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Bradley A. Gross and Rose Du

Object

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.

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Bradley A. Gross and Rose Du

OBJECTIVE

The aim of this paper is to define an overall cavernous malformation (CM) hemorrhage rate and risk factors for hemorrhage.

METHODS

The authors performed a systematic, pooled analysis via the PubMed database through October 2015 using the terms “cavernoma,” “cavernous malformation,” “natural history,” “bleeding,” and “hemorrhage.” English-language studies providing annual rates and/or risk factors for CM hemorrhage were included. Data extraction, performed independently by the authors, included demographic data, hemorrhage rates, and hemorrhage risk factors.

RESULTS

Across 12 natural history studies with 1610 patients, the mean age at presentation was 42.7 years old and 52% of patients (95% CI 49%–55%) were female. Presentation modality was seizure in 30% (95% CI 25%–35%), hemorrhage in 26% (95% CI 17%–37%), incidental in 17% (95% CI 9%–31%), and focal deficits only in 16% of cases (95% CI 11%–23%). CM location was lobar in 66% (95% CI 61%–70%), brainstem in 18% (95% CI 13%–24%), deep supratentorial in 8% (95% CI 6%–10%), and cerebellar in 8% (95% CI 5%–11%). Pooling 7 studies that did not assume CM presence since birth, the annual hemorrhage rate was 2.5% per patient-year over 5081.2 patient-years of follow-up (95% CI 1.3%–5.1%). Pooling hazard ratios across 5 studies that evaluated hemorrhage risk factors, prior CM hemorrhage was a significant risk factor for hemorrhage (HR 3.73, 95% CI 1.26–11.1; p = 0.02) while younger age, female sex, deep location, size, multiplicity, and associated developmental venous anomalies (DVAs) were not.

CONCLUSIONS

Although limited by the heterogeneity of incorporated reports and selection bias, this study found prior hemorrhage to be a significant risk factor for CM bleeding, while age, sex, CM location, size, multiplicity, and associated DVAs were not. Future natural history studies should compound annual hemorrhage rate with prospective seizure and nonhemorrhagic neurological deficit rates.

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Bradley A. Gross and Rose Du

Object

The purpose of this report was to provide overall arteriovenous malformation (AVM) hemorrhage rates and, with enhanced statistical power, to elucidate significant risk factors for hemorrhage.

Methods

The authors performed a meta-analysis via the PubMed database through January 2012 using the terms “AVM,” “arteriovenous malformation,” “natural history,” “bleed,” and “hemorrhage.” Additional studies were identified through reference searches in each reviewed article. English language studies providing annual hemorrhage rates for AVMs were included. Data extraction, performed independently by the authors, included demographic data, hemorrhage rates, and hazard ratios for hemorrhage risk factors. The analysis was performed using a random effects model.

Results

Nine natural history studies with 3923 patients and 18,423 patient-years of follow-up were identified for analysis. The overall annual hemorrhage rate was 3.0% (95% CI 2.7%–3.4%). The rate of hemorrhage was 2.2% (95% CI 1.7%–2.7%) for unruptured AVMs and 4.5% (95% CI 3.7%–5.5%) for ruptured AVMs. Prior hemorrhage (HR 3.2, 95% CI 2.1–4.3), deep AVM location (HR 2.4, 95% CI 1.4–3.4), exclusively deep venous drainage (HR 2.4, 95% CI 1.1–3.8), and associated aneurysms (HR 1.8, 95% CI 1.6–2.0) were statistically significant risk factors for hemorrhage. Any deep venous drainage (HR 1.3, 95% CI 0.9–1.75) and female sex (HR 1.4, 95% CI 0.6–2.1) demonstrated a trend toward an increased risk of hemorrhage that was not statistically significant. Small AVM size and older patient age were not significant risk factors for hemorrhage.

Conclusions

Arteriovenous malformations with prior hemorrhage, deep location, exclusively deep venous drainage, and associated aneurysms have greater annual hemorrhage rates than their counterparts, influencing surgical decision making and the selection of radiosurgery for these lesions.

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Wendy Huang, Bradley A. Gross and Rose Du

Object

Our understanding of spinal extradural arteriovenous fistulas (eAVFs) is relatively limited. In this study the authors aimed to provide the demographics, natural history, and treatment results of these rare lesions.

Methods

The authors performed a pooled analysis of data in the PubMed database through December 2012. Individualized patient data were extracted to elucidate demographic, clinical, and angioarchitectural features of spinal eAVFs as well as outcomes following different treatment strategies.

Results

Information on 101 patients was extracted from 63 eligible studies. The mean patient age was 45.9 years, and there was no significant overall sex predilection. Only 3% of the lesions were incidental, whereas 10% occurred in patients who had presented with hemorrhage. None of the 64 patients with at least 1 month of untreated follow-up sustained a hemorrhage over a total of 83.8 patient-years. Patients with lumbosacral eAVFs were significantly older (mean age 58.7 years, p < 0.0001), were significantly more often male (70% male, p = 0.02), had significantly worse presenting Aminoff-Logue motor and bladder scores (p = 0.0008 and < 0.0001, respectively), and had the greatest prevalence of lesions with intradural venous drainage (62% of cases, p < 0.0001). Neurofibromatosis Type 1 (30% of cases, p < 0.0001) and subarachnoid hemorrhage (9% of cases, p = 0.06) were associated with and exclusively found in patients with cervical eAVFs. The overall complete obliteration rate was 91%. After a mean follow-up of 1.7 years, the clinical condition was improved in 89% of patients, the same in 9%, and worse in 2%. Obliteration rates and outcome at follow-up did not significantly differ between surgical and endovascular treatment modalities.

Conclusions

Spinal eAVFs are rare lesions with a low risk of hemorrhage; they cause neurological morbidity as a result of mass effect and/or venous hypertension. Their treatment is associated with a high rate of complete obliteration and improvement in preoperative symptoms.

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Bradley A. Gross, Edward R. Smith and R. Michael Scott

Object

Cavernous malformations (CMs) of the basal ganglia are relatively rare lesions that can lead to considerable neurological impairment because of their eloquent location. The authors reviewed the clinical course and surgical outcome of a series of children with basal ganglia CMs.

Methods

The authors retrospectively reviewed the operative experience of the senior author (R.M.S.) and the 1997–2011 database of Boston Children's Hospital for children with CM of the basal ganglia (which includes CM of the caudate and/or lentiform nucleus and excludes CM of the thalamus). They evaluated baseline demographics, presenting signs, operative outcomes, and condition at long-term follow-up visits and compared these characteristics among patients who underwent surgery and those who were observed.

Results

Of 180 children with a diagnosis of CM, 11 (6%) had CM of the basal ganglia. The mean age at diagnosis was 9.3 years, and the male/female ratio was 1.8:1. Presenting signs were as follows: hemorrhage (8 children), incidental lesions (2), and seizures (1); 2 children had choreiform movement disorders. Treatment was observation or surgery. Observation was chosen for 5 children either because the lesions were asymptomatic (2 children) or because the risk for neurological dysfunction after attempted excision was believed to be high (3 children). These 5 children were observed over a combined total of 30.4 patient-years; none experienced neurological deterioration or symptomatic hemorrhage from their lesions. The other 6 children underwent microsurgical resection of the lesion because they were symptomatic from hemorrhage or increasing mass effect. All 6 of these children had hemorrhagic lesions, of which the smallest dimension was at least 1.5 cm. Of these 6 lesions, 5 were excised completely, and over a combined total of 46 patient-years of follow-up, no rebleeding or late neurological deterioration after surgery was reported.

Conclusions

In this patient population, the natural history of small and asymptomatic CMs of the basal ganglia was benign. The children with large (> 1.5 cm) symptomatic lesions underwent excision; neurological impairment was apparently minimal, and no hemorrhage or neurological deterioration occurred later.

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Bradley A. Gross, Pui Man Rosalind Lai and Rose Du

Object

The rates and risk factors for external ventricular drain (EVD) placement and long-term shunt dependence in patients with ruptured arteriovenous malformations (AVMs) have not been systematically studied. In this study the authors evaluated the rates of EVD placement and shunt dependence, and risk factors for them, in a cohort of patients with ruptured AVMs.

Methods

The records of 87 consecutive patients with ruptured AVMs were reviewed for patient demographics, hemorrhage pattern, AVM angioarchitectural features, and surgical treatment. Univariate and multivariate logistic regression analyses were performed to evaluate risk factors for EVD placement, permanent shunt dependence, and long-term outcome (as measured by the modified Rankin Scale).

Results

Thirty-eight patients (44%) required EVD placement, and 16 (18%) required a permanent shunt. Statistically significant risk factors for EVD placement in the univariate analysis included initial Glasgow Coma Scale (GCS) score (p = 0.002), the presence of intraventricular hemorrhage (IVH; p < 0.001), AVM-associated aneurysms (p = 0.002), and early surgery (p = 0.01). Multivariate analysis revealed only AVM-associated aneurysms as statistically significant (p = 0.006). Risk factors for shunt placement included initial GCS score (p = 0.003), IVH (p = 0.01), deep supratentorial location (p = 0.034), and associated aneurysms (p = 0.03). Multivariate analysis revealed initial GCS score as a statistically significant risk factor (p = 0.041) as well as a strong trend for associated aneurysms (p = 0.06). Patient age, sex, associated subarachnoid hemorrhage, AVM grade, AVM size, and deep venous drainage were not associated with EVD placement or long-term shunt dependence.

Conclusions

Hydrocephalus from AVM rupture was associated with initial GCS score, IVH, and AVM-associated aneurysms. Arteriovenous malformations with associated aneurysms thus not only have a greater risk of hemorrhage but also a greater risk of hemorrhage-associated morbidity as a result of hydrocephalus.

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Martin Pham, Bradley A. Gross, Bernard R. Bendok, Issam A. Awad and H. Hunt Batjer

The use of radiosurgery for angiographically occult vascular malformations (AOVMs) is a controversial treatment option for those that are surgically inaccessible or located in eloquent brain. To determine the efficacy of this treatment, the authors reviewed the literature reporting hemorrhage rates, seizure control, and radiation-induced morbidity. They found overall hemorrhage rates of 2–6.4%, overall postradiosurgery hemorrhage rates of 1.6–8%, and stratified postradiosurgery hemorrhage rates of 7.3–22.4% in the period immediately to 2 years after treatment; these latter rates declined to 0.8–5.2% > 2 years after treatment. Of 291 patients presenting with seizure across 16 studies, 89 (31%) attained a seizure-free status and 102 (35%) had a reduction in seizure frequency after radiosurgery. Overall radiation-induced morbidity ranged from 2.5 to 59%, with higher complication rates in patients with brainstem lesion locations. Researchers applying mean radiation doses of 15–16.2 Gy to the tumor margin saw both low radiationinduced complication rates (0–9.1%) and adequate hemorrhage control (0.8–5.2% > 2 years after treatment), whereas mean doses ≥ 16.5 Gy were associated with higher total radiation-induced morbidity rates (> 17%). Although the use of stereotactic radiosurgery remains controversial, patients with AOVMs located in surgically inaccessible areas of the brain may benefit from such treatment.

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Bradley A. Gross, Armide Storey, Darren B. Orbach, R. Michael Scott and Edward R. Smith

OBJECT

Outcomes of microsurgical treatment of arteriovenous malformations (AVMs) in children are infrequently reported across large cohorts.

METHODS

The authors undertook a retrospective review of departmental and hospital databases to obtain the medical data of all patients up to 18 years of age who were diagnosed with cerebral AVMs. Demographic and AVM angioarchitectural characteristics were analyzed, and for the patients who underwent surgery, the authors also analyzed the estimated intraoperative blood loss, postoperative angiographically confirmed obliteration rates, and neurological complications and outcomes classified according to the modified Rankin Scale (mRS).

RESULTS

Of 117 children with cerebral AVMs, 94 underwent microsurgical resection (80%). Twenty (21%) of these 94 patients underwent adjunctive preoperative embolization. The overall postoperative angiographically confirmed obliteration rate was 94%. As part of a new protocol, the last 50 patients in this series underwent immediate perioperative angiography, improving the subsequent obliteration rate from 86% to 100% (p = 0.01). No other factors, such as a hemorrhagic AVM, size of the AVM, location, drainage, or Spetzler-Martin grade, had a statistically significant impact on the obliteration rate. Perioperative neurological deficits occurred in 17% of the patients, but the vast majority of these (77%) were predictable visual field cuts. Arteriovenous malformations that were hemorrhagic or located in noneloquent regions were each associated with lower rates of postoperative neurological complications (p = 0.05 and 0.002, respectively). In total, 94% of the children had good functional outcomes (mRS Scores 0–2), and these outcomes were significantly influenced by the mRS score on presentation before surgery (p = 0.01). A review of 1- and 5-year follow-up data indicated an overall annual hemorrhage rate of 0.3% and a recurrence rate of 0.9%.

CONCLUSIONS

Microsurgical resection of AVMs in children is associated with high rates of angiographically confirmed obliteration and low rates of significant neurological complications. Implementation of a protocol using perioperative angiography in this series led to complete radiographically confirmed obliteration of all AVMs, with low annual repeat hemorrhage and recurrence rates.

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Bradley A. Gross, Felipe C. Albuquerque, Karam Moon and Cameron G. McDougall

OBJECTIVE

Many small series and technical reports chronicle the evolution of endovascular techniques for cranial dural arteriovenous fistulas (dAVFs) over the past 3 decades, but reports of large patient series are lacking. The authors provide a thorough analysis of clinical and angiographic outcomes across a large patient cohort.

METHODS

The authors reviewed their endovascular database from January 1996 to September 2015 to identify patients harboring cranial dAVFs who were treated initially with endovascular approaches. They extracted demographic, presentation, angiographic, detailed treatment, and long-term follow-up data, and they evaluated natural history, initial angiographic occlusion, complications, recurrence, and symptomatic resolution rates.

RESULTS

Across a cohort of 251 patients with 260 distinct dAVFs, the overall initial angiographic occlusion rate was 70%; recurrence or occult residual lesions were seen on subsequent angiography in 3% of cases. The overall complication rate was 8%, with permanent neurological complications occurring in 3% of cases. Among 102 patients with dAVFs without cortical venous reflux, rates of resolution/improvement of pulsatile tinnitus and ocular symptoms were 79% and 78%, respectively. Following the introduction of Onyx during the latter half of the study period, the number of treated dAVFs doubled; the initial angiographic occlusion rate increased significantly from 60% before the use of Onyx to 76% after (p = 0.01). In addition, during the latter period compared with the pre-Onyx period, the rate of dAVFs obliterated via a transarterial-only approach was significantly greater (43% vs 23%, p = 0.002), as was the number of dAVFs obliterated via a single arterial pedicle (29% vs 11%, p = 0.002).

CONCLUSIONS

Overall, in the Onyx era, the rate of initial angiographic occlusion was approximately 80%, as was the rate of meaningful clinical improvement in tinnitus and/or ocular symptoms after initial endovascular treatment of cranial dAVFs.

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Alexander E. Ropper, Bradley A. Gross and Rose Du

Object

Type I spinal dural arteriovenous fistulas (SDAVFs) are low-flow vascular shunts fed by radicular arteries in patients who most often present with myelopathy. Although some fistulas are amenable to endovascular embolization, nearly all can be treated with direct microsurgical obliteration.

Methods

The authors reviewed their experience in treating 214 craniospinal arteriovenous malformations and/or fistulas over the last 8 years. Of these, 19 were spinal (9%), of which 15 (79%) were Type I SDAVFs. The authors reviewed the patients' epidemiological characteristics, presenting symptoms, and SDAVF angioarchitecture in all cases. They subsequently analyzed surgical obliteration rates and outcomes of all 11 patients who underwent fistula microsurgical obliteration.

Results

In all patients who underwent microsurgical treatment, complete angiographic obliteration of the fistula was achieved. At follow-up, 10 (91%) of 11 patients exhibited improvement, 1 patient (9%) was the same, and no patients were worse. Specifically, 8 (73%) of 11 patients had improvement in strength and sensation, 5 (71%) of 7 had improvement of bowel/bladder function, and 3 (60%) of 5 had improvement of preoperative paresthesias. There were no wound infections, CSF leaks, or permanent neurological deficits.

Conclusions

Microsurgical treatment of SDAVF provides direct access to the fistula point, allowing for high obliteration rates with excellent long-term improvement of preoperative deficits and limited periprocedural complications.