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Adib A. Abla and Michael T. Lawton

Object

The authors describe their experience with intracranial-to-intracranial (IC-IC) bypasses for complex anterior cerebral artery (ACA) aneurysms with giant size, dolichoectatic morphology, or intraluminal thrombus; they determine how others have addressed the limitations of ACA bypass; and they discuss clinical indications and microsurgical technique.

Methods

A consecutive, single-surgeon experience with ACA aneurysms and bypasses over a 16-year period was retrospectively reviewed. Bypasses for ACA aneurysms reported in the literature were also reviewed.

Results

Ten patients had aneurysms that were treated with ACA bypass as part of their surgical intervention. Four patients presented with subarachnoid hemorrhage and 3 patients with mass effect symptoms from giant aneurysms; 1 patient with bacterial endocarditis had a mycotic aneurysm, and 1 patient's meningioma resection was complicated by an iatrogenic pseudoaneurysm. One patient had his aneurysm discovered incidentally. There were 2 precommunicating aneurysms (A1 segment of the ACA), 5 communicating aneurysms (ACoA), and 3 postcommunicating (A2–A3 segments of the ACA). In situ bypasses were used in 4 patients (A3-A3 bypass), interposition bypasses in 4 patients, reimplantation in 1 patient (pericallosal artery-to-callosomarginal artery), and reanastomosis in 1 patient (pericallosal artery). Complete aneurysm obliteration was demonstrated in 8 patients, and bypass patency was demonstrated in 8 patients. One bypass thrombosed, but 4 years later. There were no operative deaths, and permanent neurological morbidity was observed in 2 patients. At last follow-up, 8 patients (80%) were improved or unchanged. In a review of the 29 relevant reports, the A3-A3 in situ bypass was used most commonly, extracranial (EC)–IC interpositional bypasses were the second most common, and reanastomosis and reimplantation were used the least.

Conclusions

Anterior cerebral artery aneurysms requiring bypass are rare and can be revascularized in a variety of ways. Anterior cerebral artery aneurysms, more than any other aneurysms, require a thorough survey of patient-specific anatomy and microsurgical options before deciding on an individualized management strategy. The authors' experience demonstrates a preference for IC-IC reconstruction, but EC-IC bypasses are reported frequently in the literature. The authors conclude that ACA bypass with indirect aneurysm occlusion is a good alternative to direct clip reconstruction for complex ACA aneurysms.

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Adib A. Abla and Michael T. Lawton

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Adib A. Abla, Cameron M. McDougall, Jonathan D. Breshears, and Michael T. Lawton

OBJECT

Intracranial-to-intracranial (IC-IC) bypasses are alternatives to traditional extracranial-to-intracranial (EC-IC) bypasses to reanastomose parent arteries, reimplant efferent branches, revascularize branches with in situ donor arteries, and reconstruct bifurcations with interposition grafts that are entirely intracranial. These bypasses represent an evolution in bypass surgery from using scalp arteries and remote donor sites toward a more local and reconstructive approach. IC-IC bypass can be utilized preferentially when revascularization is needed in the management of complex aneurysms. Experiences using IC-IC bypass, as applied to posterior inferior cerebellar artery (PICA) aneurysms in 35 patients, were reviewed.

METHODS

Patients with PICA aneurysms and vertebral artery (VA) aneurysms involving the PICA’s origin were identified from a prospectively maintained database of the Vascular Neurosurgery Service, and patients who underwent bypass procedures for PICA revascularization were included.

RESULTS

During a 17-year period in which 129 PICA aneurysms in 125 patients were treated microsurgically, 35 IC-IC bypasses were performed as part of PICA aneurysm management, including in situ p3-p3 PICA-PICA bypass in 11 patients (31%), PICA reimplantation in 9 patients (26%), reanastomosis in 14 patients (40%), and 1 V3 VA-to-PICA bypass with an interposition graft (3%). All aneurysms were completely or nearly completely obliterated, 94% of bypasses were patent, 77% of patients were improved or unchanged after treatment, and good outcomes (modified Rankin Scale ≤ 2) were observed in 76% of patients. Two patients died expectantly. Ischemic complications were limited to 2 patients in whom the bypasses occluded, and permanent lower cranial nerve morbidity was limited to 3 patients and did not compromise independent function in any of the patients.

CONCLUSIONS

PICA aneurysms receive the application of IC-IC bypass better than any other aneurysm, with nearly one-quarter of all PICA aneurysms treated microsurgically at our center requiring bypass without a single EC-IC bypass. The selection of PICA bypass is almost algorithmic: trapped aneurysms at the PICA origin or p1 segment are revascularized with a PICA-PICA bypass, with PICA reimplantation as an alternative; trapped p2 segment aneurysms are reanastomosed, bypassed in situ, or reimplanted; distal p3 segment aneurysms are reanastomosed or revascularized with a PICA-PICA bypass; and aneurysms of the p4 segment that are too distal for PICA-PICA bypass are reanastomosed. Interposition grafts are reserved for when these 3 primary options are unsuitable. A constructive approach that preserves the PICA with direct clipping or replaces flow with a bypass when sacrificed should remain an alternative to deconstructive PICA occlusion and endovascular coiling when complete aneurysm occlusion is unlikely.

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Matthew B. Potts, Darryl Lau, Adib A. Abla, Helen Kim, William L. Young, and Michael T. Lawton

OBJECT

Resection is an appealing therapy for brain arteriovenous malformations (AVMs) because of its high cure rate, low complication rate, and immediacy, and has become the first-line therapy for many AVMs. To clarify safety, efficacy, and outcomes associated with AVM resection in the aftermath of A Randomized Trial of Unruptured Brain AVMs (ARUBA), the authors reviewed their experience with low-grade AVMs—the most favorable AVMs for surgery and the ones most likely to have been selected for treatment outside of ARUBA's randomization process.

METHODS

A prospective AVM registry was searched to identify patients with Spetzler-Martin Grade I and II AVMs treated using resection during a 16-year period.

RESULTS

Of the 232 surgical patients included, 120 (52%) presented with hemorrhage, 33% had Spetzler-Martin Grade I, and 67% had Grade II AVMs. Overall, 99 patients (43%) underwent preoperative embolization, with unruptured AVMs embolized more often than ruptured AVMs. AVM resection was accomplished in all patients and confirmed angiographically in 218 patients (94%). There were no deaths among patients with unruptured AVMs. Good outcomes (modified Rankin Scale [mRS] score 0–1) were found in 78% of patients, with 97% improved or unchanged from their preoperative mRS scores. Patients with unruptured AVMs had better functional outcomes (91% good outcome vs 65% in the ruptured group, p = 0.0008), while relative outcomes were equivalent (98% improved/unchanged in patients with ruptured AVMs vs 96% in patients with unruptured AVMs).

CONCLUSIONS

Surgery should be regarded as the “gold standard” therapy for the majority of low-grade AVMs, utilizing conservative embolization as a preoperative adjunct. High surgical cure rates and excellent functional outcomes in patients with both ruptured and unruptured AVMs support a dominant surgical posture for low-grade AVMS, with radiosurgery reserved for risky AVMs in deep, inaccessible, and highly eloquent locations. Despite the technological advances in endovascular and radiosurgical therapy, surgery still offers the best cure rate, lowest risk profile, and greatest protection against hemorrhage for low-grade AVMs. ARUBA results are influenced by a low randomization rate, bias toward nonsurgical therapies, a shortage of surgical expertise, a lower rate of complete AVM obliteration, a higher rate of delayed hemorrhage, and short study duration. Another randomized trial is needed to reestablish the role of surgery in unruptured AVM management.

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W. Caleb Rutledge, Adib A. Abla, Jeffrey Nelson, Van V. Halbach, Helen Kim, and Michael T. Lawton

Object

Management of unruptured arteriovenous malformations (AVMs) is controversial. In the first randomized trial of unruptured AVMs (A Randomized Trial of Unruptured Brain Arteriovenous Malformations [ARUBA]), medically managed patients had a significantly lower risk of death or stroke and had better outcomes. The University of California, San Francisco (UCSF) was one of the participating ARUBA sites. While 473 patients were screened for eligibility, only 4 patients were enrolled in ARUBA. The purpose of this study is to report the treatment and outcomes of all ARUBA-eligible patients at UCSF.

Methods

The authors compared the treatment and outcomes of ARUBA-eligible patients using prospectively collected data from the UCSF brain AVM registry. Similar to ARUBA, they compared the rate of stroke or death in observed and treated patients and used the modified Rankin Scale to grade outcomes.

Results

Of 74 patients, 61 received an intervention and 13 were observed. Most treated patients had resection with or without preoperative embolization (43 [70.5%] of 61 patients). One of the 13 observed patients died after AVM hemorrhage. Nine of the 61 treated patients had a stroke or died. There was no significant difference in the rate of stroke or death (HR 1.34, 95% CI 0.12–14.53, p = 0.81) or clinical impairment (Fisher’s exact test, p > 0.99) between observed and treated patients.

Conclusions

The risk of stroke or death and degree of clinical impairment among treated patients was lower than reported in ARUBA. The authors found no significant difference in outcomes between observed and treated ARUBA-eligible patients at UCSF. Results in ARUBA-eligible patients managed outside that trial led to an entirely different conclusion about AVM intervention, due to the primary role of surgery, judicious surgical selection with established outcome predictors, and technical expertise developed at high-volume AVM centers.

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Adib A. Abla, Jeffrey Nelson, W. Caleb Rutledge, William L. Young, Helen Kim, and Michael T. Lawton

Object

Patients with posterior fossa arteriovenous malformations (AVMs) are more likely to present with hemorrhage than those with supratentorial AVMs. Observed patients subject to the AVM natural history should be informed of the individualized effects of AVM characteristics on the clinical course following a new, first-time hemorrhage. The authors hypothesize that the debilitating effects of first-time bleeding from an AVM in a previously intact patient with an unruptured AVM are more pronounced when AVMs are located in the posterior fossa.

Methods

The University of California, San Francisco prospective registry of brain AVMs was searched for patients with a ruptured AVM who had a pre-hemorrhage modified Rankin Scale (mRS) score of 0 and a post-hemorrhage mRS score obtained within 2 days of the hemorrhagic event. A total of 154 patients met the inclusion criteria for this study. Immediate post-hemorrhage presentation mRS scores were dichotomized into nonsevere outcome (mRS ≤ 3) and severe outcome (mRS > 3). There were 77 patients in each group. Univariate and multivariate logistic regression analyses using severe outcome as the binary response were run. The authors also performed a logistic regression analysis to measure the effects of hematoma volume and AVM location on severe outcome.

Results

Posterior fossa location was a significant predictor of severe outcome (OR 2.60, 95% CI 1.20–5.67, p = 0.016) and the results were strengthened in a multivariate model (OR 4.96, 95% CI 1.73–14.17, p = 0.003). Eloquent location (OR 3.47, 95% CI 1.37–8.80, p = 0.009) and associated arterial aneurysms (OR 2.58, 95% CI 1.09, 6.10; p = 0.031) were also significant predictors of poor outcome. Hematoma volume for patients with a posterior fossa AVM was 10.1 ± 10.1 cm3 compared with 25.6 ±28.0 cm3 in supratentorial locations (p = 0.003). A logistic analysis (based on imputed hemorrhage volume values) found that posterior fossa location was a significant predictor of severe outcome (OR 8.03, 95% CI 1.20–53.77, p = 0.033) and logarithmic hematoma volume showed a positive, but not statistically significant, association in the model (p = 0.079).

Conclusions

Patients with posterior fossa AVMs are more likely to have severe outcomes than those with supratentorial AVMs based on this natural history study. Age, sex, and ethnicity were not associated with an increased risk of severe outcome after AVM rupture, but posterior fossa location, associated aneurysms, and eloquent location were associated with poor post-hemorrhage mRS scores. Posterior fossa hematomas are poorly tolerated, with severe outcomes observed even with smaller hematoma volumes. These findings support an aggressive surgical posture with respect to posterior fossa AVMs, both before and after rupture.

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Adib A. Abla, William Caleb Rutledge, Zachary A. Seymour, Diana Guo, Helen Kim, Nalin Gupta, Penny K. Sneed, Igor J. Barani, David Larson, Michael W. McDermott, and Michael T. Lawton

OBJECT

The surgical treatment of many large arteriovenous malformations (AVMs) is associated with substantial risks, and many are considered inoperable. Furthermore, AVMs larger than 3 cm in diameter are not usually treated with conventional single-session radiosurgery encompassing the entire AVM volume. Volume-staged stereotactic radiosurgery (VS-SRS) is an option for large AVMs, but it has mixed results. The authors report on a series of patients with high-grade AVMs who underwent multiple VS-SRS sessions with resultant downgrading of the AVMs, followed by resection.

METHODS

A cohort of patients was retrieved from a single-institution AVM patient registry consisting of prospectively collected data. VS-SRS was performed as a planned intentional treatment. Surgery was considered as salvage therapy in select patients.

RESULTS

Sixteen AVMs underwent VS-SRS followed by surgery. Four AVMs presented with rupture. The mean patient age was 25.3 years (range 13–54 years). The average initial Spetzler-Martin grade before any treatment was 4, while the average supplemented Spetzler-Martin grade (Spetzler-Martin plus Lawton-Young) was 7.1. The average AVM size in maximum dimension was 5.9 cm (range 3.3–10 cm). All AVMs were supratentorial in location and all except one were in eloquent areas of the brain, with 7 involving primary motor cortex. The mean number of VS-SRS sessions was 2.7 (range 2–5 sessions). The mean interval between first VS-SRS session and resection was 5.7 years. There were 4 hemorrhages that occurred after VS-SRS. The average Spetzler-Martin grade was reduced to 2.5 (downgrade, −1.5) and the average supplemented Spetzler-Martin grade was reduced to 5.6 (downgrade, −1.5). The maximum AVM size was reduced to an average of 3.0 cm (downsize = −2.9 cm). The mean modified Rankin Scale (mRS) scores were 1.2, 2.3, and 2.2 before VS-SRS, before surgery, and at last follow-up, respectively (mean follow-up, 6.9 years). Fifteen AVMs were cured after surgery. Ten patients had good outcomes at last follow-up (7 with mRS Score 0 or 1, and 3 with mRS Score 2). There were 2 deaths (both mRS Score 1 before treatment) and 4 patients with mRS Score 3 outcome (from mRS Scores 0, 1, and 2 [n = 2]).

CONCLUSIONS

Volume-staged SRS can downgrade AVMs, transforming high-grade AVMs (initially considered inoperable) into operable AVMs with acceptable surgical risks. This treatment paradigm offers an alternative to conservative observation for young patients with unruptured AVMs and long life expectancy, where the risk of hemorrhage is substantial. Difficult AVMs were cured in 15 patients. Surgical morbidity associated with downgraded AVMs is reduced to that of postradiosurgical/preoperative supplemented Spetzler-Martin grades, not their initial AVM grades.

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Joseph H. Garcia, Ramin A. Morshed, Ethan A. Winkler, Yi Li, Christine K. Fox, Heather J. Fullerton, Caleb Rutledge, Angad S. Beniwal, Michael T. Lawton, Adib A. Abla, Nalin Gupta, and Steven W. Hetts

OBJECTIVE

Moyamoya is a progressive arteriopathy that predisposes patients to stroke due to stenosis of the intracranial internal carotid arteries and their proximal branches. Despite the morbidity caused by this condition, the ability to accurately predict prognosis for individual patients remains challenging. The goal of this study was to develop a systematic scoring method based on parenchymal findings on preoperative brain MRI to predict long-term outcomes for surgically treated pediatric patients with moyamoya.

METHODS

A retrospective surgical cohort of pediatric patients (≤ 18 years of age at the time of the initial surgery) with moyamoya from a single center were studied. Radiological variables with existing correlations between outcomes in moyamoya or other vascular diseases were chosen to score preoperative MRI based on easily defined parenchymal findings that could be rapidly assessed and used to make a numeric score. Calculated scores were correlated with clinical outcome measures using the Pearson correlation coefficient and area under the receiver operating characteristic curve (AUROC).

RESULTS

A total of 35 children with moyamoya disease or moyamoya syndrome were included in the study, with a median follow-up time of 2.6 years from the time of surgery. The pediatric moyamoya MRI score (PMMS) consists of ischemic changes (0–2; 0 = none, 1 = focal, 2 = diffuse), encephalomalacia (0–2; 0 = none, 1 = focal, 2 = diffuse), and hemorrhage (0–1; 0 = not present, 1 = present). PMMSs were highly correlated with pediatric modified Rankin Scale scores at the last follow-up (r = 0.7, 95% CI 0.44–0.84; p < 0.001) as a six-point scale, and when dichotomized (AUROC = 0.85).

CONCLUSIONS

The PMMS was found to be a simple tool based on preoperative MRI data that could be quickly and easily calculated and correlated with disability. This scoring method may aid future development of predictive models of outcomes for children with moyamoya disease and moyamoya syndrome.

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Joseph H. Garcia, Ethan A. Winkler, Ramin A. Morshed, Alex Lu, Simon G. Ammanuel, Satvir Saggi, Elaina J. Wang, Steve Braunstein, Christine K. Fox, Heather J. Fullerton, Helen Kim, Daniel L. Cooke, Steven W. Hetts, Michael T. Lawton, Adib A. Abla, and Nalin Gupta

OBJECTIVE

Children with cerebral arteriovenous malformations (AVMs) can present with seizures, potentially increasing morbidity and impacting clinical management. However, the factors that lead to seizures as a presenting sign are not well defined. While AVM-related seizures have been described in case series, most studies have focused on adults and have included patients who developed seizures after an AVM rupture. To address this, the authors sought to analyze demographic and morphological characteristics of AVMs in a large cohort of children.

METHODS

The demographic, clinical, and AVM morphological characteristics of 189 pediatric patients from a single-center database were studied. Univariate and multivariate logistic regression models were used to test the effect of these characteristics on seizures as an initial presenting symptom in patients with unruptured brain AVMs.

RESULTS

Overall, 28 of 189 patients initially presented with seizures (14.8%). By univariate comparison, frontal lobe location (p = 0.02), larger AVM size (p = 0.003), older patient age (p = 0.04), and the Supplemented Spetzler-Martin (Supp-SM) grade (0.0006) were associated with seizure presentation. Multivariate analysis confirmed an independent effect of frontal lobe AVM location and higher Supp-SM grade. All patients presenting with seizures had AVMs in the cortex or subcortical white matter.

CONCLUSIONS

While children and adults share some risk factors for seizure presentation, their risk factor profiles do not entirely overlap. Pediatric patients with cortical AVMs in the frontal lobe were more likely to present with seizures. Additionally, the Supp-SM grade was highly associated with seizure presentation. Future clinical research should focus on the effect of therapeutic interventions targeting AVMs on seizure control in these patients.

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Sen Gao, Jeffrey Nelson, Shantel Weinsheimer, Ethan A. Winkler, Caleb Rutledge, Adib A. Abla, Nalin Gupta, Joseph T. Shieh, Daniel L. Cooke, Steven W. Hetts, Tarik Tihan, Christopher P. Hess, Nerissa Ko, Brian P. Walcott, Charles E. McCulloch, Michael T. Lawton, Hua Su, Ludmila Pawlikowska, and Helen Kim

OBJECTIVE

Sporadic brain arteriovenous malformation (BAVM) is a tangled vascular lesion characterized by direct artery-to-vein connections that can cause life-threatening intracerebral hemorrhage (ICH). Recently, somatic mutations in KRAS have been reported in sporadic BAVM, and mutations in other mitogen-activated protein kinase (MAPK) signaling pathway genes have been identified in other vascular malformations. The objectives of this study were to systematically evaluate somatic mutations in MAPK pathway genes in patients with sporadic BAVM lesions and to evaluate the association of somatic mutations with phenotypes of sporadic BAVM severity.

METHODS

The authors performed whole-exome sequencing on paired lesion and blood DNA samples from 14 patients with sporadic BAVM, and 295 genes in the MAPK signaling pathway were evaluated to identify genes with somatic mutations in multiple patients with BAVM. Digital droplet polymerase chain reaction was used to validate KRAS G12V and G12D mutations and to assay an additional 56 BAVM samples.

RESULTS

The authors identified a total of 24 candidate BAVM-associated somatic variants in 11 MAPK pathway genes. The previously identified KRAS G12V and G12D mutations were the only recurrent mutations. Overall, somatic KRAS G12V was present in 14.5% of BAVM lesions and G12D was present in 31.9%. The authors did not detect a significant association between the presence or allelic burden of KRAS mutation and three BAVM phenotypes: lesion size (maximum diameter), age at diagnosis, and age at ICH.

CONCLUSIONS

The authors confirmed the high prevalence of somatic KRAS mutations in sporadic BAVM lesions and identified several candidate somatic variants in other MAPK pathway genes. These somatic variants may contribute to understanding of the etiology of sporadic BAVM and the clinical characteristics of patients with this condition.