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Cover Journal of Neurosurgery

Letter to the Editor: “Cured” intracranial dural arteriovenous fistulas

Michael M. McDowell and Andrew F. Ducruet

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Cover Journal of Neurosurgery: Pediatrics

High-flow bypass and tandem microsurgical-endovascular occlusion of recurrent proximal middle cerebral artery aneurysms in a pediatric patient

Case report

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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Cover Neurosurgical Focus

Motor cortex arteriovenous malformation

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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Cover Journal of Neurosurgery: Pediatrics

Spinal arteriovenous malformation associated with Schimmelpenning syndrome

Case report

Kaith K. Almefty, Andrew F. Ducruet, R. Webster Crowley, Ruth Bristol, Sean D. Lavine, and Felipe C. Albuquerque

The authors report the presentation and management of a 13-year-old girl with Schimmelpenning syndrome, a rare neurocutaneous syndrome; this patient suffered hemorrhage of a spinal arteriovenous malformation. This is the first case of a spinal arteriovenous malformation reported in association with Schimmelpenning syndrome. Neurosurgeons should be aware of this rare phacomatosis as well as of the various neurological disorders associated with this diagnosis. The threshold for imaging the neuraxis in these patients should be low.

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Cover Journal of Neurosurgery: Pediatrics

Complex dural arteriovenous fistula in Bannayan-Riley-Ruvalcaba syndrome

Case report

Karam Moon, Andrew F. Ducruet, R. Webster Crowley, Kathleen Klas, Ruth Bristol, and Felipe C. Albuquerque

In this paper the authors report the case of a complex dural arteriovenous fistula (dAVF) with high-risk features in a 14-year-old girl with Bannayan-Riley-Ruvalcaba syndrome (BRRS), a phosphatase and tensin homolog–associated syndrome, presenting with signs and symptoms of increased intracranial pressure (ICP) that had previously been attributed to pseudotumor cerebri. This fistula was obliterated following 2 stages of embolization, and the patient experienced immediate symptomatic improvement. At the 2-month follow-up evaluation, the fistula remained angiographically occluded, and her symptoms continue to improve. This is the third reported case of an intracranial dAVF in a patient with BRRS. Because high-risk dAVFs can result in devastating morbidity, early detection with vascular imaging is crucial for patients with BRRS presenting with signs of increased ICP. Goals of treatment should include complete fistula obliteration whenever possible.

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Cover Neurosurgical Focus

Endovascular occlusion of a ruptured transitional aneurysm associated with a developmental venous anomaly

Case report

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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Cover Neurosurgical Focus

Role of matrix metalloproteinases in the pathogenesis of intracranial aneurysms

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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Cover Journal of Neurosurgery

Resolution of cranial neuropathies following treatment of intracranial aneurysms with the Pipeline Embolization Device

Clinical article

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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Cover Journal of Neurosurgery

Use of the Apollo detachable-tip microcatheter for endovascular embolization of arteriovenous malformations and arteriovenous fistulas

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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Cover Journal of Neurosurgery

Preoperative embolization versus no embolization for WHO grade I intracranial meningioma: a retrospective matched cohort study

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.