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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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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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Matthew B. Potts, Sunil A. Sheth, Jonathan Louie, Matthew D. Smyth, Penny K. Sneed, Michael W. McDermott, Michael T. Lawton, William L. Young, Steven W. Hetts, Heather J. Fullerton, and Nalin Gupta

Object

Stereotactic radiosurgery (SRS) is an established treatment modality for brain arteriovenous malformations (AVMs) in children, but the optimal treatment parameters and associated treatment-related complications are not fully understood. The authors present their single-institution experience of using SRS, at a relatively low marginal dose, to treat AVMs in children for nearly 20 years; they report angiographic outcomes, posttreatment hemorrhage rates, adverse treatment-related events, and functional outcomes.

Methods

The authors conducted a retrospective review of 2 cohorts of children (18 years of age or younger) with AVMs treated from 1991 to 1998 and from 2000 to 2010.

Results

A total of 80 patients with follow-up data after SRS were identified. Mean age at SRS was 12.7 years, and 56% of patients had hemorrhage at the time of presentation. Median target volume was 3.1 cm3 (range 0.09–62.3 cm3), and median prescription marginal dose used was 17.5 Gy (range 12–20 Gy). Angiograms acquired 3 years after treatment were available for 47% of patients; AVM obliteration was achieved in 52% of patients who received a dose of 18–20 Gy and in 16% who received less than 18 Gy. At 5 years after SRS, the cumulative incidence of hemorrhage was 25% (95% CI 16%–37%). No permanent neurological deficits occurred in patients who did not experience posttreatment hemorrhage. Overall, good functional outcomes (modified Rankin Scale Scores 0–2) were observed for 78% of patients; for 66% of patients, functional status improved or remained the same as before treatment.

Conclusions

A low marginal dose minimizes SRS-related neurological deficits but leads to low rates of obliteration and high rates of hemorrhage. To maximize AVM obliteration and minimize posttreatment hemorrhage, the authors recommend a prescription marginal dose of 18 Gy or more. In addition, SRS-related symptoms such as headache and seizures should be considered when discussing risks and benefits of SRS for treating AVMs in children.

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Andreu Gabarrós Canals, Ana Rodríguez-Hernández, William L. Young, Michael T. Lawton, and for the UCSF Brain AVM Study Project

Object

Descriptions of temporal lobe arteriovenous malformations (AVMs) are inconsistent. To standardize reporting, the authors blended existing descriptions in the literature into an intuitive classification with 5 anatomical subtypes: lateral, medial, basal, sylvian, and ventricular. The authors' surgical experience with temporal lobe AVMs was reviewed according to these subtypes.

Methods

Eighty-eight patients with temporal lobe AVMs were treated surgically.

Results

Lateral temporal lobe AVMs were the most common (58 AVMs, 66%). Thirteen AVMs (15%) were medial, 9 (10%) were basal, and 5 (6%) were sylvian. Ventricular AVMs were least common (3 AVMs, 3%). A temporal craniotomy based over the ear was used in 64%. Complete AVM resection was achieved in 82 patients (93%). Four patients (5%) died in the perioperative period (6 in all were lost to follow-up); 71 (87%) of the remaining 82 patients had good outcomes (modified Rankin Scale scores 0–2); and 68 (83%) were unchanged or improved after surgery.

Conclusions

Categorization of temporal AVMs into subtypes can assist with surgical planning and also standardize reporting. Lateral AVMs are the easiest to expose surgically, with circumferential access to feeding arteries and draining veins at the AVM margins. Basal AVMs require a subtemporal approach, often with some transcortical dissection through the inferior temporal gyrus. Medial AVMs are exposed tangentially with an orbitozygomatic craniotomy and transsylvian dissection of anterior choroidal artery and posterior cerebral artery feeders in the medial cisterns. Medial AVMs posterior to the cerebral peduncle require transcortical approaches through the temporo-occipital gyrus. Sylvian AVMs require a wide sylvian fissure split and differentiation of normal arteries, terminal feeding arteries, and transit arteries. Ventricular AVMs require a transcortical approach through the inferior temporal gyrus that avoids the Meyer loop. Surgical results with temporal lobe AVMs are generally good, and classifying them does not offer any prediction of surgical risk.

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Yong Bae Kim, William L. Young, and Michael T. Lawton

Object

Parafalcine arteriovenous malformations (AVMs) have a midline plane in common, but differ in their location (anterior, middle, or posterior) and depth (superficial or deep). Surgical management varies with AVM location and depth in terms of patient position, head position, craniotomy, and surgical approach. This study examined surgical strategies, patient outcomes, and regional factors influencing results.

Methods

Patients with AVMs located on the medial surface of the cerebral hemisphere were identified retrospectively from a consecutive, single-neurosurgeon series that is registered prospectively as part of the UCSF Brain Arteriovenous Malformation Study Project. During a 12-year period, 443 patients with AVMs were treated surgically. Of these 443 patients, 132 (30%) had parafalcine AVMs, which were distributed in zones as follows: superficial-anterior, 25 (18.9%); superficial-middle, 26 (19.7%); superficial-posterior, 39 (29.5%); deep-anterior, 25 (18.9%); deep-posterior, 17 (12.9%). Five different surgical strategies were used depending on AVM zone.

Results

Complete AVM resection was achieved in 123 (93.2%) of 132 patients. Overall, neurological condition improved in 74 patients (56.1%) and remained unchanged in 41 patients (31.1%). Neurological condition deteriorated in 12 patients (9.1%), and 5 patients (3.8%) died. Patients with AVMs in the superficial-middle zone had the highest rate of neurological deterioration (26.9%).

Conclusions

Parafalcine AVMs lie on a midline surface that, when exposed with a bilateral craniotomy across the superior sagittal sinus and a wide opening of the interhemispheric fissure, makes them superficial. However, unlike convexity AVMs, which are approached perpendicularly, parafalcine AVMs are approached tangentially. Gravity retraction is useful with deeply located AVMs (those in the deep-anterior and deep-posterior zones), because it widens the interhemispheric fissure and accesses deep arterial feeding vessels from the anterior and posterior cerebral arteries. Surgical risks were increased in the superficial-middle zone, which is likely explained by the proximity of sensorimotor cortex. The authors' regional classification of parafalcine AVMs may serve as a guide to surgical planning.

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William L. Young, Pui-Yan Kwok, Ludmila Pawlikowska, Michael T. Lawton, Helen Kim, Pirro G. Hysi, and Douglas A. Marchuk

Object.

Important central nervous system (CNS) manifestations in patients with hereditary hemorrhagic telangiectasia (HHT) include arteriovenous malformations (AVMs) and dural arteriovenous fistulas (DAVFs). Hereditary hemorrhagic telangiectasia is caused by germline mutations of two genes: ENG (HHT Type 1) and ACVRL1 (HHT Type 2). The ENG gene variations have been associated with the formation of intracranial aneurysms. The authors studied whether sequence variations in ACVRL1 or ENG are associated with the development of clinically sporadic arteriovenous dysplasias and aneurysms of the CNS.

Methods.

The coding sequence (in 44 patients with AVMs and 27 with aneurysms) and the 5′ end and the polyA site (in 53 patients with AVMs) of the ACVRL1 gene were analyzed for sequence variations using direct sequencing and single-strand conformational polymorphism analysis. One ENG and three ACVRL1 gene polymorphisms were genotyped using restriction enzyme–based analysis in 101 patients with sporadic AVMs and DAVFs of the CNS, 79 patients treated for intracranial aneurysms, and 202 control volunteers.

The authors identified a statistically significant association between the IVS3 −35A/T polymorphism in intron 3 of the ACVRL1 gene and the development of AVMs and DAVFs (p = 0.004; odds ratio [OR] 1.73; 95% confidence interval [CI] 1.19–2.51; after adjustments for age and sex), but not aneurysms (crude OR 0.82; 95% CI 0.55–1.18).

Conclusions.

The results of this study link ACVRL1 (HHT Type 2 gene) to the formation of the clinically sporadic variants of vascular malformations of the CNS most commonly seen in patients with HHT, that is, AVMs and DAVFs.

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Rose Du, Tomoki Hashimoto, Tarik Tihan, William L. Young, Victor Perry, and Michael T. Lawton

✓ Data on the growth, regression, and de novo formation of arteriovenous malformations (AVMs) suggest that some of these lesions are not formed and developed only during embryogenesis. Patients with hereditary hemorrhagic telangiectasia (HHT) have a genetic propensity to form AVMs. The authors report on the growth and regression of AVMs in a single patient with HHT. This 26-day-old boy with a family history of HHT1 and a mutation in ENG on chromosome 9 presented with a generalized seizure. Results of computed tomography revealed a left frontoparietal intra-parenchymal hemorrhage. Cerebral angiography revealed multiple AVMs. Follow-up angiograms obtained 5 months later showed both growth and regression of the AVMs. A craniotomy was performed for complete resection of the left parietal AVM. Histopathological features of the surgical specimen were examined. Active angiogenesis, as indicated by increased endothelial proliferation, might be a part of the underlying pathophysiology of the growth and regression of AVMs.

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Tae Sung Park

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René O. Sanchez-Mejia, Sravana K. Chennupati, Nalin Gupta, Heather Fullerton, William L. Young, and Michael T. Lawton

Object

Young age is considered an important factor in determining outcomes after microsurgical resection of arteriovenous malformations (AVMs), but better results in children have not been adequately explained. A consecutive series of pediatric and adult patients was reviewed to determine whether differences in outcomes between these two groups were due to differences in AVM anatomy, rupture rates, neurological condition at presentation, treatment techniques, or other causes.

Methods

As assessed using the modified Rankin Scale (mRS), patient characteristics, clinical presentation, AVM anatomy, treatment techniques, and outcomes were compared between age groups. Thirty-two pediatric and 192 adult patients underwent microsurgical AVM resection during a 6.4-year period; complete resection was achieved in 97% of the children and 98% of adults. Superior outcomes were observed in children, who had better final mRS scores (p = 0.003) and more favorable changes in these scores (the condition of 94% of children improved or remained unchanged, compared with 70% of adults; p = 0.001). The change in the mean mRS scores was 1.31 for children and 0.14 for adults (p = 0.001). There were no significant clinical, anatomical, or therapeutic differences between children and adults.

Conclusions

This analysis confirms the observation that children fare better than adults after microsurgical AVM resection. This discrepancy cannot be explained by differences in AVM anatomy, lesion rupture rates, presenting neurological condition, or treatment techniques, leading the authors to infer that neural plasticity may augment surgical tolerance and recovery in children. These findings bolster the choice of aggressive microsurgical management of AVMs and recalibration of surgical risk assessment in children.

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G. Edward Vates, Tomoki Hashimoto, William L. Young, and Michael T. Lawton

Object

The goal of this study was to examine the roles of vascular endothelial growth factor (VEGF) and angiopoietin- 2 (Ang-2) in the formation of blood vessels in the brain in a developmental animal model not routinely used for such a study.

Methods

Either VEGF, Ang-2, or a combination of the two factors were injected into the optic tectum of 4-day-old quail embryos. Immunohistochemical analysis and laser confocal microscopy were used to observe the effects on endothelial cells in the brain. Vascular endothelial growth factor and Ang-2 had very different effects on the development of blood vessels; the former caused expansion and the latter retraction of these vessels. Treatment with a combination of VEGF and Ang-2 caused retroorbital or intraventricular hemorrhage, and brain blood vessels appeared enlarged and dysmorphic, with dramatically extended filopodia.

Conclusions

Some of these observations may provide insight into how one may develop a better model of brain arteriovenous malformations.