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Colin J. Przybylowski, Xiaochun Zhao, Jacob F. Baranoski, Leandro Borba Moreira, Sirin Gandhi, Kristina M. Chapple, Kaith K. Almefty, Nader Sanai, Andrew F. Ducruet, Felipe C. Albuquerque, Andrew S. Little and Peter Nakaji

OBJECTIVE

The controversy continues over the clinical utility of preoperative embolization for reducing tumor vascularity of intracranial meningiomas prior to resection. Previous studies comparing embolization and nonembolization patients have not controlled for detailed tumor parameters before assessing outcomes.

METHODS

The authors reviewed the cases of all patients who underwent resection of a WHO grade I intracranial meningioma at their institution from 2008 to 2016. Propensity score matching was used to generate embolization and nonembolization cohorts of 52 patients each, and a retrospective review of clinical and radiological outcomes was performed.

RESULTS

In total, 52 consecutive patients who underwent embolization (mean follow-up 34.8 ± 31.5 months) were compared to 52 patients who did not undergo embolization (mean follow-up 32.8 ± 28.7 months; p = 0.63). Variables controlled for included patient age (p = 0.82), tumor laterality (p > 0.99), tumor location (p > 0.99), tumor diameter (p = 0.07), tumor invasion into a major dural sinus (p > 0.99), and tumor encasement around the internal carotid artery or middle cerebral artery (p > 0.99). The embolization and nonembolization cohorts did not differ in terms of estimated blood loss during surgery (660.4 ± 637.1 ml vs 509.2 ± 422.0 ml; p = 0.17), Simpson grade IV resection (32.7% vs 25.0%; p = 0.39), perioperative procedural complications (26.9% vs 19.2%; p = 0.35), development of permanent new neurological deficits (5.8% vs 7.7%; p = 0.70), or favorable modified Rankin Scale (mRS) score (a score of 0–2) at last follow-up (96.0% vs 92.3%; p = 0.43), respectively. When comparing the final mRS score to the preoperative mRS score, patients in the embolization group were more likely than patients in the nonembolization group to have an improvement in mRS score (50.0% vs 28.8%; p = 0.03).

CONCLUSIONS

After controlling for patient age, tumor size, tumor laterality, tumor location, tumor invasion into a major dural sinus, and tumor encasement of the internal carotid artery or middle cerebral artery, preoperative meningioma embolization intended to decrease tumor vascularity did not improve the surgical outcomes of patients with WHO grade I intracranial meningiomas, but it did lead to a greater chance of clinical improvement compared to patients not treated with embolization.

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Gregory J. Zipfel, David M. Hasan, Felipe C. Albuquerque and Adam S. Arthur

Over the past decade substantial advances in diagnostic imaging, classification, and understanding the natural history of intracranial dural arteriovenous fistula (dAVF) have been made. Paralleling these improvements in patient evaluation and risk assessment have been considerable innovations and refinements in the microsurgical and endovascular techniques by which appropriately selected patients with dAVF are treated. On the microsurgical front, minimally invasive surgical approaches with less soft tissue and bony disruption, along with enhanced tools for the intraoperative assessment of vascular anatomy and completeness of dAVF obliteration, are now commonly utilized. On the endovascular front, liquid embolic agents, balloons, and flow-directed catheters have transformed our capacity to safely and effectively treat dAVFs with a variety of anatomic configurations and locations. Innovative combinations of microsurgical and endovascular approaches are even being applied to select cases. In this issue of Neurosurgical Focus, we present a series of narrated videos that demonstrate the decision-making, vascular anatomy, and technical nuances of many of these advanced techniques, while also providing narrated videos demonstrating tried-and-true microsurgical and endovascular approaches that have proven highly effective over the years. We hope this video supplement provides a meaningful update and demonstration of modern microsurgical and endovascular approaches to patients with dAVF and aids all of us in our unending quest to provide even better care for our patients in the future. We thank the authors for their outstanding contributions.

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Robert F. Spetzler, Felipe C. Albuquerque, Joseph M. Zabramski and Peter Nakaji

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Robert F. Spetzler, Cameron G. McDougall, Joseph M. Zabramski, Felipe C. Albuquerque, Nancy K. Hills, Peter Nakaji, John P. Karis and Robert C. Wallace

OBJECTIVE

The authors present the 10-year results of the Barrow Ruptured Aneurysm Trial (BRAT) for saccular aneurysms. The 1-, 3-, and 6-year results of the trial have been previously reported, as have the 6-year results with respect to saccular aneurysms. This final report comparing the safety and efficacy of clipping versus coiling is limited to an analysis of those patients presenting with subarachnoid hemorrhage (SAH) from a ruptured saccular aneurysm.

METHODS

In the study, 362 patients had saccular aneurysms and were randomized equally to the clipping and the coiling cohorts (181 each). The primary outcome analysis was based on the assigned treatment group; poor outcome was defined as a modified Rankin Scale (mRS) score > 2 and was independently adjudicated. The extent of aneurysm obliteration was adjudicated by a nontreating neuroradiologist.

RESULTS

There was no statistically significant difference in poor outcome (mRS score > 2) or deaths between these 2 treatment arms during the 10 years of follow-up. Of 178 clip-assigned patients with saccular aneurysms, 1 (< 1%) was crossed over to coiling, and 64 (36%) of the 178 coil-assigned patients were crossed over to clipping. After the initial hospitalization, 2 of 241 (0.8%) clipped saccular aneurysms and 23 of 115 (20%) coiled saccular aneurysms required retreatment (p < 0.001). At the 10-year follow-up, 93% (50/54) of the clipped aneurysms were completely obliterated, compared with only 22% (5/23) of the coiled aneurysms (p < 0.001). Two patients had documented rebleeding, both died, and both were in the assigned and treated coiled cohort (2/83); no patient in the clipped cohort (0/175) died (p = 0.04). In 1 of these 2 patients, the hemorrhage was not from the target aneurysm but from an incidental basilar artery aneurysm, which was coiled at the same time.

CONCLUSIONS

There was no significant difference in clinical outcomes between the 2 assigned treatment groups as measured by mRS outcomes or deaths. Clinical outcomes in the patients with posterior circulation aneurysms were better in the coiling group at 1 year, but after 1 year this difference was no longer statistically significant. Rates of complete aneurysm obliteration and rates of retreatment favored patients who actually underwent clipping compared with those who underwent coiling.

Clinical trial registration no.: NCT01593267 (clinicaltrials.gov)

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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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Bradley A. Gross, Felipe C. Albuquerque, Cameron G. McDougall, Brian T. Jankowitz, Ashutosh P. Jadhav, Tudor G. Jovin and Rose Du

OBJECTIVE

The rarity of cerebral dural arteriovenous fistulas (dAVFs) has precluded analysis of their natural history across large cohorts. Investigators from a considerable proportion of the few reports that do exist have evaluated heterogeneous groups of untreated and partially treated lesions. In the present study, the authors exclusively evaluated the untreated course of dAVFs across a multi-institutional data set to delineate demographic, angiographic, and natural history data.

METHODS

A multi-institutional database of dAVFs was queried for demographic and angiographic data as well as untreated disease course. After dAVFs were stratified by Djindjian type, annual nonhemorrhagic neurological deficit (NHND) and hemorrhage rates were derived, as were risk factors for each. A multivariable Cox proportional-hazards regression model was used to calculate hazard ratios.

RESULTS

Two hundred ninety-five dAVFs had at least 1 month of untreated follow-up. For 126 Type I dAVFs, there were no episodes of NHND or hemorrhage over 177 lesion-years. Respective annualized NHND and hemorrhage rates were 4.5% and 3.4% for Type II, 6.0% and 4.0% for Type III, and 4.5% and 9.1% for Type IV dAVFs. The respective annualized NHND and hemorrhage rates were 2.3% and 2.9% for asymptomatic Type II–IV dAVFs, 23.1% and 3.3% for dAVFs presenting with NHND, and 0% and 46.2% for lesions presenting with hemorrhage. On multivariate analysis, NHND presentation (HR 11.49, 95% CI 3.19–63) and leptomeningeal venous drainage (HR 5.03, 95% CI 0.42–694) were significant risk factors for NHND; hemorrhagic presentation (HR 17.67, 95% CI 2.99–117) and leptomeningeal venous drainage (HR 10.39, 95% CI 1.11–1384) were significant risk factors for hemorrhage.

CONCLUSIONS

All Type II–IV dAVFs should be considered for treatment. Given the high risk of rebleeding, lesions presenting with NHND and/or hemorrhage should be treated expediently.

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Robert M. Starke, Felipe C. Albuquerque and Michael T. Lawton

It is with great pleasure that we present this Neurosurgical Focus video supplement on supratentorial cerebral arteriovenous malformations (AVMs). We were privileged to view a remarkable number of outstanding videos demonstrating current state-of-the-art management of brain AVMs using endovascular and microsurgical modalities. Careful and critical review was required to narrow down the submitted videos to a workable volume for this supplement, which reflects the excellent work being done at multiple centers with these lesions.

This issue consists of videos that represent modern microsurgical and neuroendovascular techniques for the treatment of supratentorial cerebral AVMs. The videos demonstrate cutting-edge therapies as well as standard ones, which will be valuable to both novice and expert neurointerventionists and neurosurgeons. We are honored to be involved with this project and proud of its content and expert authors. We believe you will enjoy the video content of this supplement and hope that it will raise the collective expertise of our community of AVM surgeons.

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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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Al-Wala Awad, Karam Moon, Nam Yoon, Marcus D. Mazur, M. Yashar S. Kalani, Philipp Taussky, Cameron G. McDougall, Felipe C. Albuquerque and Min S. Park

OBJECTIVE

Flow diversion has proven to be an efficacious means of treating cerebral aneurysms that are refractory to other therapeutic means. Patients with tandem aneurysms treated with flow diversion have been included in larger, previously reported series; however, there are no dedicated reports on using this technique during a single session to treat this unique subset of patients. Therefore, the authors analyzed the outcomes of patients who had undergone single-session flow diversion for the treatment of tandem aneurysms.

METHODS

The authors conducted a retrospective review of flow diversion with the Pipeline embolization device (PED) for the treatment of tandem aneurysms in a single session at 2 participating medical centers: University of Utah, Salt Lake City, Utah, and Barrow Neurological Institute, Phoenix, Arizona. Patient demographic data, aneurysm characteristics, treatment strategy and results, complications, and follow-up data were collected from the medical record and analyzed.

RESULTS

Between January 2011 and December 2015, 17 patients (12 female, 5 male) with a total of 38 aneurysms (mean size 4.7 ± 2.7 mm, mean ± SD) were treated. Sixteen patients had aneurysms in the anterior circulation, and 1 patient had tandem aneurysms in the posterior circulation. Twelve patients underwent only placement of a PED, whereas 5 underwent adjunctive coil embolization of at least 1 aneurysm. One PED was used in each of 9 patients, and 2 PEDs were required in each of 8 patients. There were 2 intraprocedural complications; however, in both instances, the patients were asymptomatic at the last follow-up. The follow-up imaging studies were available for 15 patients at a mean of 7 months after treatment (216 days, range 0–540 days). The mean initial Raymond score after treatment was 2.7 ± 0.7, and the mean final score was 1.3 ± 0.7.

CONCLUSIONS

In this series, the use of flow diversion for the treatment of tandem cerebral aneurysms had an acceptable safety profile, indicating that it should be considered as an effective therapy for this complicated subset of patients. Further prospective studies must be performed before more definitive conclusions can be made.

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David S. Xu, Michael R. Levitt, M. Yashar S. Kalani, Leonardo Rangel-Castilla, Celene B. Mulholland, Isaac J. Abecassis, Ryan P. Morton, John D. Nerva, Adnan H. Siddiqui, Elad I. Levy, Robert F. Spetzler, Felipe C. Albuquerque and Cameron G. McDougall

OBJECTIVE

Fusiform dolichoectatic vertebrobasilar aneurysms are rare, challenging lesions. The natural history of these lesions and medium- and long-term patient outcomes are poorly understood. The authors sought to evaluate patient prognosis after diagnosis of fusiform dolichoectatic vertebrobasilar aneurysms and to identify clinical and radiographic predictors of neurological deterioration.

METHODS

The authors reviewed multiple, prospectively maintained, single-provider databases at 3 large-volume cerebrovascular centers to obtain data on patients with unruptured, fusiform, basilar artery dolichoectatic aneurysms diagnosed between January 1, 2000, and January 1, 2015.

RESULTS

A total of 50 patients (33 men, 17 women) were identified; mean clinical follow-up was 50.1 months and mean radiographic follow-up was 32.4 months. At last follow-up, 42% (n = 21) of aneurysms had progressed and 44% (n = 22) of patients had deterioration of their modified Rankin Scale scores. When patients were dichotomized into 2 groups— those who worsened and those who did not—univariate analysis showed 5 variables to be statistically significantly different: sex (p = 0.007), radiographic brainstem compression (p = 0.03), clinical posterior fossa compression (p < 0.001), aneurysmal growth on subsequent imaging (p = 0.001), and surgical therapy (p = 0.006). A binary logistic regression was then created to evaluate these variables. The only variable found to be a statistically significant predictor of clinical worsening was clinical symptoms of posterior fossa compression at presentation (p = 0.01).

CONCLUSIONS

Fusiform dolichoectatic vertebrobasilar aneurysms carry a poor prognosis, with approximately one-half of the patients deteriorating or experiencing progression of their aneurysm within 5 years. Despite being high risk, intervention—when carefully timed (before neurological decline)—may be beneficial in select patients.