Publications by authors named "Gary K Steinberg"

281 Publications

Surgical treatment of brainstem cavernous malformations: an international Delphi consensus.

J Neurosurg 2021 Oct 1:1-11. Epub 2021 Oct 1.

1Department of Neurosurgery and Spine Surgery, University Hospital Essen, Germany.

Objective: Indication for surgery in brainstem cavernous malformations (BSCMs) is based on many case series, few comparative studies, and no randomized controlled trials. The objective of this study was to seek consensus about surgical management aspects of BSCM.

Methods: A total of 29 experts were invited to participate in a multistep Delphi consensus process on the surgical treatment of BSCM.

Results: Twenty-two (76%) of 29 experts participated in the consensus. Qualitative analysis (content analysis) of an initial open-ended question survey resulted in 99 statements regarding surgical treatment of BSCM. By using a multistep survey with 100% participation in each round, consensus was reached on 52 (53%) of 99 statements. These were grouped into 4 categories: 1) definitions and reporting standards (7/14, 50%); 2) general and patient-related aspects (11/16, 69%); 3) anatomical-, timing of surgery-, and BSCM-related aspects (22/37, 59%); and 4) clinical situation-based decision-making (12/32, 38%). Among other things, a consensus was reached for surgical timing, handling of associated developmental venous anomalies, handling of postoperative BSCM remnants, assessment of specific anatomical BSCM localizations, and treatment decisions in typical clinical BSCM scenarios.

Conclusions: A summary of typical clinical scenarios and a catalog of various BSCM- and patient-related aspects that influence the surgical treatment decision have been defined, rated, and interpreted.
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http://dx.doi.org/10.3171/2021.3.JNS2156DOI Listing
October 2021

Increased Autoimmunity in Individuals With Down Syndrome and Moyamoya Disease.

Front Neurol 2021 8;12:724969. Epub 2021 Sep 8.

Department of Neurology, Keck School of Medicine at the University of Southern California, Los Angeles, CA, United States.

To determine if elevated rates of autoimmune disease are present in children with both Down syndrome and moyamoya disease given the high rates of autoimmune disease reported in both conditions and unknown etiology of angiopathy in this population. A multi-center retrospective case-control study of children with Down syndrome and moyamoya syndrome, idiopathic moyamoya disease, and Down syndrome without cerebrovascular disease was performed. Outcome measures included presence of autoimmune disease, presence of autoantibodies and angiopathy severity data. Comparisons across groups was performed using the Kruskal-Wallis, χ2 and multivariate Poisson regression. The prevalence of autoimmune disease were 57.7, 20.3, and 35.3% in persons with Down syndrome and moyamoya syndrome, idiopathic moyamoya disease, and Down syndrome only groups, respectively ( < 0.001). The prevalence of autoimmune disease among children with Down syndrome and moyamoya syndrome is 3.2 times ( < 0.001, 95% CI: 1.82-5.58) higher than the idiopathic moyamoya group and 1.5 times ( = 0.002, 95% CI: 1.17-1.99) higher than the Down syndrome only group when adjusting for age and sex. The most common autoimmune diseases were thyroid disorders, type I diabetes and Celiac disease. No individuals with idiopathic moyamoya disease had more than one type of autoimmune disorder while 15.4% of individuals with Down syndrome and moyamoya syndrome and 4.8% of individuals with Down syndrome only had >1 disorder ( = 0.05, 95%CI: 1.08-6.08). This study reports elevated rates of autoimmune disease in persons with Down syndrome and moyamoya syndrome providing a nidus for study of the role of autoimmunity in angiopathy in this population.
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http://dx.doi.org/10.3389/fneur.2021.724969DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8455812PMC
September 2021

Introduction. Translational research advances in the evaluation and management of moyamoya disease.

Neurosurg Focus 2021 09;51(3):E1

4Department of Neurosurgery, Huashan Hospital, Shanghai, China.

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http://dx.doi.org/10.3171/2021.6.FOCUS21373DOI Listing
September 2021

Arteriovenous Malformations-Current Understanding of the Pathogenesis with Implications for Treatment.

Int J Mol Sci 2021 Aug 21;22(16). Epub 2021 Aug 21.

Division Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, Stanford University, Stanford, CA 94305, USA.

Arteriovenous malformations are a vascular anomaly typically present at birth, characterized by an abnormal connection between an artery and a vein (bypassing the capillaries). These high flow lesions can vary in size and location. Therapeutic approaches are limited, and AVMs can cause significant morbidity and mortality. Here, we describe our current understanding of the pathogenesis of arteriovenous malformations based on preclinical and clinical findings. We discuss past and present accomplishments and challenges in the field and identify research gaps that need to be filled for the successful development of therapeutic strategies in the future.
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http://dx.doi.org/10.3390/ijms22169037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8396465PMC
August 2021

Age-dependent Intracranial Artery Morphology in Healthy Children.

Clin Neuroradiol 2021 Aug 24. Epub 2021 Aug 24.

Department of Radiology, Faculty of Medicine, University of Calgary, HMRB Building, Room 155, 3330 Hospital Drive NW, AB T2N 4N1, Calgary, Canada.

Purpose: Evaluation of intracranial artery morphology plays an important role in diagnosing a variety of neurovascular diseases. In addition to clinical symptoms, diagnosis currently relies on qualitative rather than quantitative evaluation of vascular imaging sequences, such as magnetic resonance angiography (MRA). However, there is a paucity of literature on normal arterial morphology in the pediatric population across brain development. We aimed to quantitatively assess normal, age-related changes in artery morphology in children.

Methods: We performed retrospective analysis of pediatric MRA data obtained from a tertiary referral center. An MRA dataset from 98 children (49 boys/49 girls) aged 0.6-20 years (median = 11.5 years) with normal intracranial vasculature was retrospectively collected between 2011 and 2018. All arteries were automatically segmented to determine the vessel radius. Using an atlas-based approach, the average radius and density of arteries were measured in the three main cerebral vascular territories and the radius of five major arteries was determined at corresponding locations.

Results: The radii of the major arteries as well as the average artery radius and density in the different vascular territories in the brain remained constant throughout childhood and adolescence (|r| < 0.369 in all cases).

Conclusion: This study presents the first automated evaluation of intracranial vessel morphology on MRA across childhood. Our results can serve as a framework for quantitative evaluation of cerebral vessel morphology in the setting of pediatric neurovascular diseases.
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http://dx.doi.org/10.1007/s00062-021-01071-9DOI Listing
August 2021

A neurovascular-unit-on-a-chip for the evaluation of the restorative potential of stem cell therapies for ischaemic stroke.

Nat Biomed Eng 2021 08 12;5(8):847-863. Epub 2021 Aug 12.

Department of Neurosurgery, Stanford University School of Medicine, Stanford, CA, USA.

The therapeutic efficacy of stem cells transplanted into an ischaemic brain depends primarily on the responses of the neurovascular unit. Here, we report the development and applicability of a functional neurovascular unit on a microfluidic chip as a microphysiological model of ischaemic stroke that recapitulates the function of the blood-brain barrier as well as interactions between therapeutic stem cells and host cells (human brain microvascular endothelial cells, pericytes, astrocytes, microglia and neurons). We used the model to track the infiltration of a number of candidate stem cells and to characterize the expression levels of genes associated with post-stroke pathologies. We observed that each type of stem cell showed unique neurorestorative effects, primarily by supporting endogenous recovery rather than through direct cell replacement, and that the recovery of synaptic activities is correlated with the recovery of the structural and functional integrity of the neurovascular unit rather than with the regeneration of neurons.
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http://dx.doi.org/10.1038/s41551-021-00744-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524779PMC
August 2021

Brain-wide neural dynamics of poststroke recovery induced by optogenetic stimulation.

Sci Adv 2021 Aug 11;7(33). Epub 2021 Aug 11.

Department of Neurosurgery, Stanford University, Stanford, CA, USA.

Poststroke optogenetic stimulations can promote functional recovery. However, the circuit mechanisms underlying recovery remain unclear. Elucidating key neural circuits involved in recovery will be invaluable for translating neuromodulation strategies after stroke. Here, we used optogenetic functional magnetic resonance imaging to map brain-wide neural circuit dynamics after stroke in mice treated with and without optogenetic excitatory neuronal stimulations in the ipsilesional primary motor cortex (iM1). We identified key sensorimotor circuits affected by stroke. iM1 stimulation treatment restored activation of the ipsilesional corticothalamic and corticocortical circuits, and the extent of activation was correlated with functional recovery. Furthermore, stimulated mice exhibited higher expression of axonal growth-associated protein 43 in the ipsilesional thalamus and showed increased Synaptophysin/channelrhodopsin presynaptic axonal terminals in the corticothalamic circuit. Selective stimulation of the corticothalamic circuit was sufficient to improve functional recovery. Together, these findings suggest early involvement of corticothalamic circuit as an important mediator of poststroke recovery.
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http://dx.doi.org/10.1126/sciadv.abd9465DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8357234PMC
August 2021

Stem Cells for Aging-Related Disorders.

Stem Cell Rev Rep 2021 Dec 10;17(6):2054-2058. Epub 2021 Aug 10.

Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine, Stanford, CA, 94305, USA.

This review captures recent advances in biological and translational research on stem cells. In particular, we discuss new discoveries and concepts regarding stem cell treatment of aging-related disorders. A myriad of stem cell sources exists, from hematopoietic to mesenchymal and neural cell lineages. We examine current applications of exogenous adult bone marrow-derived stem cells as an effective and safe transplantable cell source, as well as the use of electrical stimulation to promote endogenous neurogenesis for Parkinson's disease. We also explore the potential of transplanting exogenous umbilical cord blood cells and mobilizing host resident stem cells in vascular dementia and aging. In addition, we assess the ability of small molecules to recruit resident stem cells in Alzheimer's disease. Finally, we evaluate mechanisms of action recently implicated in stem cell therapy, such as the role of long non-coding RNAs, G-protein coupled receptor 5, and NeuroD1. Our goal is to provide a synopsis of recent milestones regarding the application of stem cells in aging.
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http://dx.doi.org/10.1007/s12015-021-10222-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8602738PMC
December 2021

Early Experience With Virtual and Synchronized Augmented Reality Platform for Preoperative Planning and Intraoperative Navigation: A Case Series.

Oper Neurosurg (Hagerstown) 2021 09;21(4):189-196

Department of Neurosurgery, George Washington University Hospital, Washington, District of Columbia, USA.

Background: Virtual reality (VR) allows for presurgical planning. Intraoperatively, augmented reality (AR) enables integration of segmented anatomic information with neuronavigation into the microsurgical scene to provide guidance without workflow disruption. Combining VR and AR solutions may help guide microsurgical technique to improve safety, efficiency, and ergonomics.

Objective: To describe a VR/AR platform that provides VR planning and intraoperative guidance via microscope ocular injection of a comprehensive AR overlay of patient-specific 360°/3D anatomic model aligned and synchronized with neuronavigation.

Methods: Custom 360° models from preoperative imaging of 49 patients were utilized for preoperative planning using a VR-based surgical rehearsal platform. Each model was imported to SyncAR, the platform's intraoperative counterpart, which was coregistered with Medtronic StealthStation S8 and Zeiss or Leica microscope. The model was injected into the microscope oculars and referenced throughout by adjusting overlay opacity. For anatomic shifts or misalignment, the overlay was reregistered via manual realignment with known landmarks.

Results: No SyncAR-related complications occurred. SyncAR contributed positively to the 3D understanding of patient-specific anatomy and ability to operate. Preoperative planning and intraoperative AR with 360° models allowed for more precise craniotomy planning and execution. SyncAR was useful for guiding dissection, identifying critical structures including hidden anatomy, understanding regional anatomy, and facilitating resection. Manual realignment was performed in 48/49 surgeries. Gross total resection was achieved in 34/40 surgeries. All aneurysm clipping and microvascular decompression procedures were completed without complications.

Conclusion: SyncAR combined with VR planning has potential to enhance surgical performance by providing critical information in a user-friendly, continuously available, heads-up display format.
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http://dx.doi.org/10.1093/ons/opab188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8453400PMC
September 2021

Radiosurgery as a microsurgical adjunct: outcomes after microsurgical resection of intracranial arteriovenous malformations previously treated with stereotactic radiosurgery.

J Neurosurg 2021 Jun 11:1-12. Epub 2021 Jun 11.

1Department of Neurosurgery and Stanford Stroke Center, Stanford University Medical Center, Stanford.

Objective: Microsurgical resection of arteriovenous malformations (AVMs) can be aided by staged treatment consisting of stereotactic radiosurgery followed by resection in a delayed fashion. This approach is particularly useful for high Spetzler-Martin (SM) grade lesions because radiosurgery can reduce flow through the AVM, downgrade the SM rating, and induce histopathological changes that additively render the AVM more manageable for resection. The authors present their 28-year experience in managing AVMs with adjunctive radiosurgery followed by resection.

Methods: The authors retrospectively reviewed records of patients treated for cerebral AVMs at their institution between January 1990 and August 2019. All patients who underwent stereotactic radiosurgery (with or without embolization), followed by resection, were included in the study. Of 1245 patients, 95 met the eligibility criteria. Univariate and multivariate regression analyses were performed to assess relationships between key variables and clinical outcomes.

Results: The majority of lesions treated (53.9%) were high grade (SM grade IV-V), 31.5% were intermediate (SM grade III), and 16.6% were low grade (SM grade I-II). Hemorrhage was the initial presenting sign in half of all patients (49.5%). Complete resection was achieved among 84% of patients, whereas 16% had partial resection, the majority of whom received additional radiosurgery. Modified Rankin Scale (mRS) scores of 0-2 were achieved in 79.8% of patients, and 20.2% had poor (mRS scores 3-6) outcomes. Improved (44.8%) or stable (19%) mRS scores were observed among 63.8% of patients, whereas 36.2% had a decline in mRS scores. This includes 22 patients (23.4%) with AVM hemorrhage and 6 deaths (6.7%) outside the perioperative period but prior to AVM obliteration.

Conclusions: Stereotactic radiosurgery is a useful adjunct in the presurgical management of cerebral AVMs. Multimodal therapy allowed for high rates of AVM obliteration and acceptable morbidity rates, despite the predominance of high-grade lesions in this series of patients.
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http://dx.doi.org/10.3171/2020.9.JNS201538DOI Listing
June 2021

Editorial: Stem Cells and Aging.

Front Aging Neurosci 2021 17;13:690613. Epub 2021 May 17.

Department of Neurosurgery, Stanford University, Stanford, CA, United States.

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http://dx.doi.org/10.3389/fnagi.2021.690613DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8165171PMC
May 2021

Cavernous malformations of the hypothalamus: a single-institution series of 12 cases and review of the literature.

J Neurosurg 2021 May 21:1-10. Epub 2021 May 21.

Objective: There remains a paucity of literature on hypothalamic cavernous malformations (HCMs). Here, the authors present the largest series of HCMs to date and review the literature to gain additional insight into this rare disease subset.

Methods: A prospectively managed database was retrospectively reviewed for patients diagnosed with symptomatic HCM and treated surgically between 1987 and 2019. Data gathered included demographics, presenting signs, radiological measurements, surgical approach, and postoperative events. Functional outcome was measured using the modified Rankin Scale (mRS) and Glasgow Outcome Scale-Extended (GOSE) pre- and postoperatively. A PRISMA guideline systematic review of HCM in the literature was performed.

Results: Our cohort study consisted of 12 patients with symptomatic, and radiographically confirmed, HCM treated with microsurgery by the senior author (G.K.S.). An additional 16 surgically or conservatively managed patients were also identified from the literature, and the authors analyzed the data of all 28 patients (with 54% of patients being male; mean age 39 ± 16 years, range 10-68 years). Patients harboring HCMs most commonly presented with headache (16/28, 57%), short-term memory impairment (11/28, 39%), and gait disturbance (8/28, 32%). Radiographically, lesions most commonly involved the mammillary region (18/23, 78%), the tuberal/infundibulum region (13/23, 57%), and the preoptic/lamina terminalis region (12/23, 52%), with a mean diameter of 2.5 ± 1.4 cm (range 0.8-7 cm) at presentation. Acute hemorrhage was identified in 96% (23/24) of patients on presentation, with 96% (23/24) intraparenchymal and 29% (7/24) intraventricular. Of 24 patients who were managed surgically, gross-total resection (GTR) was achieved in 88% (21/24) of cases. There were no reports of perioperative infarction or mortality. With a mean follow-up period of 41 months (range 0.5-309 months), 77% (20/26) of patients experienced functional improvement, while 12% (3/26) had no change, and 12% (3/26) experienced increased disability. In our cohort of 12 patients, 83% (10/12) continued to report symptoms at the last follow-up (mean 4.8 years, range 0.1-25.7 years). However, there was a significant improvement in mRS score noted after surgery (mean 1.4 vs 3.1, p = 0.0026) and a trend toward improvement in GOSE score (mean 6.3 vs 5.1, p = 0.09).

Conclusions: Hemorrhage from HCMs can cause a symptomatic mass effect on adjacent eloquent structures. While patients are unlikely to be deficit free following surgery, GTR allows for functional improvement and reduces recurrent hemorrhage rates. Microsurgery remains a viable option for symptomatic HCMs in experienced hands.
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http://dx.doi.org/10.3171/2020.10.JNS201419DOI Listing
May 2021

Commentary: Direct vs Indirect Revascularization in a North American Cohort of Moyamoya Disease.

Neurosurgery 2021 07;89(2):E114-E115

Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine and Stanford Health Care, Stanford, California, USA.

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http://dx.doi.org/10.1093/neuros/nyab165DOI Listing
July 2021

Establishing a Data Science Unit in an Academic Medical Center: An Illustrative Model.

Acad Med 2021 Mar 23. Epub 2021 Mar 23.

M. Desai is professor of medicine and of biomedical data science, section chief of biostatistics, Division of Biomedical Informatics Research, and director, Quantitative Sciences Unit, Stanford University School of Medicine, Palo Alto, California. M. Boulos is executive director, Quantitative Sciences Unit, Stanford University School of Medicine, Palo Alto, California. G. M. Pomann is statistical research scientist and director, Duke Biostatistics Epidemiology and Research Design Methods Core, Duke University School of Medicine, Durham, North Carolina. G. K. Steinberg is Bernard and Ronni Lacroute - William Randolph Hearst Professor in Neurosurgery and Neurosciences, and chair, Department of Neurosurgery, Stanford University School of Medicine, Stanford, California. F. M. Longo is George E. and Lucy Becker Professor and chair, Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, California. M. Leonard is Arline and Pete Harman Professor and chair, Department of Pediatrics, Stanford University School of Medicine, and Adalyn Jay Physician in Chief, Lucile Packard Children's Hospital Stanford, Stanford, California. T. Montine is Stanford Medicine Endowed Professor in Pathology and chair, Department of Pathology, Stanford University School of Medicine, Stanford, California. A. L. Blomkalns is Stanford Medicine Professor of Emergency Medicine and chair, Department of Emergency Medicine, Stanford University School of Medicine, Stanford, California. R. A. Harrington is Arthur L. Bloomfield Professor of Medicine and chair, Department of Medicine, Stanford University School of Medicine, Stanford, California.

The field of data science has great potential to address critical questions relevant for academic medical centers. Data science initiatives are consequently being established within academic medicine. At the cornerstone of such initiatives are scientists who practice data science. These scientists include biostatisticians, clinical informaticians, database and software developers, computational scientists, and computational biologists. Too often, however, those involved in the practice of data science are viewed by academic leadership as providing a noncomplex service to facilitate research and further the careers of other academic faculty. The authors contend that the success of data science initiatives relies heavily on the understanding that the practice of data science is a critical intellectual contribution to the overall science conducted at an academic medical center. Further, careful thought by academic leadership is needed for allocation of resources devoted to the practice of data science. At the Stanford University School of Medicine, the authors have developed an innovative model for a data science collaboratory based on 4 fundamental elements: an emphasis on collaboration over consultation; a subscription-based funding mechanism that reflects commitment by key partners; an investment in the career development of faculty who practice data science; and a strong educational component for data science members in team science and for clinical and translational investigators in data science. As data science becomes increasingly essential to learning health systems, centers that specialize in the practice of data science are a critical component of the research infrastructure and intellectual environment of academic medical centers.
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http://dx.doi.org/10.1097/ACM.0000000000004079DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8458473PMC
March 2021

Unique Subtype of Microglia in Degenerative Thalamus After Cortical Stroke.

Stroke 2021 01 8;52(2):687-698. Epub 2021 Jan 8.

Department of Neurosurgery (Z.C., S.S.H., T.C., A.G.F., M.Y.C., G.K.S.), Stanford University School of Medicine, CA.

Background And Purpose: Stroke disrupts neuronal functions in both local and remotely connected regions, leading to network-wide deficits that can hinder recovery. The thalamus is particularly affected, with progressive development of neurodegeneration accompanied by inflammatory responses. However, the complexity of the involved inflammatory responses is poorly understood. Herein we investigated the spatiotemporal changes in the secondary degenerative thalamus after cortical stroke, using targeted transcriptome approach in conjunction with histology and flow cytometry.

Methods: Cortical ischemic stroke was generated by permanent occlusion of the left middle cerebral artery in male C57BL6J mice. Neurodegeneration, neuroinflammatory responses, and microglial activation were examined in naive and stroke mice at from poststroke days (PD) 1 to 84, in both ipsilesional somatosensory cortex and ipsilesional thalamus. NanoString neuropathology panel (780 genes) was used to examine transcriptome changes at PD7 and PD28. Fluorescence activated cell sorting was used to collect CD11c microglia from ipsilesional thalamus, and gene expressions were validated by quantitative real-time polymerase chain reaction.

Results: Neurodegeneration in the thalamus was detected at PD7 and progressively worsened by PD28. This was accompanied by rapid microglial activation detected as early as PD1, which preceded the neurodegenerative changes. Transcriptome analysis showed higher number of differentially expressed genes in ipsilesional thalamus at PD28. Notably, neuroinflammation was the top activated pathway, and microglia was the most enriched cell type. (CD11c) was the most significantly increased gene, and its expression was highly detected in microglia. Flow-sorted CD11c microglia from degenerative thalamus indicated molecular signatures similar to neurodegenerative disease-associated microglia; these included downregulated Tmem119 and CX3CR1 and upregulated ApoE, Axl, LpL, CSF1, and Cst7.

Conclusions: Our findings demonstrate the dynamic changes of microglia after stroke and highlight the importance of investigating stroke network-wide deficits. Importantly, we report the existence of a unique subtype of microglia (CD11c) with neurodegenerative disease-associated microglia features in the degenerative thalamus after stroke.
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http://dx.doi.org/10.1161/STROKEAHA.120.032402DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7855924PMC
January 2021

Cell Therapy for Chronic TBI: Interim Analysis of the Randomized Controlled STEMTRA Trial.

Neurology 2021 Jan 4. Epub 2021 Jan 4.

Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Objective: To determine if chronic motor deficits secondary to traumatic brain injury (TBI) can be improved by implantation of allogeneic modified bone marrow-derived mesenchymal stromal/stem cells (SB623).

Methods: This 6-month interim analysis of the 1-year double-blind, randomized, surgical sham-controlled, phase 2 STEMTRA trial (NCT02416492) evaluated safety and efficacy of the stereotactic intracranial implantation of SB623 in patients with stable chronic motor deficits secondary to TBI. Patients in this multi-center trial (N = 63) underwent randomization in a 1:1:1:1 ratio to 2.5 × 10, 5.0 × 10, 10 × 10 SB623 cells or control. Safety was assessed in patients who underwent surgery (N = 61), and efficacy in the modified intent-to-treat population of randomized patients who underwent surgery (N = 61; SB623 = 46, control = 15).

Results: The primary efficacy endpoint of significant improvement from baseline of Fugl-Meyer Motor Scale score at 6 months for SB623-treated patients was achieved. SB623-treated patients improved by (LS mean [SE]) +8.3 (1.4) vs +2.3 (2.5) for control at 6 months, the LS mean difference was 6.0 (95% CI: 0.3-11.8); = 0.040. Secondary efficacy endpoints improved from baseline, but were not statistically significant vs control at 6 months. There were no dose-limiting toxicities or deaths, and 100% of SB623-treated patients experienced treatment-emergent adverse events vs 93.3% of control patients ( = 0.25).

Conclusions: SB623 cell implantation appeared to be safe and well tolerated, and patients implanted with SB623 experienced significant improvement from baseline motor status at 6 months compared to controls.

Classification Of Evidence: This study provides Class I evidence that implantation of SB623 was well tolerated and associated with improvement in motor status.
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http://dx.doi.org/10.1212/WNL.0000000000011450DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8055341PMC
January 2021

Basal ganglia cavernous malformations: case series and systematic review of surgical management and long-term outcomes.

J Neurosurg 2021 Jan 1:1-9. Epub 2021 Jan 1.

1Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine and Stanford Health Center, Stanford.

Objective: Reports on basal ganglia cavernous malformations (BGCMs) are rare. Here, the authors report on their experience in resecting these malformations to offer insight into this infrequent disease subtype.

Methods: The authors retrospectively reviewed a prospectively managed departmental database of all deep-seated cerebral cavernous malformations (CCMs) treated at Stanford between 1987 and 2019 and included for further analysis those with a radiographic diagnosis of BGCM. Moreover, a systematic literature review was undertaken using the PubMed and Web of Science databases.

Results: The departmental database search yielded 331 patients with deep-seated CCMs, 44 of whom had a BGCM (13.3%). Headache was the most common presenting sign (53.5%), followed by seizure (32.6%) and hemiparesis (27.9%). Lesion location involved the caudate nucleus in 21.4% of cases compared to 78.6% of cases within the lentiform nucleus. Caudate BGCMs were larger on presentation and were more likely to present to the ependymal surface (p < 0.001) with intraventricular hemorrhage and hydrocephalus (p = 0.005 and 0.007, respectively). Dizziness and diplopia were also more common with lesions involving the caudate. Because of their anatomical location, caudate BGCMs were preferentially treated via an interhemispheric approach and were less likely to be associated with worsening perioperative deficits than lentiform BGCMs (p = 0.006 and 0.045, respectively). Ten patients (25.6%) were clinically worse in the immediate postoperative period, 4 (10.2%) of whom continued to suffer permanent morbidity at the last follow-up. A long-term good outcome (modified Rankin Scale [mRS] score 0-1) was attained in 74.4% of cases compared to the 69.2% of patients who had presented with an mRS score 0-1. Relative to their presenting mRS score, 89.8% of patients had an improved or unchanged status at the last follow-up. The median postoperative follow-up was 11 months (range 1-252 months). Patient outcomes after resection did not differ among surgical approaches; however, patients presenting with hemiparesis and lesions involving the globus pallidus or posterior limb of the internal capsule were more likely to suffer neurological deficits during the immediate perioperative period. Patients who had undergone awake surgeries were more likely to suffer neurological decline at the early as well as the late follow-up. When adjusting for awake craniotomy as a potential confounder of lesion location, a BGCM involving the posterior limb was predictive of developing early postoperative deficits, but this finding did not persist at the long-term follow-up.

Conclusions: Surgery is a safe and effective treatment modality for managing BGCMs, with an estimated long-term permanent morbidity rate of around 10%.
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http://dx.doi.org/10.3171/2020.7.JNS2098DOI Listing
January 2021

Revisiting Stem Cell-Based Clinical Trials for Ischemic Stroke.

Front Aging Neurosci 2020 14;12:575990. Epub 2020 Dec 14.

Department of Neurosurgery, Stanford University School of Medicine, Stanford, CA, United States.

Stroke is the leading cause of serious long-term disability, significantly reducing mobility in almost half of the affected patients aged 65 years and older. There are currently no proven neurorestorative treatments for chronic stroke. To address the complex problem of restoring function in ischemic brain tissue, stem cell transplantation-based therapies have emerged as potential restorative therapies. Aligning with the major cell types found within the ischemic brain, stem-cell-based clinical trials for ischemic stroke have fallen under three broad cell lineages: hematopoietic, mesenchymal, and neural. In this review article, we will discuss the scientific rationale for transplanting cells from each of these lineages and provide an overview of published and ongoing trials using this framework.
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http://dx.doi.org/10.3389/fnagi.2020.575990DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7767918PMC
December 2020

Staged Surgical Resection of Brain Arteriovenous Malformations.

World Neurosurg 2021 02 16;146:e925-e930. Epub 2020 Nov 16.

Department of Neurosurgery and Stanford Stroke Center, Stanford School of Medicine, Stanford, California, USA. Electronic address:

Background: Staged treatment of brain arteriovenous malformations (AVMs) is sometimes necessary to minimize risks associated with sudden changes in cerebral hemodynamics. With the increasing availability and optimization of endovascular techniques, multiple surgical resections are rarely necessary, although, due to specific anatomic circumstances, some AVMs still require staged surgery. Here, we describe the largest reported series of staged surgical resections of brain AVMs.

Methods: This is a retrospective review of surgically resected AVMs at a single institution from 1998-2018. Patients who underwent ≥2 resections within 1 year were reviewed. Only those in whom initial resection was terminated with intention for further resection were included in analysis.

Results: Twenty patients underwent deliberately staged resection from 1998-2018. Average age at treatment was 36.2 years (SD 16.5 years). Eleven patients (55%) were female, and 12 (60%) had left-sided AVMs. Median Spetzler-Martin grade was 4 (interquartile range [IQR]: 3-4). Average AVM nidus diameter was 5.0 cm (SD 1.7 cm). Seven patients (35%) presented with AVM rupture, and 12 (60%) presented with focal neurologic deficits without hemorrhage. Seventeen patients (85%) underwent preoperative embolization, median number of embolizations was 3 (IQR: 2-4). Three patients (15%) underwent preoperative radiosurgery. Median number of days between surgeries was 28 (IQR: 8-41 days). Perioperative course was complicated by hemorrhage in 3 patients (15%); 1 required decompressive hemicraniectomy prior to the second stage of surgery. Good functional outcome (defined as modified Rankin Scale score ≤2) was achieved in 14 patients (70%).

Conclusions: Staged surgical resection of large and complex AVMs can be performed with good outcomes in carefully selected patients.
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http://dx.doi.org/10.1016/j.wneu.2020.11.036DOI Listing
February 2021

Efficacy and safety of embolization of dural arteriovenous fistulas via the ophthalmic artery.

Interv Neuroradiol 2021 Jun 26;27(3):444-450. Epub 2020 Oct 26.

Division of Neuroimaging and Neurointervention, Department of Radiology, Stanford University School of Medicine, Stanford, CA, USA.

Introduction: Dural arteriovenous fistulae (DAVF) are vascular lesions with arteriovenous shunting that may be treated with surgical obliteration or endovascular embolization. Some DAVF, such as anterior cranial fossa DAVF (AC-DAVF) derive their arterial supply from ophthalmic artery branches in nearly all cases, and trans-arterial embolization carries a risk of vision loss. We determined the efficacy and safety of trans-ophthalmic artery embolization of DAVF.

Materials And Methods: We performed a retrospective cohort study of all patients with DAVF treated by trans-ophthalmic artery embolization from 2012 to 2020. Primary outcome was angiographic cure of the DAVF. Secondary outcomes included vision loss, visual impairment, orbital cranial nerve injury, stroke, modified Rankin Scale at 90-days, and mortality.

Results: 12 patients met inclusion criteria (9 males; 3 females). 10 patients had AC-DAVF. Patient age was 59.7  ±  9.5 (mean ± SD) years. Patients presented with intracranial hemorrhage (4 patients), headache (4 patients), amaurosis fugax (1 patients), or were incidentally discovered (2 patients). DAVF Cognard grades were: II (1 patient), III (6 patients), and IV (5 patients). DAVF were embolized with Onyx (10 patients), nBCA glue (1 patient), and a combination of coils and Onyx (1 patient). DAVF cure was achieved in 11 patients (92%). No patients experienced vision loss, death, or permanent disability. One patient experienced a minor complication of blurry vision attributed to posterior ischemic optic neuropathy. 90-day mRS was 0 (10 patients) and 1 (2 patients).

Conclusions: Trans-ophthalmic artery embolization is an effective and safe treatment for DAVF.
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http://dx.doi.org/10.1177/1591019920969270DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8190942PMC
June 2021

In Reply to the Letter to the Editor Regarding "Contralateral Vasospasm in an Uncomplicated Elective Anterior Communicating Artery Aneurysm Clipping".

World Neurosurg 2020 10;142:540

Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine and Stanford Health Center, Stanford, California, USA. Electronic address:

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http://dx.doi.org/10.1016/j.wneu.2020.07.193DOI Listing
October 2020

Microsurgical Resection of an Orbital Arteriovenous Malformation With Intraoperative Digital Subtraction Angiography.

Ophthalmic Plast Reconstr Surg 2021 May-Jun 01;37(3S):S141-S144

Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine.

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http://dx.doi.org/10.1097/IOP.0000000000001815DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8191182PMC
May 2021

Incidental De Novo Cerebral Microhemorrhages are Predictive of Future Symptomatic Macrohemorrhages After Surgical Revascularization in Moyamoya Disease.

Neurosurgery 2020 12;88(1):74-81

Stanford Stroke Center, Department of Neurosurgery, Stanford University School of Medicine, Stanford, California.

Background: Patients with moyamoya disease who develop incidental cerebral microhemorrhages (CMHs) on magnetic resonance imaging (MRI) have higher risk of developing subsequent symptomatic repeat macro hemorrhages.

Objective: To evaluate the effect of surgical revascularization on development of de novo CMHs and assess its correlation with repeat hemorrhage rates and functional outcome in hemorrhagic onset moyamoya disease (HOMMD).

Methods: We retrospectively reviewed a prospectively managed departmental database of all patients presenting with HOMMD treated between 1987 and 2019. The search yielded 121 patients with adequate MRI follow-up for inclusion into the study.

Results: In total, 42 preoperative CMHs were identified in 18 patients (15%). Patients presenting with preoperative CMH were more likely to develop de novo CMH after surgical revascularization. 7 de novo CHMs were identified in 6 patients (5%) on routine postoperative MRI at distinct locations from previous sites of hemorrhage or CMH. Symptomatic repeat macro hemorrhage was confirmed radiographically in 15 patients (12%). A total 5 (83%) of 6 patients with de novo CMHs later suffered symptomatic repeat macro hemorrhage with 4 of 5 (80%) hemorrhages occurring at sites of previous CMH. On univariate and multivariate analysis, de novo CMHs was the only significant variable predictive for developing repeat symptomatic hemorrhage. Development of delayed repeat symptomatic hemorrhage was prognostic for higher modified Rankin Score and therefore poorer functional status, whereas preoperative functional status was predictive of final outcome.

Conclusion: De novo CMHs after surgical revascularization might serve as a radiographic biomarker for refractory disease and suggest patients are at risk for future symptomatic macro hemorrhage.
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http://dx.doi.org/10.1093/neuros/nyaa319DOI Listing
December 2020

Clinical Course of Unilateral Moyamoya Disease.

Neurosurgery 2020 Nov;87(6):1262-1268

Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine, Stanford, California.

Background: The natural history of unilateral moyamoya disease (MMD) progressing to bilateral MMD remains an enigma in modern vascular neurosurgery. Few, small series with limited follow-up have reported relatively high rates of contralateral stenosis progression.

Objective: To review our large series of unilateral MMD patients and evaluate radiographic and surgical progression rates, and identify any factors associated with progression.

Methods: We included all unilateral MMD cases treated from 1991 to 2017 in an observational study. We examined time to contralateral radiographic progression and contralateral progression requiring surgery. Using Cox regression analysis, we evaluated factors potentially associated with contralateral progression.

Results: There were 217 patients treated for unilateral MMD. About 71% were female, and the average age at first surgery was 33.8 yr. Average follow-up was 5.8 yr (range 1-22 yr). A total of 18 patients (8.3%) developed contralateral progression. And 8 of these (3.7%) developed progression requiring bypass surgery. Baseline stenosis and hyperlipidemia (HLD) were significantly associated with radiographic progression (hazard ratio [HR] = 9.7, P = .006; HR = 4.0, P = .024). Baseline stenosis was associated with surgical progression (HR = 44.2, P = .002). Results were similar when controlling for possible confounders using multivariate regression.

Conclusion: Previous series showed relatively high rates of progression in unilateral MMD (15%-30%), but these studies were small and long-term follow-up was rarely available. Our large series indicates that the rate of progression is lower than previously reported but still warrants yearly noninvasive screening. These data may provide indirect support for statin therapy in MMD.
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http://dx.doi.org/10.1093/neuros/nyaa284DOI Listing
November 2020

Treatment of posterior circulation fusiform aneurysms.

J Neurosurg 2020 07 24;134(6):1894-1900. Epub 2020 Jul 24.

Departments of1Neurosurgery and.

Objective: Perforator arteries, the absence of an aneurysm discrete neck, and the often-extensive nature of posterior circulation fusiform aneurysms present treatment challenges. There have been advances in microsurgical and endovascular approaches, including flow diversion, and the authors sought to review these treatments in a long-term series at their neurovascular referral center.

Methods: The authors performed a retrospective chart review from 1990 to 2018. Primary outcomes were modified Rankin Scale (mRS) scores and Glasgow Outcome Scale (GOS) scores at follow-up. The authors also examined neurological complication rates. Using regression techniques, they reviewed independent and dependent variables, including presenting features, aneurysm location and size, surgical approach, and pretreatment and posttreatment thrombosis.

Results: Eighty-four patients met the inclusion criteria. Their mean age was 53 years, and 49 (58%) were female. Forty-one (49%) patients presented with subarachnoid hemorrhage. Aneurysms were located on the vertebral artery (VA) or posterior inferior cerebellar artery (PICA) in 50 (60%) patients, basilar artery (BA) or vertebrobasilar junction (VBJ) in 22 (26%), and posterior cerebral artery (PCA) in 12 (14%). Thirty-one (37%) patients were treated with microsurgical and 53 (63%) with endovascular approaches. Six aneurysms were treated with endovascular flow diversion. The authors found moderate disability or better (mRS score ≤ 3) in 85% of the patients at a mean 14-month follow-up. The GOS score was ≥ 4 in 82% of the patients. The overall neurological complication rate was 12%. In the regression analysis, patients with VA or PICA aneurysms had better functional outcomes than the other groups (p < 0.001). Endovascular strategies were associated with better outcomes for BA-VBJ aneurysms (p < 0.01), but microsurgery was associated with better outcomes for VA-PICA and PCA aneurysms (p < 0.05). There were no other significant associations between patient, aneurysm characteristics, or treatment features and neurological complications (p > 0.05). Patients treated with flow diversion had more complications than those who underwent other endovascular and microsurgical strategies, but the difference was not significant in regression models.

Conclusions: Posterior circulation fusiform aneurysms remain a challenging aneurysm subtype, but an interdisciplinary treatment approach can result in good outcomes. While flow diversion is a useful addition to the armamentarium, traditional endovascular and microsurgical techniques continue to offer effective options.
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http://dx.doi.org/10.3171/2020.4.JNS192838DOI Listing
July 2020

Predicting PET Cerebrovascular Reserve with Deep Learning by Using Baseline MRI: A Pilot Investigation of a Drug-Free Brain Stress Test.

Radiology 2020 09 14;296(3):627-637. Epub 2020 Jul 14.

From the Department of Radiology, The Richard M. Lucas Center for Imaging, Stanford University, 1201 Welch Rd, Stanford, CA 94305 (D.Y.T.C., A.P.F., M.Y.Z., G.Z.); Department of Medical Imaging, Taipei Medical University-Shuan-Ho Hospital, New Taipei City, Taiwan (D.Y.T.C.); Department of Radiology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan (D.Y.T.C.); Department of Neurosurgery, Tokyo Medical and Dental University, Tokyo, Japan (Y.I.); Department of Bioengineering, University of California Riverside, Riverside, Calif (J.G.); and Department of Neurosurgery, Stanford University, Stanford, Calif (G.K.S.).

Background Cerebrovascular reserve (CVR) may be measured by using an acetazolamide test to clinically evaluate patients with cerebrovascular disease. However, acetazolamide use may be contraindicated and/or undesirable in certain clinical settings. Purpose To predict CVR images generated from acetazolamide vasodilation with a deep learning network by using only images before acetazolamide administration. Materials and Methods Simultaneous oxygen 15 (O)-labeled water PET/MRI before and after acetazolamide injection were retrospectively analyzed for patients with Moyamoya disease and healthy control participants from April 2017 to May 2019. Inputs to deep learning models were perfusion-based images (arterial spin labeling [ASL]), structural scans (T2 fluid-attenuated inversion-recovery, T1), and brain location. Two models, that is, O-labeled water PET cerebral blood flow (CBF) and MRI (PET-plus-MRI model) before acetazolamide administration and only MRI (MRI-only model) before acetazolamide administration, were trained and tested with sixfold cross-validation. The models learned to predict a voxelwise relative CBF change (rΔCBF) map by using rΔCBF measured with PET due to acetazolamide as ground truth. Quantitative analysis included image quality metrics (peak signal-to-noise ratio, root mean square error, and structural similarity index), as well as comparison between the various methods by using correlation and Bland-Altman analyses. Identification of vascular territories with impaired rΔCBF was evaluated by using receiver operating characteristic metrics. Results Thirty-six participants were included: 24 patients with Moyamoya disease (mean age ± standard deviation, 41 years ± 12; 17 women) and 12 age-matched healthy control participants (mean age, 39 years ± 16; nine women). The rΔCBF maps predicted by both deep learning models demonstrated better image quality metrics than did ASL (all < .001 in patients) and higher correlation coefficient with PET than with ASL (PET-plus-MRI model, 0.704; MRI-only model, 0.690 vs ASL, 0.432; both < .001 in patients). Both models also achieved high diagnostic performance in identifying territories with impaired rΔCBF (area under receiver operating characteristic curve, 0.95 for PET-plus-MRI model [95% confidence interval: 0.90, 0.99] and 0.95 for MRI-only model [95% confidence interval: 0.91, 0.98]). Conclusion By using only images before acetazolamide administration, PET-plus-MRI and MRI-only deep learning models predicted cerebrovascular reserve images without the need for vasodilator injection. © RSNA, 2020
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http://dx.doi.org/10.1148/radiol.2020192793DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7457949PMC
September 2020

Optogenetic Stimulation Reduces Neuronal Nitric Oxide Synthase Expression After Stroke.

Transl Stroke Res 2021 04 13;12(2):347-356. Epub 2020 Jul 13.

Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine, Stanford, CA, USA.

Post-stroke optogenetic stimulation has been shown to enhance neurovascular coupling and functional recovery. Neuronal nitric oxide synthase (nNOS) has been implicated as a key regulator of the neurovascular response in acute stroke; however, its role in subacute recovery remains unclear. We investigated the expression of nNOS in stroke mice undergoing optogenetic stimulation of the contralesional lateral cerebellar nucleus (cLCN). We also examined the effects of nNOS inhibition on functional recovery using a pharmacological inhibitor targeting nNOS. Optogenetically stimulated stroke mice demonstrated significant improvement on the horizontal rotating beam task at post-stroke days 10 and 14. nNOS mRNA and protein expression was significantly and selectively decreased in the contralesional primary motor cortex (cM1) of cLCN-stimulated mice. The nNOS expression in cM1 was negatively correlated with improved recovery. nNOS inhibitor (ARL 17477)-treated stroke mice exhibited a significant functional improvement in speed at post-stroke day 10, when compared to stroke mice receiving vehicle (saline) only. Our results show that optogenetic stimulation of cLCN and systemic nNOS inhibition both produce functional benefits after stroke, and suggest that nNOS may play a maladaptive role in post-stroke recovery.
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http://dx.doi.org/10.1007/s12975-020-00831-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7925487PMC
April 2021

Direct versus indirect bypass procedure for the treatment of ischemic moyamoya disease: results of an individualized selection strategy.

J Neurosurg 2020 Jun 12;134(5):1578-1589. Epub 2020 Jun 12.

1Department of Neurosurgery and Stanford Stroke Center, Stanford University School of Medicine.

Objective: The only effective treatment for ischemic moyamoya disease (iMMD) is cerebral revascularization by an extracranial to intracranial bypass. The preferred revascularization method remains controversial: direct versus indirect bypass. The purpose of this study was to test the hypothesis that method choice should be personalized based on angiographic, hemodynamic, and clinical characteristics to balance the risk of perioperative major stroke against treatment efficacy.

Methods: Patients with iMMD were identified retrospectively from a prospectively maintained database. Those with mild to moderate internal carotid artery or M1 segment stenosis, preserved cerebrovascular reserve, intraoperative M4 segment anterograde flow ≥ 8 ml/min, or the absence of frequent and severe transient ischemic attacks (TIAs) or stroke had been assigned to indirect bypass. The criteria for direct bypass were severe ICA or M1 segment stenosis or occlusion, impaired cerebrovascular reserve or steal phenomenon, intraoperative M4 segment retrograde flow or anterograde flow < 8 ml/min, and the presence of frequent and severe TIAs or clinical strokes. The primary study endpoint was MRI-confirmed symptomatic stroke ≤ 7 days postoperatively resulting in a decline in the modified Rankin Scale (mRS) score from preoperatively to 6 months postoperatively. As a secondary endpoint, the authors assessed 6-month postoperative DSA-demonstrated revascularization, which was classified as < 1/3, 1/3-2/3, or > 2/3 of the middle cerebral artery territory.

Results: One hundred thirty-eight patients with iMMD affecting 195 hemispheres revascularized in the period from March 2016 to June 2018 were included in this analysis. One hundred thirty-three hemispheres were revascularized with direct bypass and 62 with indirect bypass. The perioperative stroke rate was 4.7% and 6.8% in the direct and indirect groups, respectively (p = 0.36). Degree of revascularization was higher in the direct bypass group (p = 0.03). The proportion of patients improving to an mRS score 0-1 (from preoperatively to 6 months postoperatively) tended to be higher in the direct bypass group, although the difference between the two bypass groups was not statistically significant (p = 0.27).

Conclusions: The selective use of an indirect bypass procedure for iMMD did not decrease the perioperative stroke rate. Direct bypass provided a significantly higher degree of revascularization. The authors conclude that direct bypass is the treatment of choice for iMMD.
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http://dx.doi.org/10.3171/2020.3.JNS192847DOI Listing
June 2020

Initial experience with the Scepter Mini dual-lumen balloon for transophthalmic artery embolization of anterior cranial fossa dural arteriovenous fistulae.

J Neurointerv Surg 2020 Nov 20;12(11):1132-1136. Epub 2020 May 20.

Radiology, Neuroadiology and Neurointervention Division, Stanford University School of Medicine, Stanford, California, USA

Background: Precise delivery of liquid embolic agents (LEAs) remains a challenge in the endovascular treatment of dural arteriovenous fistulae (dAVFs) and cerebral arteriovenous malformations (cAVMs). Despite significant advances in the past decade, LEA reflux and catheter navigability remain shortcomings of current endovascular technology, particularly in small and tortuous arteries. The Scepter Mini dual-lumen balloon microcatheter aims to address these issues by decreasing the distal catheter profile (1.6 French) while allowing for a small (2.2 mm diameter) balloon at its tip.

Methods: We report our initial experience with the Scepter Mini in two patients with anterior cranial fossa dAVFs that were treated with transophthalmic artery embolization.

Results: In both patients, the Scepter Mini catheter was able to be safely advanced into the distal ophthalmic artery close to the fistula site, and several centimeters past the origins of the central retinal and posterior ciliary arteries. A single Onyx injection without any reflux resulted in angiographic cure of the dAVF in both cases, and neither patient suffered any vision loss.

Conclusions: These initial experiences suggest that the Scepter Mini represents a significant advance in the endovascular treatment of dAVFs and cAVMs and will allow for safer and more efficacious delivery of LEAs into smaller and more distal arteries while diminishing the risk of LEA reflux.
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http://dx.doi.org/10.1136/neurintsurg-2020-016013DOI Listing
November 2020
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