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Jared Narvid, Matthew R. Amans, Daniel L. Cooke, Steven W. Hetts, William P. Dillon, Randall T. Higashida, Christopher F. Dowd, and Van V. Halbach

OBJECT

Retroclival hematomas are rare, appearing mostly as posttraumatic phenomena in children. Spontaneous retroclival hematoma (SRH) in the absence of trauma also has few descriptions in the literature. None of the reported clinical cases features the combination of an SRH and intraventricular hemorrhage (IVH). Nevertheless, despite extensive cases of idiopathic or angiographically negative subarachnoid hemorrhage (SAH) of the posterior fossa, only a single case report of a patient with a unique spontaneous retroclival hematoma has been identified. In this study, the authors reviewed the presentation, management, and clinical outcome of this rare entity.

METHODS

The authors performed a retrospective analysis of all patients with diagnosed SRH at their institution over a 3-year period. Collected data included clinical history, laboratory results, treatment, and review of all imaging studies performed.

RESULTS

Four patients had SRH. All were appropriately evaluated for coagulopathic and/or traumatic etiologies of hemorrhage, though no etiology could be found. Moreover, all of the patients demonstrated SRH that both clearly crossed the basioccipital synchondrosis and was contained within a nondependent configuration along the retroclival dura mater.

CONCLUSIONS

Spontaneous retroclival hematoma, often associated with IVH, is a rare subtype of intracranial hemorrhage frequently recognized only when MRI demonstrates compartmentalization of the posterior fossa hemorrhage. When angiography fails to reveal an underlying lesion, SRH patients, like patients with traditional angiographically negative SAH, enjoy a remarkably good prognosis.

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Fabio Settecase, Andrew D. Nicholson, Matthew R. Amans, Randall T. Higashida, Van V. Halbach, Daniel L. Cooke, Christopher F. Dowd, and Steven W. Hetts

A 13-year-old boy with meningiomatosis, McCune-Albright syndrome, and gray platelet syndrome presented with an enlarging “lump” on his right forehead. A head CT scan revealed a polyostotic fibrous dysplasia involving the entire skull. A 3.4-cm right frontal osseous cavity and an overlying right forehead subcutaneous soft-tissue mass were seen, measuring 5.2 cm in diameter and 1.6 cm thick. Ultrasound of the cavity and overlying mass showed swirling of blood and an arterialized waveform. MRI revealed an en plaque meningioma underlying the cavity. An intraosseous pseudoaneurysm fed by 3 distal anterior division branches of the right middle meningeal artery (MMA) with contrast extravasation was found on angiography. Two MMA feeders were embolized with Onyx, with anterograde filling of the intraosseous cavity with Onyx. A small pocket of residual intracavity contrast filling postembolization from a smaller third MMA feeder eventually thrombosed and the forehead lump regressed.

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Sara C. LaHue, Helen Kim, Ludmila Pawlikowska, Jeffrey Nelson, Daniel L. Cooke, Steven W. Hetts, and Vineeta Singh

OBJECTIVE

The pathogenesis of dural arteriovenous fistulas (DAVFs) remains poorly defined. Prior studies on thrombophilia as a risk factor for DAVF development are limited by small sample sizes and poor generalizability.

METHODS

In this longitudinal observational study, all patients with intracranial DAVFs evaluated at the University of California, San Francisco from December 1994 through April 2014 were identified. After obtaining patient consent, 3 thrombophilic mutations, factor V Leiden (rs6025), MTHFR (rs1801133), and prothrombin G20210A, were genotyped. The authors evaluated the association of thrombophilia status (presence of any thrombophilic mutation) and clinical and angiographic characteristics using either a 2-sample t-test or Fisher’s exact test.

RESULTS

A total of 116 patients with diagnosed intracranial DAVFs were included in the study. Twenty-five (22%) patients met criteria for thrombophilia. Focal neurological deficits tended to occur more frequently in the thrombophilia group (78% vs 57%, p = 0.09). Angiographic characteristics of DAVFs, including high-risk venous flow pattern, multiplicity of DAVF, and the presence of venous sinus thrombosis, did not differ significantly between the 2 groups but tended to be more common in the thrombophilic than in the nonthrombophilic group.

CONCLUSIONS

This study is one of the largest of thrombophilia and DAVF to date. The frequency of mutations associated with thrombophilia in this study was higher than that in the general population.

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Sabino Luzzi, Mattia Del Maestro, and Renato Galzio

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Sara C. LaHue, Helen Kim, Ludmila Pawlikowska, Jeffrey Nelson, Daniel L. Cooke, Steven W. Hetts, and Vineeta Singh

OBJECTIVE

The pathogenesis of dural arteriovenous fistulas (DAVFs) remains poorly defined. Prior studies on thrombophilia as a risk factor for DAVF development are limited by small sample sizes and poor generalizability.

METHODS

In this longitudinal observational study, all patients with intracranial DAVFs evaluated at the University of California, San Francisco from December 1994 through April 2014 were identified. After obtaining patient consent, 3 thrombophilic mutations, factor V Leiden (rs6025), MTHFR (rs1801133), and prothrombin G20210A, were genotyped. The authors evaluated the association of thrombophilia status (presence of any thrombophilic mutation) and clinical and angiographic characteristics using either a 2-sample t-test or Fisher’s exact test.

RESULTS

A total of 116 patients with diagnosed intracranial DAVFs were included in the study. Twenty-five (22%) patients met criteria for thrombophilia. Focal neurological deficits tended to occur more frequently in the thrombophilia group (78% vs 57%, p = 0.09). Angiographic characteristics of DAVFs, including high-risk venous flow pattern, multiplicity of DAVF, and the presence of venous sinus thrombosis, did not differ significantly between the 2 groups but tended to be more common in the thrombophilic than in the nonthrombophilic group.

CONCLUSIONS

This study is one of the largest of thrombophilia and DAVF to date. The frequency of mutations associated with thrombophilia in this study was higher than that in the general population.

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Steven W. Hetts, Parham Moftakhar, Neil Maluste, Heather J. Fullerton, Daniel L. Cooke, Matthew R. Amans, Christopher F. Dowd, Randall T. Higashida, and Van V. Halbach

OBJECTIVE

Intracranial dural arteriovenous fistulas (DAVFs) are rare in children. This study sought to better characterize DAVF presentation, angioarchitecture, and treatment outcomes.

METHODS

Children with intracranial DAVFs between 1986 and 2013 were retrospectively identified from the neurointerventional database at the authors' institution. Demographics, clinical presentation, lesion angioarchitecture, treatment approaches, angiographic outcomes, and clinical outcomes were assessed.

RESULTS

DAVFs constituted 5.7% (22/423) of pediatric intracranial arteriovenous shunting lesions. Twelve boys and 10 girls presented between 1 day and 18 years of age; boys presented at a median of 1.3 years and girls presented at a median of 4.9 years. Four of 8 patients ≤ 1 year of age presented with congestive heart failure compared with 0/14 patients > 1 year of age (p = 0.01). Five of 8 patients ≤ 1 year old presented with respiratory distress compared with 0/14 patients > 1 year old (p = 0.0021). Ten of 14 patients > 1 year old presented with focal neurological deficits compared with 0/8 patients ≤ 1 year old (p = 0.0017). At initial angiography, 16 patients harbored a single intracranial DAVF and 6 patients had 2–6 DAVFs. Eight patients (38%) experienced DAVF obliteration by the end of treatment. Good clinical outcome (modified Rankin Scale score 0–2) was documented in 77% of patients > 1 year old at presentation compared with 57% of patients ≤ 1 year old at presentation. Six patients (27%) died.

CONCLUSIONS

Young children with DAVFs presented predominantly with cardiopulmonary symptoms, while older children presented with focal neurological deficits. Compared with other pediatric vascular shunts, DAVFs had lower rates of angiographic obliteration and poorer clinical outcomes.

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Parham Moftakhar, Daniel L. Cooke, Heather J. Fullerton, Nerissa U. Ko, Matthew R. Amans, Jared A. Narvid, Christopher F. Dowd, Randall T. Higashida, Van V. Halbach, and Steven W. Hetts

OBJECT

Although the development and prevalence of cerebral vasospasm (CV) has been extensively investigated in adults, little data exist on the development of CV in children. The authors hypothesized that even though children have highly vasoreactive arteries, because of a robust cerebral collateral blood flow, they rarely develop symptomatic CV.

METHODS

The authors retrospectively reviewed their university hospital's neurointerventional database for children (that is, patients ≤ 18 years) who were examined or treated for aneurysmal or traumatic subarachnoid hemorrhage (SAH) during the period 1990–2013. Images from digital subtraction angiography (DSA) were analyzed for the extent of CV and collateralization of the cerebral circulation. Results from transcranial Doppler (TCD) ultrasonography were correlated with those from DSA. Cerebral vasospasm on TCD ultrasonography was defined according to criteria developed for adults. Clinical outcomes of CV were assessed with the pediatric modified Rankin Scale (mRS).

RESULTS

Among 37 children (21 boys and 16 girls ranging in age from 8 months to 18 years) showing symptoms of an aneurysmal SAH (comprising 32 aneurysms and 5 traumatic pseudoaneurysms), 17 (46%) had CV confirmed by DSA; CV was mild in 21% of these children, moderate in 50%, and severe in 29%. Only 3 children exhibited symptomatic CV, all of whom had poor collateralization of cerebral vessels. Among the 14 asymptomatic children, 10 (71%) showed some degree of vessel collateralization. Among 16 children for whom TCD data were available that could be correlated with the DSA findings, 13 (81%) had CV according to TCD criteria. The sensitivity and specificity of TCD ultrasonography for diagnosing CV were 95% and 59%, respectively. The time to CV onset detected by TCD ultrasonography was 5 ± 3 days (range 2–10 days). Twenty-five (68%) of the children had good long-term outcomes (that is, had mRS scores of 0–2).

CONCLUSIONS

Children have a relatively high incidence of angiographically detectable, moderate-to-severe CV. Children rarely develop symptomatic CV and have good long-term outcomes, perhaps due to robust cerebral collateral blood flow. Criteria developed for detecting CV with TCD ultrasonography in adults overestimate the prevalence of CV in children. Larger studies are needed to define TCD ultrasonography–based CV criteria for children.

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Grace F. Donzelli, Jeffrey Nelson, David McCoy, Charles E. McCulloch, Steven W. Hetts, Matthew R. Amans, Christopher F. Dowd, Van V. Halbach, Randall T. Higashida, Michael T. Lawton, Helen Kim, and Daniel L. Cooke

OBJECTIVE

Preoperative embolization of brain arteriovenous malformations (AVMs) is performed to facilitate resection, although its impact on surgical performance has not been clearly defined. The authors tested for associations between embolization and surgical performance metrics.

METHODS

The authors analyzed AVM cases resected by one neurosurgeon from 2006 to 2017. They tested whether cases with and without embolization differed from one another with respect to patient and AVM characteristics using t-tests for continuous variables and Fisher’s exact tests for categorical variables. They used simple and multivariable regression models to test whether surgical outcomes (blood loss, resection time, surgical clip usage, and modified Rankin Scale [mRS] score) were associated with embolization. Additional regression analyses integrated the peak arterial afferent contrast normalized for the size of the region of interest (Cmax/ROI) into models as an additional predictor.

RESULTS

The authors included 319 patients, of whom 151 (47%) had preoperative embolization. Embolized AVMs tended to be larger (38% with diameter > 3 cm vs 19%, p = 0.001), less likely to have hemorrhaged (48% vs 63%, p = 0.013), or be diffuse (19% vs 29%, p = 0.045). Embolized AVMs were more likely to have both superficial and deep venous drainage and less likely to have exclusively deep drainage (32% vs 17% and 12% vs 23%, respectively; p = 0.002). In multivariable analysis, embolization was not a significant predictor of blood loss or mRS score changes, but did predict longer operating times (+29 minutes, 95% CI 2–56 minutes; p = 0.034) and increased clip usage (OR 2.61, 95% CI 1.45–4.71; p = 0.001). Cmax/ROI was not a significant predictor, although cases with large Cmax/ROI tended to have longer procedure times (+25 minutes per doubling of Cmax/ROI, 95% CI 0–50 minutes; p = 0.051).

CONCLUSIONS

In this series, preoperative embolization was associated with longer median resection times and had no association with intraoperative blood loss or mRS score changes.

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Joseph H. Garcia, Ethan A. Winkler, Ramin A. Morshed, Alex Lu, Simon G. Ammanuel, Satvir Saggi, Elaina J. Wang, Steve Braunstein, Christine K. Fox, Heather J. Fullerton, Helen Kim, Daniel L. Cooke, Steven W. Hetts, Michael T. Lawton, Adib A. Abla, and Nalin Gupta

OBJECTIVE

Children with cerebral arteriovenous malformations (AVMs) can present with seizures, potentially increasing morbidity and impacting clinical management. However, the factors that lead to seizures as a presenting sign are not well defined. While AVM-related seizures have been described in case series, most studies have focused on adults and have included patients who developed seizures after an AVM rupture. To address this, the authors sought to analyze demographic and morphological characteristics of AVMs in a large cohort of children.

METHODS

The demographic, clinical, and AVM morphological characteristics of 189 pediatric patients from a single-center database were studied. Univariate and multivariate logistic regression models were used to test the effect of these characteristics on seizures as an initial presenting symptom in patients with unruptured brain AVMs.

RESULTS

Overall, 28 of 189 patients initially presented with seizures (14.8%). By univariate comparison, frontal lobe location (p = 0.02), larger AVM size (p = 0.003), older patient age (p = 0.04), and the Supplemented Spetzler-Martin (Supp-SM) grade (0.0006) were associated with seizure presentation. Multivariate analysis confirmed an independent effect of frontal lobe AVM location and higher Supp-SM grade. All patients presenting with seizures had AVMs in the cortex or subcortical white matter.

CONCLUSIONS

While children and adults share some risk factors for seizure presentation, their risk factor profiles do not entirely overlap. Pediatric patients with cortical AVMs in the frontal lobe were more likely to present with seizures. Additionally, the Supp-SM grade was highly associated with seizure presentation. Future clinical research should focus on the effect of therapeutic interventions targeting AVMs on seizure control in these patients.

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Joseph H. Garcia, Caleb Rutledge, Ethan A. Winkler, Luis Carrete, Ramin A. Morshed, Alex Y. Lu, Satvir Saggi, Christine K. Fox, Heather J. Fullerton, Helen Kim, Daniel L. Cooke, Steven W. Hetts, Michael T. Lawton, Nalin Gupta, and Adib A. Abla

OBJECTIVE

Pediatric brain arteriovenous malformations (AVMs) are the leading cause of spontaneous intracranial hemorrhage (SICH) in children. Although the incidence of SICH is low in pediatric populations, such events cause substantial morbidity. The recently created Ruptured Arteriovenous Malformation Grading Scale (RAGS) is proposed as a reliable and novel grading system to specifically serve as a predictor of clinical outcomes in patients following AVM rupture, similar to the Hunt and Hess (HH) grade for ruptured aneurysms. While these data are promising, pediatric patients were notably absent from the original study validating the RAGS. Therefore, correlation of the RAGS score with clinical outcomes following AVM rupture in individuals younger than 18 years of age using the RAGS score is needed. The objective of this study was to validate the RAGS in a cohort of pediatric patients with AVMs who presented with hemorrhage, thereby demonstrating the score’s generalizability, and expanding its external validity.

METHODS

A cohort of children with ruptured AVMs were retrospectively reviewed. Using disability, measured by the modified Rankin Scale (mRS), as the response variable, the area under the receiver operating characteristic curve (AUROC) was calculated for patients based on their RAGS scores for three time periods. The AUROC values were then compared with those generated by two commonly used clinical grading systems, the HH classification and Glasgow Coma Scale.

RESULTS

A total of 81 children who presented with ruptured AVMs were included in the study, with a mean follow-up duration of 4 years. The RAGS score outperformed other clinical grading scales in predicting mRS scores, with AUROC values of 0.81, 0.82, and 0.81 at three distinct follow-up periods.

CONCLUSIONS

The RAGS score correlated well with the clinical outcome after AVM rupture in pediatric patients. Additional validation studies across multiple treatment centers are needed to further demonstrate the generalizability of the scoring system.