Silent Arteriovenous Malformation Hemorrhage and the Recognition of “Unruptured” Arteriovenous Malformation Patients Who Benefit From Surgical Intervention

Silent Arteriovenous Malformation Hemorrhage and the Recognition of “Unruptured” Arteriovenous Malformation Patients Who Benefit From Surgical Intervention

Neurosurgery 76:592–600, 201

Arteriovenous malformation (AVM) patients present in 4 ways relative to hemorrhage: (1) unruptured, without a history or radiographic evidence of old hemorrhage (EOOH); (2) silent hemorrhage, without a bleeding history but with EOOH; (3) ruptured, with acute bleeding but without EOOH; and (4) reruptured, with acute bleeding and EOOH. OBJECTIVE: We hypothesized that characteristics and outcomes in the unrecognized group of silent hemorrhage patients may differ from those of unruptured patients.

METHODS: Two hundred forty-two patients operated-on since 1997 were categorized by hemorrhage status and hemosiderin positivity in this cohort study: unruptured (group 1), silent hemorrhage (group 2), and ruptured/reruptured (group 3/4). Group 3/4 was combined because hemosiderin cannot distinguish acute hemorrhage from older silent hemorrhage.

RESULTS: Hemosiderin was found in 45% of specimens. Seventy-five patients (31.0%) had unruptured AVMs, 30 (12.4%) had silent hemorrhage, and 137 (56.6%) had ruptured/ reruptured AVMs. Deep drainage, posterior fossa location, preoperative modified Rankin Scale (mRS) score, outcome, and macrophage score were different across groups. Only the macrophage score was different between the groups without clinical hemorrhage. Outcomes were better in silent hemorrhage patients than in those with frank rupture (mean mRS scores of 1.2 and 1.7, respectively).

CONCLUSION: One-third of patients present with silent AVM hemorrhage. No clinical or anatomic features differentiate these patients from unruptured patients, except the presence of hemosiderin and macrophages. Silent hemorrhage can be diagnosed using magnetic resonance imaging with iron-sensitive imaging. Silent hemorrhage portends an aggressive natural history, and surgery halts progression to rerupture. Good final mRS outcomes and better outcomes than in those with frank rupture support surgery for silent hemorrhage patients, despite the findings of ARUBA.

Current surgical results with low-grade brain arteriovenous malformations

Low-grade brain arteriovenous malformations

J Neurosurg 122:912–920, 2015

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.

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

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

J Neurosurg 122:419–432, 2015

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 highgrade 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.

Validation of the Supplemented Spetzler-Martin Grading System for Brain Arteriovenous Malformations in a Multicenter Cohort of 1009 Surgical Patients

AVM

Neurosurgery 76:25–33, 2015

The supplementary grading system for brain arteriovenous malformations (AVMs) was introduced in 2010 as a tool for improving preoperative risk prediction and selecting surgical patients.

OBJECTIVE: To demonstrate in this multicenter validation study that supplemented Spetzler-Martin (SM-Supp) grades have greater predictive accuracy than Spetzler-Martin (SM) grades alone.

METHODS: Data collected from 1009 AVM patients who underwent AVM resection were used to compare the predictive powers of SM and SM-Supp grades. Patients included the original 300 University of California, San Francisco patients plus those treated thereafter (n = 117) and an additional 592 patients from 3 other centers.

RESULTS: In the combined cohort, the SM-Supp system performed better than SM system alone: area under the receiver-operating characteristics curve (AUROC) = 0.75 (95% confidence interval, 0.71-0.78) for SM-Supp and AUROC = 0.69 (95% confidence interval, 0.65-0.73) for SM (P , .001). Stratified analysis fitting models within 3 different follow-up groupings (,6 months, 6 months-2 years, and .2 years) demonstrated that the SM-Supp system performed better than SM system for both medium (AUROC = 0.71 vs 0.62; P = .003) and long (AUROC = 0.69 vs 0.58; P = .001) follow-up. Patients with SMSupp grades #6 had acceptably low surgical risks (0%-24%), with a significant increase in risk for grades .6 (39%-63%).

CONCLUSION: This study validates the predictive accuracy of the SM-Supp system in a multicenter cohort. An SM-Supp grade of 6 is a cutoff or boundary for AVM operability. Supplemented grading is currently the best method of estimating neurological outcomes after AVM surgery, and we recommend it as a starting point in the evaluation of AVM operability.

Management of perisylvian arteriovenous malformations

Management of perisylvian arteriovenous malformations

Neurosurg Focus 37 (3):E13, 2014

Sylvian arteriovenous malformations (sAVMs) are challenging lesions of the central nervous system. The natural history of these unique lesions as well as clinical outcomes following treatment of sAVMs has been limited to case series owing to the rarity of these lesions. The authors present their experience with sAVMs and review the literature.

Methods. In accordance with the Henry Ford Institutional Review Board, medical records of patients with sAVMs treated from 2000 to 2012 were reviewed. Clinical data were retrospectively collected to calculate pre- and posttreatment modified Rankin Scale scores for all patients.

Results. The authors identified 15 patients with sAVMs who received treatment. Of these, 12 were female and 3 were male, and the average age at presentation was 39.6 ± 12.94 years (± SD). Two patients (13.3%) had Spetzler- Martin Grade I lesions, 6 patients (40%) had Grade II lesions, 5 patients (33.3%) had Grade III lesions, and another 2 (13.3%) harbored Grade IV arteriovenous malformations (AVMs). According to the Sugita classification, 6 patients (40%) had medial lesions, 6 (40%) had lateral lesions, 2 (13.3%) had deep lesions, and 1 patient (6.67%) had a pure sAVM. Eight patients (53.3%) underwent stereotactic radiosurgery while 7 patients (46.7%) had microsurgical resection; 1 patient underwent surgical extirpation after incomplete response following radiosurgery. After treatment, 9 patients were unchanged from pretreatment (60%), 3 patients worsened, and 2 patients had improved functional outcome (20% and 13.3%, respectively). The authors’ literature search yielded 348 patients with sAVMs, most of them harboring Spetzler-Martin Grade II and III lesions. Approximately 98% of the patients underwent resection with excellent outcomes.

Conclusions. While the ideal choice of therapeutic modality for cerebral AVMs remains controversial in light of the recent publication of the ARUBA (A Randomized trial of Unruptured Brain AVMs) trial, a multidisciplinary treatment approach for the management of sAVMs can lead to acceptable neurological outcome.

Microsurgery for cerebral arteriovenous malformations: postoperative outcomes and predictors of complications in 264 cases

AVM PF

Neurosurg Focus 37 (3):E10, 2014

The authors conducted a study to assess the safety and efficacy of microsurgical resection of arteriovenous malformations (AVMs) and determine predictors of complications.

Methods. A total of 264 patients with cerebral AVMs were treated with microsurgical resection between 1994 and 2010 at the Jefferson Hospital for Neuroscience. A review of patient data was performed, including initial hemorrhage, clinical presentation, Spetzler-Martin (SM) grade, treatment modalities, clinical outcomes, and obliteration rates. Univariate and multivariate analyses were used to determine predictors of operative complications.

Results. Of the 264 patients treated with microsurgery, 120 (45%) patients initially presented with hemorrhage. There were 27 SM Grade I lesions (10.2%), 101 Grade II lesions (38.3%), 96 Grade III lesions (36.4%), 31 Grade IV lesions (11.7%), and 9 Grade V lesions (3.4%). Among these patients, 102 (38.6%) had undergone prior endovascular embolization. In all patients, resection resulted in complete obliteration of the AVM. Complications occurred in 19 (7.2%) patients and resulted in permanent neurological deficits in 5 (1.9%). In multivariate analysis, predictors of complications were increasing AVM size (OR 3.2, 95% CI 1.5–6.6; p = 0.001), increasing number of embolizations (OR 1.6, 95% CI 1.1–2.2; p = 0.01), and unruptured AVMs (OR 2.7, 95% CI 1–7.2; p = 0.05).

Conclusions. Microsurgical resection of AVMs is highly efficient and can be undertaken with low rates of morbidity at high-volume neurovascular centers. Unruptured and larger AVMs were associated with higher complication rates.

Computational Fractal-Based Analysis of Brain Arteriovenous Malformation Angioarchitecture

Computational Fractal-Based Analysis of Brain Arteriovenous Malformation Angioarchitecture

Neurosurgery 75:72–79, 2014

Neuroimaging is the gold standard for diagnosis and follow-up of brain arteriovenous malformations (bAVMs), but no objective parameter has been validated for the assessment of the nidus angioarchitecture and for prognostication following treatment. The fractal dimension (FD), which is a mathematical parameter able to quantify the space-filling properties and roughness of natural objects, may be useful in quantifying the geometrical complexity of bAVMs nidus.

OBJECTIVE: To propose FD as a neuroimaging biomarker of the nidus angioarchitecture, which might be related to radiosurgical outcome.

METHODS: We retrospectively analyzed 54 patients who had undergone stereotactic radiosurgery for the treatment of bAVMs. The quantification of the geometric complexity of the vessels forming the nidus, imaged in magnetic resonance imaging, was assessed by means of the box-counting method to obtain the fractal dimension.

RESULTS: FD was found to be significantly associated with the size (P = .03) and volume (P , .001) of the nidus, in addition to several angioarchitectural parameters. A nonsignificant association between clinical outcome and FD was observed (area under the curve, 0.637 [95% confidence interval, 0.49-0.79]), indicative of a potential inverse relationship between FD and bAVM obliteration.

CONCLUSION: In our exploratory methodological research, we showed that the FD is an objective computer-aided parameter for quantifying the geometrical complexity and roughness of the bAVM nidus. The results suggest that more complex bAVM angioarchitecture, having higher FD values, might be related to decreased response to radiosurgery and that the FD of the bAVM nidus could be used as a morphometric neuroimaging biomarker.

Indocyanine Green Angiography in the Surgical Management of Cerebral Arteriovenous Malformations

Indocyanine Green Angiography in the Surgical Management of Cerebral Arteriovenous Malformations

Operative Neurosurgery 10:246–251, 2014

Indocyanine green (ICG) angiography is commonly used to map the vascular configuration of cerebral arteriovenous malformations (AVMs) during resection.

OBJECTIVE: To determine whether ICG improves rates of resection and clinical outcomes.

METHODS: A retrospective chart review was done for all patients undergoing resection of an AVM by the senior author (R.F.S.) between 2007 and 2011. Operative reports, hospital records, and radiographic imaging were used to determine the use of ICG, the incidence of residual disease, and clinical outcomes.

RESULTS: A total of 130 cases (56 ICG, 74 non-ICG) were identified. Average AVM grade (2.2 vs 2.4) and size (2.7 vs 2.7 cm) were similar between the ICG and non-ICG groups, respectively. ICG was more often used when the AVM nidus was close to the cortical surface (71.4% vs 17.6%; P = .001) or lobar (82.1% vs 54.1%; P = .008). Eighteen patients (13.8%) were noted to have residual disease. Reoperation rates and change in modified Rankin Scale score were not different between the 2 groups (12.5% vs 14.9%, P = .8; 0.6 vs 0.4, P = .17). There were no ICG-attributable complications.

CONCLUSION: ICG videoangiography is a quick and safe method of intraoperatively mapping the angioarchitecture of superficial AVMs, but it is less helpful for deep-seated lesions. This modality alone does not improve the identification of residual disease or clinical outcomes. Surgeon experience with extensive study of preoperative vascular imaging is paramount to achieving acceptable clinical outcomes. Formal angiography remains the gold standard for the evaluation of AVM obliteration.

Stereotactic radiosurgery for Spetzler-Martin Grade III arteriovenous malformations

Spetzler-Martin grade III AVMs

J Neurosurg 120:973–981, 2014

The purpose of this study was to define the outcomes and risks of stereotactic radiosurgery (SRS) for Spetzler-Martin (SM) Grade III arteriovenous malformations (AVMs).

Methods. Between 1987 and 2009, SRS was performed in 474 patients with SM Grade III AVMs. The AVMs were categorized by scoring the size (S), drainage (D), and location (L): IIIa was a small AVM (S1D1L1, N = 282); IIIb was a medium/deep AVM (S2D1L0, N = 44); and IIIc was a medium/eloquent AVM (S2D0L1, N = 148). The median target volume was 3.8 ml (range 0.1–26.3 ml) and the margin dose was 20 Gy (range 13–25 Gy). Eighty-one patients (17%) underwent prior embolization, and 58 (12%) underwent prior resection.

Results. At a mean follow-up of 89 months, the total obliteration rates documented by angiography or MRI for all SM Grade III AVMs increased from 48% at 3 years to 69% at 4 years, 72% at 5 years, and 77% at 10 years. The SM Grade IIIa AVMs were more likely to obliterate than other subgroups. The cumulative rate of hemorrhage was 2.3% at 1 year, 4.4% at 2 years, 5.5% at 3 years, 6.4% at 5 years, and 9% at 10 years. The SM Grade IIIb AVMs had a significantly higher cumulative rate of hemorrhage. Symptomatic adverse radiation effects were detected in 6%.

Conclusions. Treatment with SRS was an effective and relatively safe management option for SM Grade III AVMs. Although patients with residual AVMs remained at risk for hemorrhage during the latency interval, the cumulative 10-year 9% hemorrhage risk in this series may represent a significant reduction compared with the expected natural history.

Spinal juvenile (Type III) extradural-intradural arteriovenous malformations

Spinal extradural-intradural AVMs

 J Neurosurg Spine 20:452–458, 2014

Owing to their rarity, demographics, natural history, and treatment, results for spinal juvenile (Type III) extradural-intradural arteriovenous malformations (AVMs) are frequently only provided in case report format.

Methods. A pooled analysis was performed utilizing the PubMed database through April 2013. Individualized patient data were extracted to elucidate demographics, hemorrhage risk, and treatment result information.

Results. Twenty-nine studies describing 51 patients were included. The mean age at presentation was 15.0 ± 10.5 years with a slight male predilection (63%, 1.7:1 sex ratio). Presentation modality included progressive deficits in 35%, hemorrhage in 31%, acute deficits not attributed to hemorrhage in 22%, and asymptomatic/incidental in 12% of patients. The annual hemorrhage rate was 2.1%; statistically significant risk factors for hemorrhage included presentation age (HR 0.39 [95% CI 0.18–0.87]) and associated aneurysms (HR 8.74 [95% CI 1.76–43.31]). Seventy-seven percent of patients underwent treatment; after a mean follow-up of 2.6 ± 3.2 years, 73% were improved, 10% were the same, and 17% were worse neurologically. Of 25 cases with described angiographic results, 8 lesions were obliterated (32%). Of these 25 patients, 8 had AVMs with associated aneurysms, and the aneurysm was obliterated in all 8 patients. Over the course of 57.9 patient-years of follow-up, including 55.3 patient-years for partially treated AVMs, no hemorrhages were described, reflecting a trend toward protection from hemorrhage after treatment (p = 0.12, likelihood ratio test).

Conclusions. Spinal juvenile (Type III) extradural-intradural AVMs commonly present symptomatically. Associated arterial aneurysms increase their hemorrhage risk, and protection from hemorrhage may be achieved from partial obliteration of these lesions, particularly if targeted toward associated aneurysms.

Stereotactic radiosurgery for arteriovenous malformations of the cerebellum

Bowden et al

J Neurosurg 120:583–590, 2014

Arteriovenous malformations (AVMs) of the posterior fossa have an aggressive natural history and propensity for hemorrhage. Although the cerebellum accounts for the majority of the posterior fossa volume, there is a paucity of stereotactic radiosurgery (SRS) outcome data for AVMs of this region. The authors sought to evaluate the long-term outcomes and risks of cerebellar AVM radiosurgery.

Methods. This single-institution retrospective analysis reviewed the authors’ experience with Gamma Knife surgery during the period 1987–2007. During this time 64 patients (median age 47 years, range 8–75 years) underwent SRS for a cerebellar AVM. Forty-seven patients (73%) presented with an intracranial hemorrhage. The median target volume was 3.85 cm3 (range 0.2–12.5 cm3), and the median marginal dose was 21 Gy (range 15–25 Gy).

Results. Arteriovenous malformation obliteration was confirmed by MRI or angiography in 40 patients at a median follow-up of 73 months (range 4–255 months). The actuarial rates of total obliteration were 53% at 3 years, 69% at 4 years, and 76% at 5 and 10 years. Elevated obliteration rates were statistically higher in patients who underwent AVM SRS without prior embolization (p = 0.005). A smaller AVM volume was also associated with a higher rate of obliteration (p = 0.03). Four patients (6%) sustained a hemorrhage during the latency period and 3 died. The cumulative rates of AVM hemorrhage after SRS were 6% at 1, 5, and 10 years. This correlated with an overall annual hemorrhage rate of 2.0% during the latency interval. One patient experienced a hemorrhage 9 years after confirmed MRI and angiographic obliteration. A permanent neurological deficit due to adverse radiation effects developed in 1 patient (1.6%) and temporary complications were seen in 2 additional patients (3.1%).

Conclusions. Stereotactic radiosurgery proved to be most effective for patients with smaller and previously nonembolized cerebellar malformations. Hemorrhage during the latency period occurred at a rate of 2.0% per year until obliteration occurred.

A prospective study of microscope-integrated intraoperative fluorescein videoangiography during arteriovenous malformation surgery

intraoperative fluorescein videoangiography during arteriovenous malformation surgery

Neurosurg Focus 36 (2):E15, 2014

The authors report on the use of a recently developed microscope-integrated fluorescent module using low-dose intravenous fluorescein for videoangiography during arteriovenous malformation (AVM) surgery.

Methods. The authors analyzed the application of a low-dose intraoperative fluorescein in 4 consecutive patients undergoing AVM surgery. The ability to distinguish the associated vessels of the AVM from normal vessels and to assess the degree of AVM obliteration based on videoangiography of venous drainage was specifically analyzed.

Results. All 4 patients underwent fluorescein angiography without complication. In each case, videoangiography confirmed recognition of feeding arteries and draining veins through the operating oculars under the fluorescent mode. In one case involving a large frontal AVM, videoangiography demonstrated mainly cortical veins on the surface of the AVM and alerted the senior author to first tackle the feeding arteries in the interhemispheric space. While evaluating the flow within the different draining veins after most of the AVM was disconnected, videoangiography also prioritized the order for disconnection of large draining veins to allow mobilization the AVM and exposure of the remaining deep arterial feeders. In the other 3 cases, videoangiography allowed easy recognition of the angioarchitecture of the AVMs, estimated its cortical boundaries, and most importantly, assessed the flow within the draining veins before their disconnection.

Conclusions. The authors found fluorescein videoangiography to be a useful adjunct in resection of AVMs. This technology offers the unique ability to visualize fluorescent vessels and nonfluorescent tissues in near-natural colors simultaneously and permits microsurgical manipulation of relevant structures under the fluorescent mode. Largerscale studies are needed to establish its efficacy and wider applicability.

Temporal Lobe Arteriovenous Malformations: Surgical Outcomes With a Focus on Visual Field Defects and Epilepsy

Temporal lobe AVM

Neurosurgery 73:854–862, 2013

Temporal lobe arteriovenous malformations (AVMs) represent a subgroup of intracranial AVMs with particular characteristics and management issues.

OBJECTIVE: To characterize the surgical outcomes of temporal lobe AVMs with emphasis on visual field deficits (VFDs) and seizures.

METHODS: Between 1992 and 2008, 29 patients were operated on for temporal lobe AVMs. Patient data were retrospectively collected and analyzed.

RESULTS: Twelve of 29 patients (41.4%) presented with seizures and 4 (13.7%) presented with VFDs. Postoperatively, 6 patients (24%) showed new VFDs and 2 improved, with a rate of preservation of full visual fields of 84%. Larger AVMs (.3 cm) were significantly associated with postoperative VFD (P = .008). Epilepsy outcomes assessed by the Engel scale were as follows: 9 patients (75%) were in class I (seizure free), 1 patient (8.3%) was in class III, and 2 patients (16.6%) were in class IV (no change or worsening). Postoperative modified Rankin Scale outcomes were excellent (grade 0-1) in 18 patients, good (grade 2) in 7, and poor (grade 3-4) in 4. Older age at diagnosis correlated with a worse functional outcome (Spearman r = 0.369; P = .049). AVMs were totally removed in 27 of 29 patients (93.1%). Complete surgical excision was confirmed with angiography. Two patients needed reoperation for AVM remnant. Three patients had persistent hemiparesis (10.3% permanent morbidity). There was no mortality.

CONCLUSION: Seizure control is usually underappreciated in the surgical management of AVMs. However, in temporal lobe AVMs, good outcomes with low morbidity and good visual field preservation can be accomplished.

Impact on Seizure Control of Surgical Resection or Radiosurgery for Cerebral Arteriovenous Malformations

AVM

Neurosurgery 73:648–656, 2013

Seizures are a common presenting symptom of arteriovenous malformations (AVMs). However, the impact of treatment modality on seizure control remains unclear.

OBJECTIVE: To compare seizure control after surgical resection or radiosurgery for AVMs.

METHODS: We analyzed retrospectively collected information for 378 patients with cerebral AVMs treated at our institution from 1990 to 2010. The application of strict inclusion criteria resulted in a study population of 164 patients.

RESULTS: In our cohort, 31 patients (20.7%) had Spetzler-Martin grade I AVMs, 51 (34.0%) grade II, 47 (31.3%) grade III, 20 (13.3%) grade IV, and 1 (0.7%) grade V. Of the 49 patients (30%) presenting with seizures, 60.4% experienced seizure persistence after treatment. For these patients, radiosurgery was associated with seizure recurrence (odds ratio: 4.32, 95% confidence interval: 1.24-15.02, P = .021). AVM obliteration was predictive of seizure freedom at last follow-up (P = .002). In contrast, for patients presenting without seizures, 18.4% experienced de novo seizures after treatment, for which surgical resection was identified as an independent risk factor (hazard ratio: 8.65, 95% confidence interval: 3.05-24.5, P < .001).

CONCLUSION: Although our data suggest that achieving seizure freedom should not be the primary goal of AVM treatment, surgical resection may result in improved seizure control compared with radiosurgery for patients who present with seizures. Conversely, in patients without presenting seizures, surgical resection increases the risk of newonset seizures compared with radiosurgery, but primarily within the early posttreatment period. Surgical resection and radiosurgery result in divergent seizure control rates depending on seizure presentation.

Indocyanine Green Videoangiography “In Negative”: Definition and Usefulness in Intracranial Dural Arteriovenous Fistulae

Indocyanine Green Videoangiography “In Negative”- Definition and Usefulness in Intracranial Dural Arteriovenous Fistulae

Neurosurgery 73[ONS Suppl 1]:ons86–ons92, 2013

Indocyanine green videoangiography (IGV) raises important limitations when we use it in vascular pathology, especially in cases with arterialization of the venous system such as arteriovenous malformations and fistulae.

OBJECTIVE: Our objective was to provide a simple procedure that overcomes the limitations of conventional IGV. We define IGV in negative (IGV-IN), so-called because, in its first phase, the vessel to analyze is clipped, and we report 3 cases of intracranial dural arteriovenous fistulae treated with this procedure.

METHODS: In 2011, we applied IGV-IN to 3 patients at our center with Borden type III intracranial arteriovenous fistulae.

RESULTS: In all 3 cases, IGV-IN enabled both diagnosis and post-dural arteriovenous fistula exclusion control in 1 integrated procedure no longer than 1 minute, requiring only 1 visualization.

CONCLUSION: IGV-IN is an improvement over the conventional IGV method and is able to provide more information in a shorter period of time. It is an intuitive and highly visual procedure, and, more importantly, it is reversible. Studies with larger samples are necessary to determine whether IGV-IN can further reduce the need for postoperative digital subtraction angiography.

Temporal lobe arteriovenous malformations: anatomical subtypes, surgical strategy, and outcomes

Temporal lobe AVM

J Neurosurg 119:616–628, 2013

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 temporooccipital 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.

Deep Arteriovenous Malformations in the Basal Ganglia, Thalamus, and Insula: Microsurgical Management, Techniques, and Results

Surgery for Deep AVM-1

Neurosurgery 73:417–429, 2013

Arteriovenous malformations (AVMs) in the basal ganglia, thalamus, and insula are considered inoperable given their depth, eloquence, and limited surgical exposure. Although many neurosurgeons opt for radiosurgery or observation, others have challenged the belief that deep AVMs are inoperable. Further discussion of patient selection, technique, and multimodality management is needed.

OBJECTIVE: To describe and discuss the technical considerations of microsurgical resection for deep-seated AVMs.

METHODS: Patients with deep AVMs who underwent surgery during a 14-year period were reviewed through the use of a prospective AVM registry.

RESULTS: Microsurgery was performed in 48 patients with AVMs in the basal ganglia (n = 10), thalamus (n = 13), or insula (n = 25). The most common Spetzler-Martin grade was III2 (68%). Surgical approaches included transsylvian (67%), transcallosal (19%), and transcortical (15%). Complete resection was achieved in 34 patients (71%), and patients with incomplete resection were treated with radiosurgery. Forty-five patients (94%) were improved or unchanged (mean follow-up, 1.6 years).

CONCLUSION: This experience advances the notion that select deep AVMs may be operable lesions. Patients were highly selected for small size, hemorrhagic presentation, young age, and compactness—factors embodied in the Spetzler-Martin and Supplementary grading systems. Overall, 10 different approaches were used, exploiting direct, transcortical corridors created by hemorrhage or maximizing anatomic corridors through subarachnoid spaces and ventricles that minimize brain transgression. The same cautious attitude exercised in selecting patients for surgery was also exercised in deciding extent of resection, opting for incomplete resection and radiosurgery more than with other AVMs to prioritize neurological outcomes.

Cerebral microarteriovenous malformations

microAVM

J Neurosurg 119:594–602, 2013

Microarteriovenous malformations (micro-AVMs) are a rare subgroup of brain AVMs characterized by a nidus smaller than 1 cm. The authors’ purpose in this study was to assess the clinical presentation, radiological features, therapeutic management, and outcome of these lesions.

METHODS
All angiography studies performed at the authors’ institution since 2000 for the diagnosis of AVM were retrospectively reviewed. Clinicoradiological findings, therapeutic management, and outcome were evaluated.

RESULTS
Twenty-eight patients had presented with AVMs having a nidus diameter smaller than 1 cm or no clearly identifiable nidus but an early draining vein. All patients, except 2, presented with intracranial hemorrhage, and 12 patients had a focal deficit. Supratentorial hematomas were large (mean volume 25 ml), and in 8 patients hematomas were evacuated urgently. In 6 patients cerebral digital subtraction angiography studies were normal. Magnetic resonance imaging and dynamic MR angiography revealed an AVM in 4 of these 6 patients. Treatment of the AVM consisted of surgery in 16 cases, radiosurgery in 6, and endovascular embolization in 2, and there were no posttreatment deficits. Four patients received no treatment because of their poor condition. The AVM was occluded at the follow-up in all patients treated with surgery or embolization and in 4 of the 6 patients treated with radiosurgery. The Glasgow Outcome Scale (GOS) score was good (GOS 4–5) in 23 patients (82%) and poor (GOS 3–2) in 5 (18%).

CONCLUSIONS
Patients with micro-AVMs generally present with large intracranial hemorrhages and neurological deficits. If the initial angiography is negative, then delayed or superselective angiography is recommended. Magnetic resonance imaging may reveal the existence of these lesions. Surgery is the treatment of choice for superficial micro-AVMs, and radiosurgery or embolization can be considered for deep lesions.

The failure of preoperative ethylene-vinyl alcohol copolymer embolization to improve outcomes in arteriovenous malformation management: case series

AVM-before

J Neurosurg 118:969–977, 2013

Ethylene-vinyl alcohol copolymer embolization is increasingly used preoperatively in the resection of brain arteriovenous malformations (AVMs). However, the case for embolization improving the outcome of resection has not been evaluated. In this paper the authors set out to compare outcomes after surgery for brain AVMs in 2 consecutive periods of practice. In the first period, selective embolization was used without the use of ethylene-vinyl alcohol copolymer. In the second period, selective embolization with ethylene-vinyl alcohol copolymer was performed.

Methods. A consecutive case series (prospectively collected data) was retrospectively analyzed. Adverse outcomes were considered to be an outcome modified Rankin Scale score greater than 2 due to embolization or surgery.

Results. A total of 538 surgical cases were included. The percentages of adverse outcomes were as follows: 0.34% for Spetzler-Martin AVMs less than Grade III (1 of 297 cases); 5.23% (95% CI 2.64%–9.78%) for Grade III AVMs (9 of 172 cases); and 17% (95% CI 10%–28%) for AVMs greater than Grade III (12 of 69 cases). There was no improvement in outcomes from the first period to the second period. The adverse outcome for Grade III brain AVMs in the first period was 5.2% (7 of 135 cases) and in the second period (after ethylene-vinyl alcohol copolymer was introduced) it was 5.4% (2 of 37 cases). For AVMs greater than Grade III, the adverse outcome was 12% (6 of 49 cases) in the first period and 30% (6 of 20 cases) in the second period.

Conclusions. Outcomes for brain AVM surgery were not improved by ethylene-vinyl alcohol copolymer embolization. Preoperative embolization of high-grade AVMs with an ethylene-vinyl alcohol copolymer did not prevent those hemorrhagic complications which embolization is hypothesized to prevent based on theoretical speculations but not demonstrated in practice.

Characteristics and long-term outcome of 251 patients with dural arteriovenous fistulas in a defined population

DAVF-headache

J Neurosurg 118:923–934, 2013

Management of dural arteriovenous fistulas (DAVFs) has changed during the last decades due to increased knowledge of their pathophysiology and natural history as well as advances in treatment modalities. The authors describe the characteristics and long-term outcome of a large consecutive series of patients with DAVFs.

Methods. Altogether 251 patients with 261 DAVFs were treated in 2 of the 5 neurosurgery departments at Helsinki and Kuopio University Hospitals between 1944 and 2006. Clinical data and radiological examinations were reviewed to assess patients’ overall long-term clinical outcome.

Results. The detection rate of DAVFs increased markedly in the 1970s and again in the 1990s when digital subtraction angiography was introduced. The incidence of DAVFs in a defined southern Finnish population was 0.51 per 100,000 individuals per year, which represents 32% of all the brain arteriovenous malformations. In the early part of the series, DAVFs were treated by proximal ligation of the feeding arteries. Later, most of the patients underwent preoperative embolization and subsequent craniotomy, and since 2000 stereotactic radiosurgery has been increasingly used in the treatment of DAVFs. Fifty-nine percent of the 261 fistulas were totally occluded. Treatment-related major complications were seen in 21 patients.

Conclusions. The advances in diagnostic methods (digital subtraction angiography, CT, and MRI) increased the detection rate of DAVFs, and as treatment modalities developed, the results of treatment and outcome of patients markedly improved with the introduction of endovascular techniques and stereotactic radiosurgery. Microsurgery is of limited use in DAVFs resistant to other treatment modalities.