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Natural history of cerebral arteriovenous malformations: a meta-analysis

Clinical article

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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Hemorrhage from cerebral cavernous malformations: a systematic pooled analysis

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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Spinal juvenile (Type III) extradural-intradural arteriovenous malformations

Clinical article

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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Spinal extradural arteriovenous fistulas

Clinical article

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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Intramedullary spinal cord cavernous malformations

Bradley A. Gross, Rose Du, A. John Popp, and Arthur L. Day

Although originally the subject of rare case reports, intramedullary spinal cord cavernous malformations (CMs) have recently surfaced in an increasing number of case series and natural history reports in the literature. The authors reviewed 27 publications with 352 patients to consolidate modern epidemiological, natural history, and clinical and surgical data to facilitate decision making when managing these challenging vascular malformations. The mean age at presentation was 42 years without a sex predilection. Thirty-eight percent of the cases were cervical, 57% thoracic, 4% lumbar, and 1% unspecified location. Nine percent of the patients had a family history of CNS CMs. Twenty-seven percent of the patients had an associated cranial CM. On presentation 63% of the patients had motor deficits, 65% had sensory deficits, 27% had pain, and 11% had bowel or bladder dysfunction. Presentation was acute in 30%, recurrent in 16%, and progressive in 54% of cases. An overall annual hemorrhage rate was calculated as 2.5% for 92 patients followed up for a total of 2571 patient-years. Across 24 reviewed surgical series, a 91% complete resection rate was found. Transient morbidity was seen in 36% of cases. Sixty-one percent of patients improved, 27% were unchanged, and 12% were worse at the long-term follow-up. Using this information, the authors review surgical nuances in treating these lesions and propose a management algorithm.

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Stereotactic radiosurgery for cerebral dural arteriovenous fistulas

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

Object

Given the feasibility of curative surgical and endovascular therapy for cerebral dural arteriovenous fistulas (DAVFs), there is a relative paucity of radiosurgical series for these lesions as compared with their arteriovenous malformation counterparts.

Methods

The authors reviewed records of 56 patients with 70 cerebral DAVFs treated at their institution over the past 6 years. Ten DAVFs (14%) in 9 patients were treated with stereotactic radiosurgery (SRS), with follow-up obtained for 8 patients with 9 DAVFs. They combined their results with those obtained from a comprehensive review of the literature, focusing on obliteration rates, post-SRS hemorrhage rates, and other complications.

Results

In the authors' group of 9 DAVFs, angiographic obliteration was seen in 8 cases (89%), and no post-SRS hemorrhage or complications were observed after a mean follow-up of 2.9 years. Combining the results in these cases with data obtained from their review of the literature, they found 558 DAVFs treated with SRS across 14 series. The overall obliteration rate was 71%; transient worsening occurred in 9.1% of patients, permanent worsening in 2.4% (including 1 death, 0.2% of cases), and post-SRS hemorrhage occurred in 1.6% of cases (4.8% of those with cortical venous drainage [CVD]). The obliteration rate for cavernous DAVFs was 84%, whereas the rates for transversesigmoid and for tentorial DAVFs were 58% and 59%, respectively (adjusted p values, pcav,TS = 1.98 × 10−4, pcav,tent = 0.032). Obliteration rates were greater for DAVFs without CVD (80%, compared with 60% for those with CVD, p = 7.59 × 10−4). Both transient worsening and permanent worsening were less common in patients without CVD than in those with CVD (3.4% vs 7.3% for transient worsening and 0.9% vs 2.4% for permanent worsening).

Conclusions

Stereotactic radiosurgery with or without adjunctive embolization is an effective therapy for DAVFs that are not amenable to surgical or endovascular monotherapy. It is best suited for lesions without CVD and for cavernous DAVFs.

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Hydrocephalus after arteriovenous malformation rupture

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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Cavernous malformations of the basal ganglia in children

Clinical article

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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The natural history of intracranial cavernous malformations

Bradley A. Gross, Ning Lin, Rose Du, and Arthur L. Day

Literature reports on the natural history of cerebral cavernous malformations (CMs) are numerous, with considerable variability in lesion epidemiology, hemorrhage rates, and risk factors for hemorrhage. In this review, the authors performed a meta-analysis of 11 natural history studies. The overall male-to-female ratio was 1:1, and the mean age at presentation was 30.6 years. Overall, 37% of patients presented with seizures, 36% with hemorrhage, 23% with headaches, 22% with focal neurological deficits, and 10% were asymptomatic. Some patients had more than one symptom. Seizure presentation was most prevalent among supratentorial CMs, while focal neurological deficits were common in patients with infratentorial CMs. By location, CMs were in the cerebral hemispheres (66%), brainstem (18%), basal ganglia or thalamus (8%), cerebellum (6%), and other (2.5% [combined supra- and infratentorial, callosal or insular]). Overall, 19% of patients harbored multiple intracranial CMs, and 9% had radiographically apparent associated developmental venous anomalies. An overall annual hemorrhage rate of 2.4% per patient-year (range 1.6%–3.1%) was identified across 3 studies. Prior hemorrhage and female sex were risk factors for bleeding, while CM size and multiplicity did not affect hemorrhage rates. Although not impacting the hemorrhage rate itself, deep location was a risk factor for increased clinical aggressiveness.

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Cerebral dural arteriovenous fistulas and aneurysms

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

Object

The association of aneurysms and cerebral arteriovenous malformations is well established in the literature. Aside from a small number of case reports and small patient series, this association has not been well explored with cerebral dural arteriovenous fistulas (DAVFs). This study was designed to elucidate this relationship in the authors' own patient cohort with DAVFs.

Methods

Cerebral angiograms of 56 patients with 70 DAVFs were reviewed for the presence of cerebral aneurysms. Background patient demographics, mode of presentation, and DAVF and aneurysm angiographic characteristics were noted.

Results

Twelve patients (21%) had aneurysms in addition to their DAVF. Three patients had multiple aneurysms. Of a total of 15 aneurysms, 5 (33%) occurred on DAVF feeding arteries and 10 (67%) were in remote locations. These patients more commonly presented with hemorrhage (58% vs 20% for those without aneurysms). Aneurysms were associated with DAVFs in any location (feeding artery or remote), but flow-related feeding artery aneurysms were more likely to be associated with Borden Type III DAVFs.

Conclusions

Twenty-one percent of patients with cerebral DAVFs also had aneurysms in this patient cohort. It is thus prudent to perform 6-vessel digital subtraction angiography on patients with DAVFs to rule out potential feeding artery and remote aneurysms. This association may be explained by flow-related phenomena, the initial inciting event leading to DAVF formation, as well as a potential genetic component or predisposition to develop these lesions.