Intermediate-grade brain arteriovenous malformations and the boundary of operability using the supplemented Spetzler-Martin grading system.

OBJECTIVE: Supplemented Spetzler-Martin grading (Supp-SM), which is the combination of Spetzler-Martin and Lawton-Young grades, was validated as being more accurate than stand-alone Spetzler-Martin grading, but an operability cutoff was not established. In this study, the authors surgically treated intermediate-grade AVMs to provide prognostic factors for neurological outcomes and to define AVMs at the boundary of operability. METHODS: Surgically treated Supp-SM intermediate-grade (5, 6, and 7) AVMs were analyzed from 2011 to 2018 at two medical centers. Worsened neurological outcomes were defined as increased modified Rankin Scale (mRS) scores on postoperative examinations. A second analysis of 2000-2011 data for Supp-SM grade 6 and 7 AVMs was performed to determine the subtypes with improved or unchanged outcomes. Patients were separated into three groups based on nidus size (S1: < 3 cm, S2: 3-6 cm, S3: > 6 cm) and age (A1: < 20 years, A2: 20-40 years, A3: > 40 years), followed by any combination of the combined supplemented grade: low risk (S1A1, S1A2, S2A1), intermediate risk (S2A2, S1A3, S3A1, or high risk (S3A3, S3A2, S2A3). RESULTS: Two hundred forty-six patients had intermediate Supp-SM grade AVMs. Of these patients, 102 had Supp-SM grade 5 (41.5%), 99 had Supp-SM grade 6 (40.2%), and 45 had Supp-SM grade 7 (18.3%). Significant differences in the proportions of patients with worse mRS scores at follow-up were found between the groups, with 24.5% (25/102) of patients in Supp-SM grade 5, 29.3% (29/99) in Supp-SM grade 6, and 57.8% (26/45) in Supp-SM grade 7 (p < 0.001). Patients with Supp-SM grade 7 AVMs had significantly increased odds of worse postoperative mRS scores (p < 0.001; OR 3.7, 95% CI 1.9-7.3). In the expanded cohort of 349 Supp-SM grade 6 AVM patients, a significantly higher proportion of older patients with larger Supp-SM grade 6 AVMs (grade 6+, 38.6%) had neurological deterioration than the others with Supp-SM grade 6 AVMs (22.9%, p = 0.02). Conversely, in an expanded cohort of 197 Supp-SM grade 7 AVM patients, a significantly lower proportion of younger patients with smaller Supp-SM grade 7 AVMs (grade 7-, 19%) had neurological deterioration than the others with Supp-SM grade 7 AVMs (44.9%, p = 0.01). CONCLUSIONS: Patients with Supp-SM grade 7 AVMs are at increased risk of worse postoperative neurological outcomes, making Supp-SM grade 6 an appropriate operability cutoff. However, young patients with small niduses in the low-risk Supp-SM grade 7 group (grade 7-) have favorable postoperative outcomes. Outcomes in Supp-SM grade 7 patients did not improve with surgeon experience, indicating that the operability boundary is a hard limit reflecting the complexity of high-grade AVMs.

Spetzler-Martin Grade III Arteriovenous Malformations: A Comparison of Modified and Supplemented Spetzler-Martin Grading Systems.

BACKGROUND: The modified Spetzler-Martin (SM) grading system proposes that grade III arteriovenous malformation (AVM) subtypes are associated with variable microsurgical risks, with small AVMs (III-) having lower risk and medium/eloquent AVMs (III+) having higher risk. Adding patient age and AVM bleeding status and compactness to the SM grade produces a score - the supplemented SM (Supp-SM) grade - to more accurately assess preoperative risk. OBJECTIVE: To compare the predictive power of the modified SM and Supp-SM grades for risk assessment in patients with grade III AVMs. METHODS: Patients with SM grade III AVMs treated between 2011 and 2018 were retrospectively reviewed. Good outcomes were defined as modified Rankin Scale (mRS) scores ≤ 2 or unchanged/improved mRS scores (pre- vs postsurgery). RESULTS: Of 102 patients with SM grade III AVMs, 59% had grade III- and 24% had grade III+ AVMs. Supp SM grade 6 and grade 7 AVMs accounted for 44% and 24%, respectively. Overall, 33% of patients worsened but outcomes did not significantly differ by SM III subtype. Neurological outcomes were associated with Supp-SM grade, with proportions of patients with worsening increasing from 0% with Supp-SM grade 4 AVMs to 54% with Supp-SM grade 7 AVMs. Analyses of factors associated with neurological worsening identified age > 60 yr and Supp-SM grade 7 as significant. CONCLUSION: Supp-SM grades were more predictive of microsurgical outcomes than modified SM grades for grade III AVMs, with a hard cutoff for acceptable surgical risk at Supp-SM grade 6. Supp-SM grading is a better decision-making tool than subtyping with the modified SM scale.

Modern radiosurgical and endovascular classification schemes for brain arteriovenous malformations.

Stereotactic radiosurgery (SRS) and endovascular techniques are commonly used for treating brain arteriovenous malformations (bAVMs). They are usually used as ancillary techniques to microsurgery but may also be used as solitary treatment options. Careful patient selection requires a clear estimate of the treatment efficacy and complication rates for the individual patient. As such, classification schemes are an essential part of patient selection paradigm for each treatment modality. While the Spetzler-Martin grading system and its subsequent modifications are commonly used for microsurgical outcome prediction for bAVMs, the same system(s) may not be easily applicable to SRS and endovascular therapy. Several radiosurgical- and endovascular-based grading scales have been proposed for bAVMs. However, a comprehensive review of these systems including a discussion on their relative advantages and disadvantages is missing. This paper is dedicated to modern classification schemes designed for SRS and endovascular techniques.

Transdural Blood Supply in Cerebral Arteriovenous Malformations: A Systematic Evaluation of Angioarchitecture.

BACKGROUND AND PURPOSE: Arterial transdural blood supply is a rare angiographic phenomenon in cerebral AVMs. This study aimed to evaluate angiographic transdural blood supply characteristics and to describe the clinical peculiarities of these lesions. MATERIALS AND METHODS: A prospective AVM data base of 535 patients, enrolled from 1990 to 2016, was analyzed retrospectively. Clinical information was reviewed through patients' medical charts and radiologic studies. Patients with previous AVM treatment were excluded (n = 28). RESULTS: Patients with (n = 32, male/female ratio = 10:22; mean age, 46 ± 15 years; range, 13-75 years) and without transdural blood supply (n = 475, male/female ratio = 260:215; mean age, 40 ± 18 years; range, 2-87 years) did not show significant differences in clinical presentation (age, hemorrhage, seizures, chronic headache). The predominant nidus size in patients with transdural blood supply was ≥30 mm, with significantly more patients with large AVMs (>60 mm, P = .001). To describe the transdural blood supply, we used 3 grades based on the angiographic transdural blood supply proportion and intensity of AVM nidus perfusion (I-III). Fifty-seven percent of patients with chronic headache had a strong and substantial transdural nidus perfusion (III) and a high-flow transdural blood supply. CONCLUSIONS: Cerebral AVMs with transdural blood supply represent a rare and heterogeneous subgroup. Lesions can be graded by quantifying the transdural blood supply of the nidus and by capturing hemodynamic characteristics. The broad spread of angiographic features and comparable clinical patterns of patients with or without transdural blood supply raises questions about the relevance of the transdural blood supply to the natural history risk of an AVM and the intention for treatment.

Gamma knife radiosurgery for arteriovenous malformations: general principles and preliminary results in a Swiss cohort.

INTRODUCTION: Arteriovenous malformations (AVMs) are a type of vascular malformation characterised by an abnormal connection between arteries and veins, bypassing the capillary system. This absence of capillaries generates an elevated pressure (hyperdebit), in both the AVM and the venous drainage, increasing the risk of rupture. Management modalities are: observation, microsurgical clipping, endovascular treatment and radiosurgery. The former can be used alone or in the frame of a multidisciplinary approach. We review our single-institution experience with gamma knife radiosurgery (GKR) over a period of 5 years. MATERIALS AND METHODS: The study was open-label, prospective and nonrandomised. Fifty-seven consecutive patients, benefitting from 64 GKR treatments, were included. All were treated with Leksell Gamma Knife Perfexion (Elekta Instruments, AB, Sweden) between July 2010 and August 2015. All underwent stereotactic multimodal imaging: standard digital subtraction angiography, magnetic resonance imaging and computed tomography angiography. We report obliteration rates, radiation-induced complications and haemorrhages during follow-up course. RESULTS: The mean age was 46 years (range 13-79 years). The mean follow-up period was 36.4 months (median 38, range 12-75 months). Most common pretherapeutic clinical presentation was haemorrhage (50%). The most common Pollock-Flickinger score was between 1.01 and 1.5 (46%) and Spetzler-Martin grade III (46%). In 39 (60.1%) of cases, GKR was performed as upfront therapeutic option. The mean gross target volume (GTV) was 2.3 ml (median 1.2, range 0.03-11.3 ml). Mean marginal dose was 22.4 Gy (median 24, range 18-24 Gy). The mean prescription isodose volume (PIV) was 2.9 ml (median 1.8, range 0.065-14.6 ml). The overall obliteration rates (all treatments combined) at 12, 24, 36, 48 and 60 months were 4.8, 16.9%, 37.4, 63.6 and 78.4%, respectively. The main predictive factors for complete obliteration were: higher mean marginal dose (23.3 vs 21.0 Gy), lower GTV (mean 1.5 vs 3.5 ml) and absence of previous embolisation (at 60 months 61.8% prior embolisation compared with 82.4% without prior embolisation) (for all p <0.05). Eight (14%) patients experienced complications after GKR. Overall definitive morbidity rate was 3.1%. No patient died from causes related to GKR. However, during the obliteration period, one case of extremely rare fatal haemorrhage occurred. CONCLUSION: Radiosurgery is a safe and effective treatment modality for intracranial AVMs in selected cases. It can be used as upfront therapy or in the frame of a combined management. Obliteration rates are high, with minimal morbidity. The treatment effect is progressive and subsequent and regular clinical and radiological follow-up is needed to evaluate this effect.

Modern classification and outcome predictors of surgery in patients with brain arteriovenous malformations.

Brain arteriovenous malformations (bAVM) are challenging lesions. Part of this challenge stems from the infinite diversity of these lesions regarding shape, location, anatomy, and physiology. This diversity has called on a variety of treatment modalities for these lesions, of which microsurgical resection prevails as the mainstay of treatment. As such, outcome prediction and managing strategy mainly rely on unraveling the nature of these complex tangles and ways each lesion responds to various therapeutic modalities. This strategy needs the ability to decipher each lesion through accurate and efficient categorization. Therefore, classification schemes are essential parts of treatment planning and outcome prediction. This article summarizes different surgical classification schemes and outcome predictors proposed for bAVMs.

Stereotactic radiosurgery for Spetzler-Martin Grade IV and V arteriovenous malformations: an international multicenter study.

OBJECTIVE Due to the complexity of Spetzler-Martin (SM) Grade IV-V arteriovenous malformations (AVMs), the management of these lesions remains controversial. The aims of this multicenter, retrospective cohort study were to evaluate the outcomes after single-session stereotactic radiosurgery (SRS) for SM Grade IV-V AVMs and determine predictive factors. METHODS The authors retrospectively pooled data from 233 patients (mean age 33 years) with SM Grade IV (94.4%) or V AVMs (5.6%) treated with single-session SRS at 8 participating centers in the International Gamma Knife Research Foundation. Pre-SRS embolization was performed in 71 AVMs (30.5%). The mean nidus volume, SRS margin dose, and follow-up duration were 9.7 cm3, 17.3 Gy, and 84.5 months, respectively. Statistical analyses were performed to identify factors associated with post-SRS outcomes. RESULTS At a mean follow-up interval of 84.5 months, favorable outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RIC) and was achieved in 26.2% of patients. The actuarial obliteration rates at 3, 7, 10, and 12 years were 15%, 34%, 37%, and 42%, respectively. The annual post-SRS hemorrhage rate was 3.0%. Symptomatic and permanent RIC occurred in 10.7% and 4% of the patients, respectively. Only larger AVM diameter (p = 0.04) was found to be an independent predictor of unfavorable outcome in the multivariate logistic regression analysis. The rate of favorable outcome was significantly lower for unruptured SM Grade IV-V AVMs compared with ruptured ones (p = 0.042). Prior embolization was a negative independent predictor of AVM obliteration (p = 0.024) and radiologically evident RIC (p = 0.05) in the respective multivariate analyses. CONCLUSIONS In this multi-institutional study, single-session SRS had limited efficacy in the management of SM Grade IV-V AVMs. Favorable outcome was only achieved in a minority of unruptured SM Grade IV-V AVMs, which supports less frequent utilization of SRS for the management of these lesions. A volume-staged SRS approach for large AVMs represents an alternative approach for high-grade AVMs, but it requires further investigation.

A proposed grading system to evaluate the endovascular curability of deep-seated arteriovenous malformations.

BACKGROUND: Aggressive treatment of deep-seated AVMs is paramount because of their high tendency to bleed (or to re-bleed). In the literature concerning endovascular therapy, AVMs of the basal ganglia, the semi-ovale center and the midbrain are always considered as a single entity. In this study, the authors address the anatomical classification of these AVMs and propose a classification that considers factors influencing their endovascular curability. METHODS: From 1995 to 2013, clinical and angiographic data of cerebral AVMs were prospectively collected. We reviewed data from patients treated for a deep-seated AVM with the goal to distinguish factors that influence the curability and the outcome of these AVMs. RESULTS: 134 patients (mean age: 28years) were consecutively treated by endovascular techniques. We describe an anatomical classification concerning the exact location of the nidus and distinguish 5 different sub-types (anterior, lateral, medial, posterior and midbrain). Then, we propose a grading system based on statistical analysis of our series to evaluate the curability of a deep AVM. This comprehensive score is calculated with the Spetzler-Martin grade, the location of the nidus, its type, arterial feeders and venous drainage. CONCLUSIONS: Deep-seated AVMs may be classified according to their exact location; we can distinguish 5 different sub-types (anterior, lateral, medial, posterior and midbrain). Each group presented different arterial supplies and venous drainage that influenced treatment possibilities. The comprehensive grading system that we propose in this study must be tested in another deep-seated AVMs population.

Epidemiology, genetics, pathophysiology, and prognostic classifications of cerebral arteriovenous malformations.

Arteriovenous malformations (AVMs) are vascular deformities involving fistula formation of arterial to venous structures without an intervening capillary bed. Such anomalies can prove fatal as the high arterial flow can disrupt the integrity of venous walls, thus leading to dangerous sequelae such as hemorrhage. Diagnosis of these lesions in the central nervous system can often prove challenging as intracranial AVMs represent a heterogeneous vascular pathology with various presentations and symptomatology. The literature suggests that most brain AVMs (bAVMs) are identified following evaluation of the etiology of acute cerebral hemorrhage, or incidentally on imaging associated with seizure or headache workup. Given the low incidence of this disease, most of the data accrued on this pathology comes from single-center experiences. This chapter aims to distill the most important information from these studies as well as examine meta-analyses on bAVMs in order to provide a comprehensive introduction into the natural history, classification, genetic underpinnings of disease, and proposed pathophysiology. While there is yet much to be elucidated about AVMs of the central nervous system, we aim to provide an overview of bAVM etiology, classification, genetics, and pathophysiology inherent to the disease process.

Multimodality Management of Spetzler-Martin Grade 3 Brain Arteriovenous Malformations with Subgroup Analysis.

OBJECTIVE: Spetzler-Martin grade 3 (SM3) lesions entail 4 distinct subtypes described based on size, eloquence, and deep venous drainage (3A-3D). The ideal management of each is contentious, and the results of A Randomized Trial of Unruptured Brain AVMs (ARUBA) introduced additional controversy and attention toward management strategies of unruptured brain arteriovenous malformations (bAVMs). METHODS: We retrospectively reviewed 114 patients with treated SM3 bAVMs, including both ruptured and unruptured lesions. Primary outcomes included modified Rankin score at most recent follow-up, angiographic cure, and permanent treatment-related complications (morbidity). Other outcomes included mortality, bAVM recurrence or rebleed, and transient treatment-related complications. We used univariate and multivariate modeling to determine whether any specific features were predictive of outcomes. For unruptured bAVMs, an "ARUBA eligible" subgroup analysis was performed. We also reviewed the literature on management of ruptured and unruptured SM3 bAVMs. RESULTS: Of the 114 identified SM3 bAVMs, 40% were unruptured. Most (43.5%) lesions in the unruptured group were type 3C, whereas most ruptured bAVMs (66.2%) were type 3A. Unruptured lesions were mostly managed with radiosurgery (47.8%) and ruptured ones with preoperative embolization and surgery (36.7%). Surgical intervention was predictive of angiographic cure in multivariate modeling, even after controlling for ≥2 years of follow-up, although associated with a slightly higher rate of morbidity. Focal neurological deficit was the only predictor of a worse (modified Rankin score ≥2) functional outcome in follow-up for unruptured bAVMs. For ruptured bAVMs, superficial and cerebellar locations were predictive of better outcomes in multivariate models, in the absence of a focal neurological deficit at presentation and new after surgery deficit. ARUBA SM3 bAVMs specifically underwent more embolization as a monotherapy and less microsurgical resection than the present series. CONCLUSIONS: In spite of a heterogeneous array of angioarchitectural and anatomic features, SM3 bAVMs can be treated safely and effectively with surgery and radiosurgery either without or with pretreatment embolization. Ruptured lesions are more often type 3A, with smaller nidus, deep brain location, and deep venous drainage. Focal neurological deficit predicts worse clinical outcomes. Contemporary multimodality management of SM3 bAVMs is not adequately represented in the results of ARUBA, likely due to differences in treatment strategies.

Arterial aneurysms associated with arteriovenous malformations of the brain: classification, incidence, risk of hemorrhage, and treatment-a systematic review.

BACKGROUND: Aneurysms associated with brain arteriovenous malformations (bAVMs) influence the natural history of these lesions and pose important therapeutic challenges. However, the epidemiology, natural history, and appropriate management of the aneurysms associated with bAVMs are not completely understood due to the paucity of large and uniform studies. We performed a systematic review of published series examining the association between aneurysms and bAVMs with the purpose of clarifying the prevalence, risk of hemorrhage, and appropriate management of these lesions. METHOD: PRISMA/MOOSE guidelines were followed. We conducted a comprehensive literature search of three databases (PubMed, Ovid MEDLINE, and Ovid EMBASE) on aneurysms associated with bAVMs. Only studies examining consecutive case series of aneurysms associated with bAVMs were included. From the collected studies, we extracted data regarding prevalence of bAVM-associated aneurysms, risk of aneurysm rupture in relation to bAVM location and aneurysm characteristics, and treatment-related outcomes. RESULTS: Our systematic review included 44 articles with a total of 10,093 bAVMs. The proportion of bAVMs with an associated aneurysm was 20.2 % (95 % CI = 19.4-20.9 %). Among ruptured bAVMs with associated aneurysms, the aneurysm was the source of hemorrhage in 49.2 % (95 % CI = 43.7-54.7 %) of cases. Flow-related aneurysms were the most common source of aneurysm rupture (78.5 %, 95 % CI = 70.6-84.9 %). Infratentorial bAVM-associated aneurysms presented a higher risk of rupture (60 %, 95 % CI = 47.4-71.9 %) when compared with supratentorial lesions (29 %, 95 % CI = 21.4-38.5 %). Endovascular treatment of aneurysms associated with bAVMs had a cure rate of 80.0 % (95 % CI = 73.3-85.3 %), complication rate of 8.7 % (95 % CI = 5.5-13.1 %), and a good neurological outcome rate of 78.8 % (95 % CI = 72.5-83.9 %). CONCLUSIONS: Twenty percent of bAVMs harbored arterial aneurysms. The presence of aneurysm increases the risk of bleeding of the bAVM, especially when flow-related or infratentorially located. Aneurysms associated with bAVMs should be treated promptly. Selective endovascular treatment of bAVM-associated aneurysms appears safe and effective.

De novo development of a cerebral arteriovenous malformation following radiation therapy: Case report and an update to classical arteriovenous malformation nomenclature.

Cerebral arteriovenous malformations (AVM) are traditionally considered primary congenital lesions that result from embryological aberrations in vasculogenesis. Recent insights, however, suggest that these lesions may be secondary to a vascular insult such as ischemia or trauma. Herein, the authors present a rare case of a secondary cerebral AVM, occurring in a young girl who received prior cranial radiation therapy. At age 3years, she underwent surgical resection, chemotherapy, and photon radiation therapy for treatment of a fourth ventricular ependymoma. At age 19years, she developed new onset seizures and was found to have a left medial temporal lobe AVM. Her seizures were managed successfully with anti-epileptic medications and the AVM was treated with proton radiation therapy. This case highlights a rare but possible vascular sequela of radiation therapy and adds to the growing body of evidence that cerebral AVM may arise as secondary lesions.

SLAM: Stereotactic Radiosurgery of Large Arteriovenous Malformations: Meta-analysis of Hemorrhage in High-Grade Pollock-Flickinger Arteriovenous Malformations.

BACKGROUND: The prognosis of arteriovenous malformations (AVMs) after treatment has been predicted largely by 2 grading scales: the Spetzler-Martin and Pollock-Flickinger. Although there are studies that examine the rate of hemorrhage with the Spetzler-Martin scale, there have not been studies examining hemorrhage in which the Pollock-Flickinger score was used. The annual hemorrhage rate after radiosurgery of Pollock-Flickinger AVM scores >2 is analyzed. METHODS: Literature search for radiosurgery of large AVMs from January 1, 2000 to June 1, 2014 was conducted. Articles were examined for individual patient data and aggregate patient data that reported hemorrhage rates and mortality. Patients were only included if they had an AVM score ≥2. RESULTS: Annual AVM hemorrhage rate after radiosurgery for all patients (n = 673) was 3.22% (99.3 hemorrhages, 3080.5 follow-up years, 95% confidence interval [95% CI] 2.64%-3.89%). Mortality rate from hemorrhage was 40.08% (95% CI 31.21%-49.90%). A total of 203 patients presented with hemorrhage and 395 did not. In patients with first-time hemorrhage, the annual hemorrhage rate was 3.53% (95% CI 2.66%-4.77%). The annual hemorrhage rate of those with hemorrhagic presentation was 6.10% (95% CI 4.65%-8.07%). The odds ratio comparing re-hemorrhage rate versus first-time hemorrhage is 1.768 (95% CI 1.1571-2.7014, P = 0.0084). Complete obliteration of all AVMs was equal to 33.27% (95% CI, 29.25%-37.54%). CONCLUSIONS: The annual hemorrhage rate in AVMs with scores >2 treated with radiosurgery was comparable with baseline rupture rates reported for untreated AVMs. With further stratification by hemorrhagic versus nonhemorrhagic presentation, the subsequent annual hemorrhage rates are similar to their respective natural histories. Considering the mortality rate from hemorrhage at 40.08% (95% CI, 35.54%-44.62%), the consequences of radiosurgical treatment of large AVMs is significantly worse than the reported 10%-30% fatality rate from hemorrhage of an untreated AVM. Additionally, the overall mortality rate was 6.24% however the percentage of mortalities from hemorrhage was 97.62%.

Prospective Hemorrhage Rates of Cerebral Cavernous Malformations in Children and Adolescents Based on MRI Appearance.

BACKGROUND AND PURPOSE: Current classifications of cerebral cavernous malformations focus solely on morphologic aspects. Our aim was to provide a morphologic classification that reflects hemorrhage rates. MATERIALS AND METHODS: We retrospectively categorized 355 cavernous malformations of 70 children and adolescents according to their morphologic appearance on MR imaging and calculated prospective hemorrhage rates on the basis of survival functions for 255 lesions in 25 patients with a radiologic observation period of >180 days. RESULTS: Overall, there were 199 MR imaging examinations with 1558 distinct cavernous malformation observations during a cumulative observation period of 1094.2 lesion-years. The mean hemorrhage rate of all 355 cavernous malformations was 4.5% per lesion-year. According to Kaplan-Meier survival models, Zabramski type I and II cavernous malformations had a significantly higher hemorrhage rate than type III and IV lesions. The presence of acute or subacute blood-degradation products was the strongest indicator for an increased hemorrhage risk (P = .036, Cox regression): The mean annual hemorrhage rate and mean hemorrhage-free interval for cavernous malformations with and without signs of acute or subacute blood degradation products were 23.4% and 22.6 months and 3.4% and 27.9 months, respectively. Dot-sized cavernous malformations, visible in T2* and not or barely visible in T1WI and T2WI sequences, had a mean annual hemorrhage rate of 1.3% and a mean hemorrhage-free interval of 37.8 months. CONCLUSIONS: It is possible to predict hemorrhage rates based on the Zabramski classification. Our findings imply a tripartite classification distinguishing lesions with and without acute or subacute blood degradation products and dot-sized cavernous malformations.

Evaluation of 4D vascular flow and tissue perfusion in cerebral arteriovenous malformations: influence of Spetzler-Martin grade, clinical presentation, and AVM risk factors.

BACKGROUND AND PURPOSE: The role of intracranial hemodynamics in the pathophysiology and risk stratification of brain AVMs remains poorly understood. The purpose of this study was to assess the influence of Spetzler-Martin grade, clinical history, and risk factors on vascular flow and tissue perfusion in cerebral AVMs. MATERIALS AND METHODS: 4D flow and perfusion MR imaging was performed in 17 patients with AVMs. Peak velocity and blood flow were quantified in AVM feeding and contralateral arteries, draining veins, and the straight sinus. Regional perfusion ratios (CBF, CBV, and MTT) were calculated between affected and nonaffected hemispheres. RESULTS: Regarding flow parameters, high-grade AVMs (Spetzler-Martin grade of >2) demonstrated significantly increased peak velocity and blood flow in the major feeding arteries (P < .001 and P = .004) and straight sinus (P = .003 and P = .012) and increased venous draining flow (P = .001). The Spetzler-Martin grade significantly correlated with cumulative feeding artery flow (r = 0.85, P < .001) and draining vein flow (r = 0.80, P < .001). Regarding perfusion parameters, perinidal CBF and CBV ratios were significantly lower (P < .001) compared with the remote ratios and correlated negatively with cumulative feeding artery flow (r = -0.60, P = .014 and r = -0.55, P = .026) and draining vein flow (r = -0.60, P = .013 and r = -0.56, P = .025). Multiple regression analysis revealed no significant association of AVM flow or perfusion parameters with clinical presentation (rupture and seizure history) and AVM risk factors. CONCLUSIONS: Macrovascular flow was significantly associated with increasing Spetzler-Martin grade and correlated with perinidal microvascular perfusion in cerebral AVMs. Future longitudinal studies are needed to evaluate the potential of comprehensive cerebral flow and perfusion MR imaging for AVM risk stratification.

A treatment paradigm for high-grade brain arteriovenous malformations: volume-staged radiosurgical downgrading followed by microsurgical resection.

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.

Brainstem arteriovenous malformations: anatomical subtypes, assessment of "occlusion in situ" technique, and microsurgical results.

OBJECT: The surgical management of brainstem arteriovenous malformations (AVMs) might benefit from the definition of anatomical subtypes and refinements of resection techniques. Many brainstem AVMs sit extrinsically on pia mater rather than intrinsically in the parenchyma, allowing treatment by occluding feeding arteries circumferentially, interrupting draining veins after arteriovenous shunting is eliminated, and leaving the obliterated nidus behind. The authors report here the largest series of brainstem AVMs to define 6 subtypes, assess this "occlusion in situ" technique, and analyze the microsurgical results. METHODS: Brainstem AVMs were categorized as 1 of 6 types: anterior midbrain, posterior midbrain, anterior pontine, lateral pontine, anterior medullary, and lateral medullary AVMs. Data from a prospectively maintained AVM registry were reviewed to evaluate multidisciplinary treatment results. RESULTS: During a 15-year period, the authors treated 29 patients with brainstem AVMs located in the midbrain (1 anterior and 6 posterior), pons (6 anterior and 7 lateral), and medulla (1 anterior and 8 lateral). The nidus was pial in 26 cases and parenchymal in 3 cases. Twenty-three patients (79%) presented with hemorrhage. Brainstem AVMs were either resected (18 patients, 62%) or occluded in situ (11 patients, 38%). All lateral pontine AVMs were resected, and the occlusion in situ rate was highest with anterior pontine AVMs (83%). Angiography confirmed complete obliteration in 26 patients (89.6%). The surgical mortality rate was 6.9%, and the rate of permanent neurological deterioration was 13.8%. At follow-up (mean 1.3 years), good outcomes (modified Rankin Scale [mRS] score ≤ 2) were observed in 18 patients (66.7%) and poor outcomes (mRS score of 3-5) were observed in 9 patients (33.3%). The mRS scores in 21 patients (77.8%) were unchanged or improved. The best outcomes were observed with lateral pontine (100%) and lateral medullary (75%) AVMs, and the rate of worsening/death was greatest with posterior midbrain and anterior pontine AVMs (50% each). CONCLUSIONS: Brainstem AVMs can be differentiated by their location in the brainstem (midbrain, pons, or medulla) and the surface on which they are based (anterior, posterior, or lateral). Anatomical subtypes can help the neurosurgeon determine how to advise patients, with lateral subtypes being a favorable surgical indication along with extrinsic pial location and hemorrhagic presentation. Most AVMs are dissected with the intention to resect them, and occlusion in situ is reserved for those AVMs that do not separate cleanly from the brainstem, that penetrate into the parenchyma, or are more anterior in location, where it is difficult to visualize and preserve perforating arteries (anterior pontine and lateral medullary AVMs). Although surgical morbidity is considerable, surgery results in a better obliteration rate than nonoperative management and is indicated in highly selected patients with high rerupture risks.

Surgical outcomes after classifying Grade III arteriovenous malformations according to Lawton's modified Spetzler-Martin grading system.

OBJECTIVE: We aimed to evaluate microsurgical outcomes after classifying Grade III arteriovenous malformations (AVMs) according to Lawton's modified Spetzler-Martin grading system. METHODS: Of 131 patients with Grade III AVMs, 55 had undergone microsurgery between 1995 and 2010. The 55 AVMs were classified as follows: Grade III-/S1E1V1, Grade III/S2E0V1, Grade III+/S2E1V0, or Grade III*/S3E0V0. The surgical obliteration rate, morbidity rate, and functional outcomes for each subtype were compared before surgery and after follow-up. Additionally, factors related with morbidity were investigated from demographic and morphological characteristics. RESULTS: We observed 18 Grade III-, 16 Grade III, 20 Grade III+, and 1 Grade III* AVMs. Complete resection was achieved in 49 patients (obliteration rate, 89.1%). Incomplete resection rates were higher for Grade III (12.5%) and III+ (15.0%) AVMs than that for Grade III- (5.6%) AVMs. Seven patients (12.7%) presented postoperative deficits, of which 3 (5.4%) experienced disabilities. Patients with Grade III+ (25.0%) had higher morbidity rates than those with other subtypes. Modified Rankin scale scores at the last follow-up indicated unfavorable outcomes for Grades III (18.8%) and III+ (25.0%) AVMs. AVM size (≥3 cm) and non-hemorrhagic type were associated with the occurrence of postoperative deficits (p<0.05). CONCLUSION: The modified classification of Grade III AVMs was useful to predict surgical morbidity and clinical outcomes. We recommend that microsurgery should be used to treat Grade III- AVMs, but should be considered carefully for the treatment of Grades III and III+.