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Alexander G. Weil, Aria Fallah, Evan C. Lewis and Sanjiv Bhatia

OBJECTIVE

Insular lobe epilepsy (ILE) is an under-recognized cause of extratemporal epilepsy and explains some epilepsy surgery failures in children with drug-resistant epilepsy. The diagnosis of ILE usually requires invasive investigation with insular sampling; however, the location of the insula below the opercula and the dense middle cerebral artery vasculature renders its sampling challenging. Several techniques have been described, ranging from open direct placement of orthogonal subpial depth and strip electrodes through a craniotomy to frame-based stereotactic placement of orthogonal or oblique electrodes using stereo-electroencephalography principles. The authors describe an alternative method for sampling the insula, which involves placing insular depth electrodes along the long axis of the insula through the insular apex following dissection of the sylvian fissure in conjunction with subdural electrodes over the lateral hemispheric/opercular region. The authors report the feasibility, advantages, disadvantages, and role of this approach in investigating pediatric insular-opercular refractory epilepsy.

METHODS

The authors performed a retrospective analysis of all children (< 18 years old) who underwent invasive intracranial studies involving the insula between 2002 and 2015.

RESULTS

Eleven patients were included in the study (5 boys). The mean age at surgery was 7.6 years (range 0.5–16 years). All patients had drug-resistant epilepsy as defined by the International League Against Epilepsy and underwent comprehensive noninvasive epilepsy surgery workup. Intracranial monitoring was performed in all patients using 1 parasagittal insular electrode (1 patient had 2 electrodes) in addition to subdural grids and strips tailored to the suspected epileptogenic zone. In 10 patients, extraoperative monitoring was used; in 1 patient, intraoperative electrocorticography was used alone without extraoperative monitoring. The mean number of insular contacts was 6.8 (range 4–8), and the mean number of fronto-parieto-temporal hemispheric contacts was 61.7 (range 40–92). There were no complications related to placement of these depth electrodes. All 11 patients underwent subsequent resective surgery involving the insula.

CONCLUSIONS

Parasagittal transinsular apex depth electrode placement is a feasible alternative to orthogonally placed open or oblique-placed stereotactic methodologies. This method is safe and best suited for suspected unilateral cases with a possible extensive insular-opercular epileptogenic zone.

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George M. Ibrahim, Aria Fallah and R. Loch Macdonald

Object

At present, the administration of prophylactic antiepileptic medication following aneurysmal subarachnoid hemorrhage (SAH) is controversial, and the practice is heterogeneous. Here, the authors sought to inform clinical decision making by identifying factors associated with the occurrence of seizures following aneurysm rupture.

Methods

Exploratory analysis was performed on 413 patients enrolled in CONSCIOUS-1 (Clazosentan to Overcome Neurological Ischemia and Infarction Occurring after Subarachnoid Hemorrhage), a prospective randomized trial of clazosentan for the prevention of angiographic vasospasm. The association among clinical, laboratory, and radiographic covariates and the occurrence of seizures following SAH were determined. Covariates with a significance level of p < 0.20 on univariate analysis were entered into a multivariate logistic regression model. Receiver operating characteristic (ROC) curve analysis was used to define optimal predictive thresholds.

Results

Of the 413 patients enrolled in the study, 57 (13.8%) had at least 1 seizure following SAH. On univariate analysis, a World Federation of Neurosurgical Societies grade of IV–V, a greater subarachnoid clot burden, and the presence of midline shift and subdural hematomas were associated with seizure activity. On multivariate analysis, only a subarachnoid clot burden (OR 2.76, 95% CI 1.39–5.49) and subdural hematoma (OR 5.67, 95% CI 1.56–20.57) were associated with seizures following SAH. Using ROC curve analysis, the optimal predictive cutoff for subarachnoid clot burden was determined to be 21 (of a possible 30) on the Hijdra scale (area under the curve 0.63).

Conclusions

A greater subarachnoid clot burden and subdural hematoma are associated with the occurrence of seizures after aneurysm rupture. These findings may help to identify patients at greatest risk for seizures and guide informed decisions regarding the prescription of prophylactic anticonvulsive therapy. Clinical trial registration no.: NCT00111085 (ClinicalTrials.gov).

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Anna Lo Presti, Alexander G. Weil, Aria Fallah, Eric C. Peterson, Toba N. Niazi and Sanjiv Bhatia

Sickle cell disease (SCD) is an autosomal recessive hematological disorder, characterized by sickling of the red blood cells in response to a hypoxic stress and vaso-occlusive crises. It is associated with moyamoya-like changes on cerebral angiographic imaging in 43% of patients. Cerebral aneurysms, arteriovenous malformations, and dural arteriovenous fistulas (AVFs) have been described in association with SCD and moyamoya disease. However, the description of a pial AVF (pAVF) in a patient with SCD and/or moyamoya formation has not yet been reported. The authors present the case of a 15-year-old boy with SCD-associated moyamoya disease harboring a pAVF who developed a de novo venous aneurysm 8 months after undergoing indirect superficial temporal artery-middle cerebral artery (MCA) bypass that was complicated by bilateral ischemia of the MCA territory. The pAVF was successfully treated with transarterial embolization using Onyx. The authors describe the possible pathophysiological mechanisms and management strategies for this rare occurrence.

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Alexander G. Weil, Aria Fallah, Parthasarathi Chamiraju, John Ragheb and Sanjiv Bhatia

OBJECT

Combining endoscopic third ventriculostomy (ETV) with choroid plexus cauterization (CPC) has been shown to improve the success rate compared with ETV alone in infants (less than 24 months) with hydrocephalus who were treated in developing countries. The authors sought to evaluate the safety and efficacy of this procedure, using a rigid neuroendoscope, in a single North American center, and to assess whether the ETV success score (ETVSS), the CURE Children’s Hospital of Uganda ETVSS (CCHU ETVSS), and other pre- and intraoperative variables could predict success.

METHODS

The authors performed a retrospective review of consecutive ETV/CPC procedures performed using a rigid neuroendoscope to treat infantile hydrocephalus. The infants underwent the procedure at Miami Children’s Hospital between January 2007 and 2014, with at least one postoperative follow-up. Duration of follow-up or time to failure of ETV/CPC, the primary outcome measure, was documented. A repeat CSF diversion procedure or death was considered as a failure of ETV/CPC. The time to event was measured using a Kaplan-Meier analysis. The authors analyzed ETVSS, CCHU ETVSS, and pre- and intraoperative variables to determine their suitability to predict success.

RESULTS

Eighty-five patients (45 boys) with a mean age of 4.3 months (range 1 day to 20 months) underwent ETV/CPC. Etiology included intraventricular hemorrhage of prematurity in 44 patients (51.7%), myelomeningocele (MMC) in 7 (8.2%), congenital aqueductal stenosis in 12 (14.1%), congenital communicating hydrocephalus in 6 (7.1%), Dandy-Walker complex in 6 (7.1%), postinfectious hydrocephalus in 5 (5.8%), and other cause in 5 (5.8%). Six procedure-related complications occurred in 5 (5.8%) patients, including 2 hygromas, 1 CSF leak, and 3 infections. There were 3 mortalities in this cohort. ETV/CPC was successful in 42.1%, 37.7%, and 36.8% of patients at 6, 12, and 24 months follow-up, respectively. The median (95% CI) time to ETV/CPC failure was 4.0 months (0.9–7.1 months). In univariate analyses, both the ETVSS (hazard ratio [HR] 1.03; 95% CI 1.01–1.05; p = 0.004) and CCHU ETVSS (HR 1.48; 95% CI 1.04–2.09; p = .028) were predictive of outcome following ETV/CPC. In multivariate analysis, the presence of prepontine scarring was associated with ETV/CPC failure (HR 0.34; 95% CI 0.19–0.63; p < 0.001). Other variables, such as radiological criteria (prepontine interval, prepontine space, aqueductal stenosis, Third Ventricular Morphology Index) and intraoperative findings (ventriculostomy pulsations, extent of CPC), did not predict outcome.

CONCLUSIONS

ETV/CPC is a feasible alternative to ETV and ventriculoperitoneal shunt in infants with hydrocephalus. Both the ETVSS and CCHU ETVSS predicted success following ETV/CPC in this single-center North American cohort of patients.

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Editorial

Perioperative steroids in spine surgery

Michael G. Fehlings and Aria Fallah

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Alexander G. Weil, Ngoc Minh D. Le, Prasanna Jayakar, Trevor Resnick, Ian Miller, Aria Fallah, Michael Duchowny and Sanjiv Bhatia

OBJECTIVE

Seizure onset in the insular cortex as a cause of refractory epilepsy is underrepresented in the pediatric population, possibly due to difficulties localizing seizure onset in deep anatomical structures and limited surgical access to the insula, a complex anatomical structure with a rich overlying vascular network. Insular seizure semiology may mimic frontal, temporal, or parietal lobe semiology, resulting in false localization, incomplete resection, and poor outcome.

METHODS

The authors retrospectively reviewed the records of all pediatric patients who underwent insular cortical resections for intractable epilepsy at Miami Children's Hospital from 2009 to 2015. Presurgical evaluation included video electroencephalography monitoring and anatomical/functional neuroimaging. All patients underwent excisional procedures utilizing intraoperative electrocorticography or extraoperative subdural/depth electrode recording.

RESULTS

Thirteen children (age range 6 months–16 years) with intractable focal epilepsy underwent insular-opercular resection. Seven children described symptoms that were suggestive of insular seizure origin. Discharges on scalp EEG revealed wide fields. Four patients were MRI negative (i.e., there were no insular or brain abnormalities on MRI), 4 demonstrated insular signal abnormalities, and 5 had extrainsular abnormalities. Ten patients had insular involvement on PET/SPECT. All patients underwent invasive investigation with insular sampling; in 2 patients resection was based on intraoperative electrocorticography, whereas 11 underwent surgery after invasive EEG monitoring with extraoperative monitoring. Four patients required an extended insular resection after a failed initial surgery. Postoperatively, 2 patients had transient hemiplegia. No patients had new permanent neurological deficits. At the most recent follow-up (mean 43.8 months), 9 (69%) children were seizure free and 1 had greater than 90% seizure reduction.

CONCLUSIONS

Primary insular seizure origin should be considered in children with treatment-resistant focal seizures that are believed to arise within the perisylvian region based on semiology, widespread electrical field on scalp EEG, or insular abnormality on anatomical/functional neuroimaging. There is a reasonable chance of seizure freedom in this group of patients, and the surgical risks are low.

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Aria Fallah, Alexander G. Weil, Samir Sur, Ian Miller, Prasanna Jayakar, Glenn Morrison, Sanjiv Bhatia and John Ragheb

OBJECT

Pediatric brain tumors may be associated with medically intractable epilepsy for which surgery is indicated. The authors sought to evaluate the efficacy of epilepsy surgery for seizure control in pediatric patients with brain tumors.

METHODS

The authors performed a retrospective review of consecutive patients undergoing resective epilepsy surgery related to pediatric brain tumors at Miami Children’s Hospital between June 1986 and June 2014. Time-to-event analysis for seizure recurrence was performed; an “event” was defined as any seizures that occurred following resective epilepsy surgery, not including seizures and auras in the 1st postoperative week. The authors analyzed several preoperative variables to determine their suitability to predict seizure recurrence following surgery.

RESULTS

Eighty-four patients (47 males) with a mean age (± standard deviation) of 8.7 ± 5.5 years (range 0.5–21.6 years) were included. The study included 39 (46%) patients with gliomas, 20 (24%) with dysembryoplastic neuroepithelial tumors (DNETs), 14 (17%) with gangliogliomas, and 11 (13%) with other etiologies. Among the patients with gliomas, 18 were classified with low-grade glioma, 5 had oligodendroglioma, 6 had uncategorized astrocytoma, 3 had pilocytic astrocytoma, 3 had pleomorphic xanthoastrocytoma, 3 had glioblastoma, and 1 had gliomatosis cerebri. Seventy-nine (94.0%) resections were guided by intraoperative electrocorticography (ECoG). The mean time (± standard deviation) to seizure recurrence was 81.8 ± 6.3 months. Engel Class I outcome was achieved in 66 (78%) and 63 (75%) patients at 1 and 2 years’ follow-up, respectively. Patients with ganglioglioma demonstrated the highest probability of long-term seizure freedom, followed by patients with DNETs and gliomas. In univariate analyses, temporal location (HR 1.75, 95% CI 0.26–1.27, p = 0.171) and completeness of resection (HR 1.69, 95% CI 0.77–3.74, p = 0.191) demonstrated a trend toward a longer duration of seizure freedom.

CONCLUSIONS

ECoG-guided epilepsy surgery for pediatric patients with brain tumors is highly effective. Tumors located in the temporal lobe and those in which a complete ECoG-guided resection is performed may result in a greater likelihood of long-term seizure freedom.

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Shelly Wang, Scellig Stone, Alexander G. Weil, Aria Fallah, Benjamin C. Warf, John Ragheb, Sanjiv Bhatia and Abhaya V. Kulkarni

OBJECTIVE

Endoscopic third ventriculostomy (ETV)/choroid plexus cauterization (CPC) has become an increasingly common technique for the treatment of infant hydrocephalus. Both flexible and rigid neuroendoscopy can be used, with little empirical evidence directly comparing the two. Therefore, the authors used a propensity score–matched cohort and survival analysis to assess the comparative efficacy of flexible and rigid neuroendoscopy.

METHODS

Individual data were collected through retrospective review of infants younger than 2 years of age, treated at 1 of 2 hospitals: 1) Boston Children's Hospital, exclusively utilizing flexible neuroendoscopy, and 2) Nicklaus Children's Hospital-Jackson Memorial Hospital, exclusively utilizing rigid neuroendoscopy. Patient characteristics and postoperative outcomes were assessed. A propensity score model was developed to balance patient characteristics in the case mix.

RESULTS

A propensity score model for neuroendoscope type was developed with 5 independent variables: chronological age, sex, hydrocephalus etiology, prior CSF diversion, and prepontine scarring. Propensity score decile-adjusted and 1-to-1 nearest-neighbor matching analysis revealed that compared with flexible neuroendoscopy, rigid neuroendoscopy had an ETV/CPC failure odds ratio (OR) of 1.43 (p = 0.31) and 1.31 (p = 0.47), respectively, compared with an unadjusted OR of 2.40 (p = 0.034). Furthermore, in a Cox regression analysis controlled by propensity score, rigid neuroendoscopy had a hazard ratio (HR) of 1.10 (p = 0.70), compared with an unadjusted HR of 1.61 (p = 0.031).

CONCLUSIONS

Although unadjusted analysis suggested worse ETV/CPC outcomes for infants treated by rigid neuroendoscopy, much of the difference could be attributed to the case mix and other predictors of outcome. A larger sample observational study or randomized controlled trials are required to provide evidence-based guidelines on ETV/CPC technique.

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Marie-Andrée Coulombe, Lior M. Elkaim, Naif M. Alotaibi, Daniel A. Gorman, Alexander G. Weil, Aria Fallah, Suneil K. Kalia, Nir Lipsman, Andres M. Lozano and George M. Ibrahim

OBJECTIVE

Gilles de la Tourette syndrome (GTS) is a disorder characterized by motor and vocal tics. Although by definition the onset of GTS is before age 18 years, clinical trials of deep brain stimulation (DBS) have been conducted only in adults. Using individual participant data (IPD) meta-analysis methodology, the current study investigated the safety and efficacy of DBS as a treatment for GTS in children and youth.

METHODS

A systematic review with no date or language restrictions was performed according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement. Three electronic databases were searched: PubMed, EMBASE, and Web of Science. From 843 articles screened, the IPD of 58 children and youth (ages 12–21 years) extracted from 21 articles were collected and analyzed. A mixed-effects univariable analysis followed by multivariable hierarchical regression was performed using change in the Yale Global Tic Severity Scale (YGTSS) score as the primary outcome and reported measures of comorbidities as secondary outcomes.

RESULTS

The authors’ results showed an average improvement of 57.5% ± 24.6% across studies on the YGTSS. They also found that comorbid depression and stimulation pulse width each correlated negatively with outcome (p < 0.05). In patients with less severe GTS, greater improvements were evident following thalamic stimulation. More than one-quarter (n = 16, 27.6%) of participants experienced side effects, the majority of which were minor.

CONCLUSIONS

DBS in the pediatric population may be an effective option with a moderate safety profile for treatment of GTS in carefully selected children and youth. Large, prospective studies with long-term follow-up are necessary to understand how DBS influences tic symptoms and may alter the natural course of GTS in children.

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Michael G. Fehlings and Aria Fallah