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A. Giancarlo Vishteh, Ameet C. Patel, Robert F. Spetzler, Robert C. Wallace, and C. Philip Daspit

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C. Hunter Sheldon, Robert H. Pudenz, Wallace B Hamby, and William F. Meacham

✓ In the second and final series of comments solicited for the Journal of Neurosurgery's 50th anniversary, four additional authors, each of whom was an original contributor to the first volume of the Journal, share some thoughts and anecdotes regarding their first articles.

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Farhad Pirouzmand, M. Christopher Wallace, and Robert Willinsky

✓ A spinal epidural arteriovenous fistula with secondary reflux into the perimedullary veins is a rare entity. The authors present such a case with a discussion of its pathophysiology and treatment. The mechanism for formation of a spinal dural arteriovenous fistula is outlined based on the anatomical substrates in this region.

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J. Marc C. van Dijk, Karel G. TerBrugge, Robert A. Willinsky, and M. Christopher Wallace

Object. A single-institution series of 119 consecutive patients with a dural arteriovenous fistula (DAVF) and cortical venous reflux was reviewed to assess the overall clinical outcome of multidisciplinary management after long-term follow up. The selective disconnection of the cortical venous reflux compared with the obliteration of the entire DAVF was evaluated.

Methods. Dural arteriovenous fistulas in patients in this series were diagnosed between 1984 and 2001, and treatment was instituted in 102 of them. The outcome of adequately treated patients was compared with that of a control group consisting of those with persistent cortical venous reflux and with data found in the literature. In cases of combined dural sinus drainage and cortical venous reflux, a novel treatment concept of selective disconnection of the cortical venous reflux that left the sinus drainage intact, and thus converted the aggressive DAVF into a benign lesion, was evaluated.

Endovascular treatment, which was instituted initially in 78 patients, resulted in an obliteration or selective disconnection in 26 (25.5%) of 102 cases. In 70 cases (68.6%) the DAVFs were surgically obliterated or disconnected. In six cases (5.9%), patients were left with persistent cortical venous reflux. No lasting complications were noted in this series. Follow-up angiography confirmed a durable result in 94 (97.9%) of 96 adequately treated cases, at a mean follow up of 27.6 months (range 1.4–138.3 months).

Selective disconnection was performed in 23 DAVFs with combined sinus drainage and cortical venous reflux. These patients' long-term outcomes were equal to those with obliterated DAVFs, and the complication rate was lower.

Conclusions. Considering the ominous course of DAVFs with patent cortical venous reflux, multidisciplinary treatment of these lesions is highly effective and the complication rate is low. Selective disconnection provides a valid treatment option of DAVFs with combined dural sinus drainage and cortical venous reflux, as has been shown in cranial DAVFs with direct cortical venous reflux.

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J. Marc C. Van Dijk, Karel G. TerBrugge, Robert A. Willinsky, and M. Christopher Wallace

Object. Dural arteriovenous fistulas (AVFs) are a well-known pathoanatomical and clinical entity. Excluding bilateral involvement of the cavernous sinus, multiple dural AVFs are rare, with isolated reports in the literature. The additional risk associated with multiplicity is unknown, although it has been claimed that there is a greater risk of hemorrhage at presentation. In a group of 284 patients with dural AVFs consecutively treated at a single center, the occurrence of multiplicity is investigated and its risk factors for hemorrhage are identified.

Methods. Among the 284 patients with both cranial and spinal dural AVFs, 20 patients with multiple fistulas were found. Nineteen (8.1%) of 235 patients with cranial AVFs had multiple cranial fistulas, and one (2%) of 49 patients with spinal AVFs harbored two spinal fistulas. Twelve patients were found to have a lesion at two separate sites, seven patients had them at three locations, and one patient had four fistulas, each at a different site.

In the subgroup with multiple AVFs the percentage of hemorrhage at presentation was three times higher than in the entire group (p = 0.01). Cortical venous drainage in cranial fistulas was present in 84% of patients with multiple lesions compared with 46% of patients with solitary lesions (p < 0.005).

Conclusions. Multiple dural AVFs are not rare. In this group of 284 patients it was found in 8.1% of all patients with cranial dural AVFs. Multiplicity was associated with a higher percentage of cortical venous drainage, a pattern of drainage reportedly yielding a higher risk for hemorrhage.

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Phillip J. Porter, Robert A. Willinsky, William Harper, and M. Christopher Wallace

✓ Despite recent studies of the natural history of cavernous malformations, there remains significant uncertainty concerning hemorrhage rates and the importance of lesion location. Controversy arises over varying definitions of “hemorrhage.” What is ultimately important to the patient is the occurrence of a neurological event, which may or may not be associated with radiologically documented hemorrhage, as well as the chance of recovery after such an event. The purpose of this study was to determine the rates of occurrence and sequelae of neurological events in 173 patients referred to our vascular malformation clinic with cavernous malformations.

All patient data were entered into a database. The mean age at presentation for the 173 patients was 37.5 years. The lesion location was deep (brainstem, cerebellar nuclei, thalamus, or basal ganglia) in 64 patients (37%) and superficial in 109 (63%). Thirty-one patients (18%) had multiple lesions. Disease presentation was due to seizures in 62 patients (36%), hemorrhage in 44 (25%), focal neurological deficit without documented hemorrhage in 35 (20%), headache alone in 11 (6%), and incidental findings in 21 patients (12%). The results obtained in the 110 patients eligible for follow-up review were used to derive information on the rates of hemorrhage and neurological events. An interval event (neurological deterioration) required both symptoms and signs. The total mean follow-up period was 46 months, the majority (65%) of which was prospective. There were 18 interval events in 427 patient-years of follow-up review, for an overall annual event rate of 4.2%. Location was the most important factor for predicting interval event occurrence, with significantly higher rates for deeply located (10.6%/year) compared with superficially located lesions (0%/year) (p = 0.0001). Of patients suffering a neurological event, only 37% had complete resolution of their deficits.

This largely prospective study indicates that deep cavernous malformations carry a worse prognosis than superficial lesions with respect to annual rates of neurological deterioration. The alarming rate of adverse clinical events occurring in patients with deep lesions is punctuated by the fact that less than one-half of them recover fully during long-term follow-up review.

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Robert F. Spetzler, Cameron G. McDougall, Joseph M. Zabramski, Felipe C. Albuquerque, Nancy K. Hills, Peter Nakaji, John P. Karis, and Robert C. Wallace

OBJECTIVE

The authors present the 10-year results of the Barrow Ruptured Aneurysm Trial (BRAT) for saccular aneurysms. The 1-, 3-, and 6-year results of the trial have been previously reported, as have the 6-year results with respect to saccular aneurysms. This final report comparing the safety and efficacy of clipping versus coiling is limited to an analysis of those patients presenting with subarachnoid hemorrhage (SAH) from a ruptured saccular aneurysm.

METHODS

In the study, 362 patients had saccular aneurysms and were randomized equally to the clipping and the coiling cohorts (181 each). The primary outcome analysis was based on the assigned treatment group; poor outcome was defined as a modified Rankin Scale (mRS) score > 2 and was independently adjudicated. The extent of aneurysm obliteration was adjudicated by a nontreating neuroradiologist.

RESULTS

There was no statistically significant difference in poor outcome (mRS score > 2) or deaths between these 2 treatment arms during the 10 years of follow-up. Of 178 clip-assigned patients with saccular aneurysms, 1 (< 1%) was crossed over to coiling, and 64 (36%) of the 178 coil-assigned patients were crossed over to clipping. After the initial hospitalization, 2 of 241 (0.8%) clipped saccular aneurysms and 23 of 115 (20%) coiled saccular aneurysms required retreatment (p < 0.001). At the 10-year follow-up, 93% (50/54) of the clipped aneurysms were completely obliterated, compared with only 22% (5/23) of the coiled aneurysms (p < 0.001). Two patients had documented rebleeding, both died, and both were in the assigned and treated coiled cohort (2/83); no patient in the clipped cohort (0/175) died (p = 0.04). In 1 of these 2 patients, the hemorrhage was not from the target aneurysm but from an incidental basilar artery aneurysm, which was coiled at the same time.

CONCLUSIONS

There was no significant difference in clinical outcomes between the 2 assigned treatment groups as measured by mRS outcomes or deaths. Clinical outcomes in the patients with posterior circulation aneurysms were better in the coiling group at 1 year, but after 1 year this difference was no longer statistically significant. Rates of complete aneurysm obliteration and rates of retreatment favored patients who actually underwent clipping compared with those who underwent coiling.

Clinical trial registration no.: NCT01593267 (clinicaltrials.gov)

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Robert F. Spetzler, Joseph M. Zabramski, Cameron G. McDougall, Felipe C. Albuquerque, Nancy K. Hills, Robert C. Wallace, and Peter Nakaji

OBJECTIVE

The Barrow Ruptured Aneurysm Trial (BRAT) is a prospective, randomized trial in which treatment with clipping was compared to treatment with coil embolization. Patients were randomized to treatment on presentation with any nontraumatic subarachnoid hemorrhage (SAH). Because all other randomized trials comparing these 2 types of treatments have been limited to saccular aneurysms, the authors analyzed the current BRAT data for this subgroup of lesions.

METHODS

The primary BRAT analysis included all sources of SAH: nonaneurysmal lesions; saccular, blister, fusiform, and dissecting aneurysms; and SAHs from an aneurysm associated with either an arteriovenous malformation or a fistula. In this post hoc review, the outcomes for the subgroup of patients with saccular aneurysms were further analyzed by type of treatment. The extent of aneurysm obliteration was adjudicated by an independent neuroradiologist not involved in treatment.

RESULTS

Of the 471 patients enrolled in the BRAT, 362 (77%) had an SAH from a saccular aneurysm. Patients with saccular aneurysms were assigned equally to the clipping and the coiling cohorts (181 each). In each cohort, 3 patients died before treatment and 178 were treated. Of the 178 clip-assigned patients with saccular aneurysms, 1 (1%) was crossed over to coiling, and 64 (36%) of the 178 coil-assigned patients were crossed over to clipping. There was no statistically significant difference in poor outcome (modified Rankin Scale score > 2) between these 2 treatment arms at any recorded time point during 6 years of follow-up. After the initial hospitalization, 1 of 241 (0.4%) clipped saccular aneurysms and 21 of 115 (18%) coiled saccular aneurysms required retreatment (p < 0.001). At the 6-year follow-up, 95% (95/100) of the clipped aneurysms were completely obliterated, compared with 40% (16/40) of the coiled aneurysms (p < 0.001). There was no difference in morbidity between the 2 treatment groups (p = 0.10).

CONCLUSIONS

In the subgroup of patients with saccular aneurysms enrolled in the BRAT, there was no significant difference between modified Rankin Scale outcomes at any follow-up time in patients with saccular aneurysms assigned to clipping compared with those assigned to coiling (intent-to-treat analysis). At the 6-year follow-up evaluation, rates of retreatment and complete aneurysm obliteration significantly favored patients who underwent clipping compared with those who underwent coiling.

Clinical trial registration no.: NCT01593267 (clinicaltrials.gov)

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John S. Norris, Taufik A. Valiante, M. Christopher Wallace, Robert A. Willinsky, Walter J. Montanera, Karel G. terBrugge, and Michael Tymianski

Object. The authors sought to establish prospectively whether there is a simple relationship between radiological features of brain arteriovenous malformation (AVM) hemodynamics and a patient's clinical presentation.

Methods. Thirty-one consecutive patients with AVMs underwent cerebral angiography at 3.8 frames/second during each standardized injection of contrast material. Contrast dilution curves were derived from the image sequences by using regions of interest (ROIs) traced on arteries feeding and veins draining the AVM nidus. Angiographic parameters were then analyzed in a blinded fashion. These parameters included the times required to reach the peak contrast density, the contrast decay time, and fractions thereof, in the ROI for each vessel. The authors determined whether these parameters, the arteriovenous transit time, and/or AVM size were related to patients' presentation with hemorrhage (11 patients), seizure (11 patients), or other clinical symptoms (nine patients). Statistically significant results were found only in analyses of arterial phase times to reach peak contrast density. Analyses of venous parameters, AVM size, and nidus transit time showed trends but no statistical significance. Arterial filling with contrast material was significantly slower in patients presenting with hemorrhage (mean 50%, 80%, and 100% of time to peak ± standard error [SE] = 1.19 ± 0.13, 1.97 ± 0.18, and 3.04 ± 0.34 seconds, respectively) compared with patients presenting with seizures (mean 50%, 80%, and 100% of time to peak ± SE = 0.80 ± 0.12, 1.32 ± 0.18, and 1.95 ± 0.29 seconds, respectively) according to analysis of variance (p < 0.05) and post-hoc t-tests (p < 0.05) for each parameter. Patients who presented with other symptoms had intermediate arterial filling times.

Conclusions. These simple hemodynamic parameters, which can be obtained without added risk to the patient, may help identify a subset of individuals in whom AVMs pose a higher risk of future hemorrhage and who may therefore warrant more expeditious treatment.

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Roberto C. Heros