visual acuity, and facial numbness and/or pain. Thirteen lesions were cavernous segment ICA aneurysms, whereas the remainder included supraclinoid and petrous segment ICA, posterior communicating artery, and basilar trunk aneurysms. At an average clinical follow-up of 9.55 months, 15 patients (75%) had resolution or significant improvement of their cranial neuropathies, and the remaining 5 had stable symptoms. Of the 18 patients with angiographic follow-up, 12 (66.7%) demonstrated complete obliteration or small neck residual, whereas 6 (33.3%) had residual lesion. Patients with complete or near-complete obliteration of their lesion were significantly more likely to demonstrate symptomatic improvement at follow-up (p = 0.009). Two patients with persistent symptoms were eventually treated with microsurgical bypass. Transient complications in this series included 6 (30%) extracranial hemorrhagic complications related to dual-antiplatelet therapy, all of which were managed medically. There was 1 delayed right ICA occlusion following retreatment that led to microsurgical bypass.

Conclusions

Intracranial aneurysms presenting with one or more CN palsies show a high rate of clinical improvement after treatment with the PED. Clinical outcomes must be weighed against the risks and challenges faced with flow diverters. Further research is warranted for patients whose symptoms do not respond optimally to device placement.

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Andrew F. Ducruet, Christopher P. Kellner, E. Sander Connolly Jr. and Philip M. Meyers

Developmental venous anomalies (DVAs) represent a rare cause of intraparenchymal hemorrhage. This case demonstrates an unusual DVA associated with venous hypertension, arteriovenous shunting, and a ruptured transitional aneurysm. The authors describe the first use of embolization as a treatment method for an unstable ruptured transitional aneurysm associated with a DVA. This 33-year-old man suffered acute onset of headache, gait ataxia, and left hemiparesis. Computed tomography brain scans demonstrated a deep paramedian right frontal intraparenchymal hemorrhage. No cavernous malformation was apparent on MR imaging. Diagnostic angiography revealed arteriovenous shunting from the right anterior and middle cerebral arteries to a large DVA with an associated arteriovenous fistula, with a 3-mm aneurysm in the transition from pericallosal artery to the collecting vein. Both surgical and endovascular treatment options were considered. The patient underwent repeat angiography on hospital Day 7, at which time the aneurysm had increased to 5 mm, and endovascular treatment was selected. Acrylic occlusion of the aneurysm was performed and confirmed angiographically. The patient's neurological symptoms resolved throughout the hospital stay, and he remains symptom free in the 10 months since treatment. Developmental venous anomalies are not usually associated with arteriovenous shunting and aneurysms as a source of intraparenchymal hemorrhage. Endovascular occlusion of the aneurysm without blockage of physiologically necessary venous structures is a possible method of treatment for this complex mixed vascular lesion, and has proven safe and effective in this patient. To the authors' knowledge, this is the first presentation of this situation in the literature.

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Adib A. Abla, Andrew F. Ducruet, Robert F. Spetzler, R. Webster Crowley, Cameron G. McDougall and Felipe C. Albuquerque

The authors report the case of a 7-year-old boy with headaches, in whom CT angiography showed multiple intracranial aneurysms from the terminus region of the right internal carotid artery through the proximal right middle cerebral artery (MCA). Initially, the patient underwent clip reconstruction of the M1 segment. Multiple microsurgical and endovascular treatments were required because the largest of these aneurysms recurred several times over the next 1.5 years. The first recurrence was treated with stent coiling and the second by microsurgical occlusion of the MCA combined with the use of a radial artery graft in a common carotid artery–to-MCA bypass. The aneurysm again recurred and was treated by proximal coil occlusion 15 months after the first treatment session. At a 7.5-year follow-up examination, the aneurysms remained occluded. This case highlights the benefit of combined endovascular and microsurgical techniques in the treatment of a complex and unusual case of proximal MCA aneurysmal disease. The patient, now 15 years old, is neurologically intact and able to participate in all activities.

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Bruno C. Flores, Alfred P. See, Gregory M. Weiner, Brian T. Jankowitz, Andrew F. Ducruet and Felipe C. Albuquerque

OBJECTIVE

Liquid embolic agents have revolutionized endovascular management of arteriovenous malformations (AVMs) and arteriovenous fistulas (AVFs). Nonetheless, since 2005, the US FDA has received more than 100 reports of microcatheter breakage or entrapment related to Onyx embolization, including 9 deaths. In 2014, the Apollo detachable-tip microcatheter became the first of its kind available in the US. Since then, few reports on its safety have been published.

METHODS

The authors conducted a retrospective review of endovascular cases by searching the patient databases at 2 tertiary cerebrovascular centers (Barrow Neurological Institute and University of Pittsburgh Medical Center). Patients who underwent endovascular embolization of an AVM or AVF using the Apollo microcatheter were identified. Patient demographics and lesion characteristics were collected. The authors analyzed Apollo-specific endovascular variables, such as number of microcatheterizations, sessions, and pedicles embolized; microcatheter tip detachment status; obliteration rate; and endovascular- and microcatheter-related morbidity and mortality.

RESULTS

From July 2014 to October 2016, a total of 177 embolizations using the Apollo microcatheter were performed in 61 patients (mean age 40.3 years). The most frequent presentation was hemorrhage (22/61, 36.1%). Most lesions were AVMs (51/61, 83.6%; mean diameter 30.6 mm). The mean Spetzler-Martin grade was 2.4. Thirty-nine (76.5%) of 51 patients with AVMs underwent resection. Microcatheterization was successful in 172 pedicles. Most patients (50/61, 82%) underwent a single embolization session. The mean number of pedicles per session was 2.5 (range 1–7). Onyx-18 was used in 103 (59.9%), N-butyl cyanoacrylate (NBCA) in 44 (25.6%), and Onyx-34 in 25 (14.5%) of the 172 embolizations. In 45.9% (28/61) of the patients, lesion obliteration of 75% or greater was achieved. Tip detachment occurred in 19.2% (33/172) of microcatheters. Fifty-three (86.9%) of the 61 patients who underwent embolization with the Apollo microcatheter had good functional outcomes (modified Rankin Scale score 0–2). No unintended microcatheter fractures or related morbidity was observed. One patient died of intraprocedural complications unrelated to microcatheter selection. In the univariate analysis, microcatheter tip detachment (p = 0.12), single embolized pedicles (p = 0.12), and smaller AVM nidus diameter (p = 0.17) correlated positively with high obliteration rates (> 90%). In the multivariate analysis, microcatheter tip detachment was the only independent variable associated with high obliteration rates (OR 9.5; p = 0.03).

CONCLUSIONS

The use of the Apollo detachable-tip microcatheter for embolization of AVMs and AVFs is associated with high rates of successful catheterization and obliteration and low rates of morbidity and mortality. The microcatheter was retrieved in all cases, even after prolonged injections in distal branch pedicles, often with significant reflux. This study represents the largest case series on the application of the Apollo microcatheter for neurointerventional procedures.

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Michael M. McDowell, Yin Zhao, Christopher P. Kellner, Sunjay M. Barton, Eric Sussman, Jan Claassen, Andrew F. Ducruet and E. Sander Connolly

OBJECTIVE

Pathophysiological differences that underlie the development and subsequent growth of multiple aneurysms may exist. In this study, the authors assessed the factors associated with the occurrence of multiple aneurysms in patients presenting with aneurysmal subarachnoid hemorrhage (SAH).

METHODS

Consecutive patients presenting with aneurysmal SAH between 1996 and 2012 were prospectively enrolled in the Subarachnoid Hemorrhage Outcome Project. Patients harboring 1, 2, or 3 or more aneurysms were stratified into groups, and the clinical and radiological characteristics of each group were compared using multivariate logistic regression.

RESULTS

Of 1277 patients with ruptured intracranial aneurysms, 890 had 1 aneurysm, 267 had 2 aneurysms, and 120 had 3 or more aneurysms. On multinomial regression using the single-aneurysm cohort as base case, risk factors for patients presenting with 2 aneurysms were female sex (relative risk ratio [RRR] 1.80, p < 0.001), higher body mass index (BMI) (RRR 1.02, p = 0.003), more years of smoking (RRR = 1.01, p = 0.004), and black race (RRR 1.83, p = 0.001). The risk factors for patients presenting with 3 or more aneurysms were female sex (RRR 3.10, p < 0.001), higher BMI (RRR 1.03, p < 0.001), aneurysm in the posterior circulation (RRR 2.59, p < 0.001), and black race (RRR 2.15, p = 0.001). Female sex, longer smoking history, aneurysms in the posterior circulation, BMI, and black race were independently associated with the development of multiple aneurysms in our adjusted multivariate multinomial model.

CONCLUSIONS

Significant demographic and clinical differences are found between patients presenting with single and multiple aneurysms in the setting of aneurysmal SAH. These predictors of multiple aneurysms likely reflect a predisposition toward inflammation and endothelial injury.

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Bartosz T. Grobelny, Andrew F. Ducruet, Brad E. Zacharia, Zachary L. Hickman, Kristen N. Andersen, Eric Sussman, Austin Carpenter and E. Sander Connolly Jr.

Object

Despite the prevalence of chronic subdural hematoma (CSDHs) in the rapidly growing elderly population, several aspects of disease management remain unclear. In particular, there is still conflicting evidence regarding the efficacy of antiepileptic drug (AED) prophylaxis in patients with CSDH who undergo bur hole drainage. The authors endeavored to evaluate the efficacy of AED prophylaxis in reducing the incidence of seizures and improving outcome in this patient population.

Methods

A single surgeon's clinical database (E.S.C.) was analyzed for cases involving bur hole drainage for CSDH. Cases involving nonhemorrhagic subdural effusions as well as acute subdural hemorrhages evacuated by craniotomy were excluded from this study. Patient medical records were evaluated for relevant demographic data, medical history, imaging characteristics, clinical details of the treatment, hospital stay, and discharge summaries.

Results

The authors included 88 patients with bur hole–treated CSDH. Eleven patients (12.5%) suffered at least 1 seizure between hemorrhage onset and discharge from their treatment hospital admission. Seizures were more frequent in women than men (p = 0.030) and least frequent in patients with right-sided lesions (p = 0.030). In a multiple logistic regression model, preoperative initiation of AED prophylaxis was the only significant predictor of the lower incidence of postoperative seizures (OR 0.10, p = 0.013). However, preoperative initiation of AED prophylaxis did not significantly affect outcome at discharge.

Conclusions

The finding in this study demonstrates that preoperative AED prophylaxis likely reduces the incidence of postoperative seizures in patients with CSDH treated with bur hole drainage. A future prospective randomized study is necessary to evaluate the effect of seizure reduction on clinical outcome.

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R. Webster Crowley, Andrew F. Ducruet, M. Yashar S. Kalani, Louis J. Kim, Felipe C. Albuquerque and Cameron G. McDougall

OBJECT

The widespread implementation of the embolic agent Onyx has changed the endovascular management of cerebral arteriovenous malformations (AVMs). Recent data suggest that outcomes following embolization and resection may have worsened in the Onyx era. It has been hypothesized that there may be increased complications with Onyx embolization and increased surgical aggressiveness in patients treated with Onyx. In this study the authors analyzed their institutional experience with the endovascular treatment of cerebral AVMs prior to and after the introduction of Onyx to determine factors associated with periprocedural neurological morbidity and mortality.

METHODS

A retrospective review was performed of all patients with cerebral AVMs undergoing embolization at the Barrow Neurological Institute from 1995 to 2012.

RESULTS

Endovascular treatment of 342 cerebral AVMs was performed over 446 treatment sessions (mean age 37.8 years, range 1–83 years). Clinical presentation included hemorrhage in 47.6%, seizures in 21.9%, headaches in 11.1%, and no symptoms in 10% of cases. The endovascular pretreatment strategy was preoperative in 78.9%, preradiosurgery in 9.1%, palliative in 5.3%, targeted in 4.4%, and curative in 2.3%. The median Spetzler-Martin grade was III. The mean number of arteries embolized was 3.5 (range 0–13 arteries), and the mean number of treatment sessions was 1.3 (range 1–4 sessions). Onyx was used in 105 AVMs (30.7%), and N-butyl cyanoacrylate (NBCA) without Onyx was used in 229 AVMs (67%). AVMs treated with Onyx had a higher mean number of arterial pedicles embolized than did NBCA cases (4.3 ± 2.7 vs 3.2 ± 2.4, respectively; p < 0.001) and a greater number of sessions (1.5 ± 0.7 vs 1.2 ± 0.5, respectively; p < 0.05). Unexpected immediate postprocedural permanent neurological deficits were present in 9.6% of AVMs, while transient deficits were present in 1.8%. There was 1 death (0.3%). Spetzler-Martin grade was not associated with differences in outcome, as permanent neurological deficits were observed in 12%, 9%, 13%, 11%, and 13% of AVMs for Spetzler-Martin Grades I–V, respectively (p = 0.91). The use of Onyx compared with NBCA was not associated with differences in periprocedural morbidity (p = 0.23). This lack of a difference persisted even when controlling for number of arteries and sessions (p = 0.14). Sex was not associated with differences in outcome.

CONCLUSIONS

Permanent and transient postprocedural neurological deficits were noted in 9.6% and 1.8% of all cases, respectively. AVM grade was not associated with endovascular outcome. Despite the greater number of sessions required and arteries embolized for Onyx cases, there was no statistically significant difference in the risk of neurological deficits following cerebral AVM embolization with Onyx and NBCA.