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Jeffrey P. Blount, Wayne Langburt, Hiroshi Otsubo, Shiro Chitoku, Ayako Ochi, Shelly Weiss, O. Carter Snead and James T. Rutka

Object. The technique involved in multiple subpial transections (MSTs) allows the surgeon treating patients with epilepsy the capability to make disconnective lesions in epileptogenic regions of eloquent cortex. Although there have been increasing numbers of reports in adults of the efficacy and relative safety of this technique, there are relatively few such reports in children. The authors present their experience in 30 children who underwent MSTs during the surgical management of the seizure disorder.

Methods. Thirty consecutive children who underwent MSTs with or without cortical excision form the basis of this retrospective review. An analysis of neurological adverse effects following MSTs and seizure outcome was performed.

Between 1996 and 2000, MSTs were performed either as stand-alone therapy (four patients) or in conjunction with planned cortical excisions (26 patients). Twenty-three children underwent invasive monitoring after placement of subdural grid electrodes, and in seven intraoperative electrocorticography alone was performed. The mean follow-up period for the group was 3.5 years (minimum 30 months in all cases). All 20 patients in whom MSTs were performed in the primary motor cortex experienced transient hemiparesis (mild in 12 and moderate in eight) lasting up to 6 weeks; however, no patient suffered a permanent motor deficit in the long-term follow-up period. In 26 patients who underwent cortical resections followed by MSTs, 12 (46%) were seizure free (Engel Class I) following surgery. Eleven patients (42%) (Engel Classes II and III) continued to suffer seizures but improvement in seizure control was adequate following surgery. In the 23 patients in whom subdural grids were placed to capture the ictal onset zone by invasive video-electroencephalography, MSTs comprised a mean of 37% of the surgically treated area under the grid.

Conclusions. The results of this series demonstrate that MSTs can be performed with acceptable morbidity in children undergoing epilepsy surgery. The precise role of MSTs in controlling seizure frequency and outcome, especially when combined with planned cortical resections, awaits further study.

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Çagatay Önal, Hiroshi Otsubo, Takashi Araki, Shiro Chitoku, Ayako Ochi, Shelly Weiss, William Logan, Irene Elliott, O. Carter Snead III and James T. Rutka

Object. This study was performed to evaluate the complications of invasive subdural grid monitoring during epilepsy surgery in children.

Methods. The authors retrospectively reviewed the records of 35 consecutive children with intractable localization-related epilepsy who underwent invasive video electroencephalography (EEG) with subdural grid electrodes at The Hospital for Sick Children between 1996 and 2001. After subdural grid monitoring and identification of the epileptic regions, cortical excisions and/or multiple subpial transections (MSTs) were performed. Complications after these procedures were then categorized as either surgical or neurological.

There were 17 male and 18 female patients whose mean age was 11.7 years. The duration of epilepsy before surgery ranged from 2 to 17 years (mean 8.3 years). Fifteen children (43%) had previously undergone surgical procedures for epilepsy. The number of electrodes on the grids ranged from 40 to 117 (mean 95). During invasive video EEG, cerebrospinal fluid leaks occurred in seven patients. Also, cerebral edema (five patients), subdural hematoma (five patients), and intracerebral hematoma (three patients) were observed on postprocedural imaging studies but did not require surgical intervention. Hypertrophic scars on the scalp were observed in nine patients. There were three infections, including one case of osteomyelitis and two superficial wound infections. Blood loss and the amounts of subsequent transfusions correlated directly with the size and number of electrodes on the grids (p < 0.001). Twenty-eight children derived significant benefit from cortical resections and MSTs, with a more than 50% reduction of seizures and a mean follow-up period of 30 months.

Conclusions. The results of this study indicate that carefully selected pediatric patients with intractable epilepsy can benefit from subdural invasive monitoring procedures that entail definite but acceptable risks.

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Koji Iida, Hiroshi Otsubo, Yuuri Matsumoto, Ayako Ochi, Makoto Oishi, Stephanie Holowka, Elizabeth Pang, Irene Elliott, Shelly K. Weiss, Sylvester H. Chuang, O. Carter Snead III and James T. Rutka

Object. The authors sought to validate magnetoencephalography spike sources (MEGSSs) in neuronavigation during epilepsy surgery in pediatric patients.

Methods. The distributions of MEGSSs in 16 children were defined and classified as clusters (Class I), greater than or equal to 20 MEGSSs with 1 cm or less between MEGSSs; small clusters (Class II), 6 to 19 with 1 cm or less between; and scatters (Class III), less than 6 or greater than 1 cm between spike sources. Using neuronavigation, the MEGSSs were correlated to epileptic zones from intra- and extraoperative electrocorticography (ECoG), surgical procedures, disease entities, and seizure outcomes.

Thirteen patients underwent MEGSSs: nine had clusters; two had small clusters, one with and one without clusters; and three had scatters alone. All 13 had scatters. Clusters localized within and extended from areas of cortical dysplasia and at margins of tumors or cystic lesions. All clusters were colocalized to ECoG-defined epileptic zones. Four of six patients with clusters and/or small clusters underwent complete excisions, and two underwent partial excision with or without multiple subpial transections. In the three patients with scatters alone, ECoG revealed epileptic zones buried within MEGSS areas; these regions of scatters were completely excised and treated with multiple subpial transections. Coexisting scatters were left untreated in nine of 10 patients. Postoperatively, nine of 13 patients were seizure free; the four patients with residual seizures had clusters in unresected eloquent cortex. Three patients in whom no MEGSSs were demonstrated underwent lesionectomies and were seizure free.

Conclusions. Magnetoencephalography spike source clusters indicate an epileptic zone requiring complete excision. Coexisting scatters remote from clusters are nonepileptogenic and do not require excision. Scatters alone, however, should be examined by ECoG; an epileptic zone may exist within these distributions.

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Erin N. Kiehna, Elysa Widjaja, Stephanie Holowka, O. Carter Snead III, James Drake, Shelly K. Weiss, Ayako Ochi, Eric M. Thompson, Cristina Go, Hiroshi Otsubo, Elizabeth J. Donner and James T. Rutka

OBJECT

Hemispherectomy for unilateral, medically refractory epilepsy is associated with excellent long-term seizure control. However, for patients with recurrent seizures following disconnection, workup and investigation can be challenging, and surgical options may be limited. Few studies have examined the role of repeat hemispherotomy in these patients. The authors hypothesized that residual fiber connections between the hemispheres could be the underlying cause of recurrent epilepsy in these patients. Diffusion tensor imaging (DTI) was used to test this hypothesis, and to target residual connections at reoperation using neuronavigation.

METHODS

The authors identified 8 patients with recurrent seizures following hemispherectomy who underwent surgery between 1995 and 2012. Prolonged video electroencephalography recordings documented persistent seizures arising from the affected hemisphere. In all patients, DTI demonstrated residual white matter association fibers connecting the hemispheres. A repeat craniotomy and neuronavigation-guided targeted disconnection of these residual fibers was performed. Engel class was used to determine outcome after surgery at a minimum of 2 years of follow-up.

RESULTS

Two patients underwent initial hemidecortication and 6 had periinsular hemispherotomy as their first procedures at a median age of 9.7 months. Initial pathologies included hemimegalencephaly (n = 4), multilobar cortical dysplasia (n = 3), and Rasmussen's encephalitis (n = 1). The mean duration of seizure freedom for the group after the initial procedure was 32.5 months (range 6–77 months). In all patients, DTI showed limited but definite residual connections between the 2 hemispheres, primarily across the rostrum/genu of the corpus callosum. The median age at reoperation was 6.8 years (range 1.3–14 years). The average time taken for reoperation was 3 hours (range 1.8–4.3 hours), with a mean blood loss of 150 ml (range 50–250 ml). One patient required a blood transfusion. Five patients are seizure free, and the remaining 3 patients are Engel Class II, with a minimum follow-up of 24 months for the group.

CONCLUSIONS

Repeat hemispherotomy is an option for consideration in patients with recurrent intractable epilepsy following failed surgery for catastrophic epilepsy. In conjunction with other modalities to establish seizure onset zones, advanced MRI and DTI sequences may be of value in identifying patients with residual connectivity between the affected and unaffected hemispheres. Targeted disconnection of these residual areas of connectivity using neuronavigation may result in improved seizure outcomes, with minimal and acceptable morbidity.

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Shobhan Vachhrajani, Sandrine de Ribaupierre, Hiroshi Otsubo, Ayako Ochi, Shelly K. Weiss, Elizabeth J. Donner, Elysa Widjaja, Elizabeth Kerr, Mary Lou Smith, James Drake, O. Carter Snead III and James T. Rutka

Object

Pediatric frontal lobe epilepsy (FLE) remains a challenging condition for neurosurgeons and epileptologists to manage. Postoperative seizure outcomes remain far inferior to those observed in temporal lobe epilepsies, possibly due to inherent difficulties in delineating and subsequently completely resecting responsible epileptogenic regions. In this study, the authors review their institutional experience with the surgical management of FLE and attempt to find predictors that may help to improve seizure outcome in this population.

Methods

All surgically treated cases of intractable FLE from 1990 to 2008 were reviewed. Demographic information, preoperative and intraoperative imaging and electrophysiological investigations, and follow-up seizure outcome were assessed. Inferential statistics were performed to look for potential predictors of seizure outcome.

Results

Forty patients (20 male, 20 female) underwent surgical management of FLE during the study period. Patients were an average of 5.6 years old at the time of FLE onset and 11.7 years at the time of surgery; patients were followed for a mean of 40.25 months. Most patients displayed typical FLE semiology. Twenty-eight patients had discrete lesions identified on MRI. Eight patients underwent 2 operations. Cortical dysplasia was the most common pathological diagnosis. Engel Class I outcome was obtained in 25 patients (62.5%), while Engel Class II outcome was observed in 5 patients (12.5%). No statistically significant predictors of outcome were found.

Conclusions

Control of FLE remains a challenging problem. Favorable seizure outcome, obtained in 62% of patients in this series, is still not as easily obtained in FLE as it is in temporal lobe epilepsy. While no statistically significant predictors of seizure outcome were revealed in this study, patients with FLE continue to require extensive workup and investigation to arrive at a logical and comprehensive neurosurgical treatment plan. Future studies with improved neuroimaging and advanced invasive monitoring strategies may well help define factors for success in this form of epilepsy that is difficult to control.

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Walter J. Hader, Mark Mackay, Hiroshi Otsubo, Shiro Chitoku, Shelly Weiss, Lawrence Becker, O. Carter Snead III and James T. Rutka

Object. The authors conducted a study to determine seizure-related outcomes in a group of pediatric patients with pathologically proven focal cortical dysplasia (FCD) treated by focal cortical resections and multiple subpial transections (MSTs).

Methods. The authors performed a retrospective review of pediatric patients in whom surgery was conducted to treat medically refractory epilepsy secondary to cortical dysplasia between April 1989 and January 2001. Diagnostic studies included preoperative scalp electroencephalography (EEG), magnetic resonance (MR) imaging, positron emission tomography (PET), and magnetoencephalography (MEG). Intraoperative electrocorticography (ECoG) or extraoperative subdural grid EEG monitoring was performed in all patients. Seizure outcome was classified using the Engel scheme. The authors analyzed nine data points and compared these with seizure outcome, including seizure semiology, MR imaging, PET and MEG data, as well as location of resection, intracranial video-EEG findings, MSTs, postresection ECoG data, and histological findings.

The authors analyzed data obtained in 39 children in whom the follow-up interval after epilepsy surgery was at least 18 months. Patients had suffered epilepsy for a mean of 7.7 years prior to surgical intervention and their mean age at treatment was 9.6 years (range 2 months–18 years). A good seizure-related outcome was demonstrated in 28 patients (72%), including 21 (54%) who were free of seizures (Engel Class I) and seven (18%) in whom seizures were rare (Engel Class II). In 11 patients seizure-related outcome was less favorable, including six (15%) with worthwhile improvement involving some seizures (Engel Class III) and five (13%) with no postoperative seizure improvement (Engel Class IV). There was no significant correlation between seizure outcome and data related to seizure characteristics, MR imaging, PET scanning, MEG, location of resection, intracranial video-EEG, postresection ECoG, and histological findings. Eight (50%) of 16 patients who underwent MSTs in addition to incomplete resection of FCD experienced a good outcome (Engel Class I and II). Twenty (87%) of 23 patients in whom resection of FCD was complete and in whom MSTs were not performed experienced a good seizure outcome (p < 0.05).

Conclusions. Complete resection of FCD results in good seizure outcome in a majority of children. When conducted in conjunction with incomplete cortical resection, MSTs do not improve seizure outcome in patients with FCD. Focal cortical dysplasia located outside of eloquent cortex and complete excision of the lesion are the most important predictors of seizure outcome.

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Ying Meng, Mathew R. Voisin, Suganth Suppiah, Zamir Merali, Ali Moghaddamjou, Naif M. Alotaibi, Arbelle Manicat-Emo, Shelly Weiss, Cristina Go, Blathnaid McCoy, Elizabeth J. Donner and James T. Rutka

OBJECTIVE

Intracranial electroencephalography (iEEG) monitoring is an important method of identifying the seizure focus in patients with medically refractory epilepsy. While previous studies have demonstrated low rates of surgical complications, reported rates of surgical site infection (SSI) are highly variable. To date, no studies have specifically evaluated the patient or operative risk factors contributing to SSI. The goals of this study were to examine the rate of SSI after iEEG monitoring for epilepsy workup in pediatric patients and to determine the variables that might contribute to the development of SSI.

METHODS

A retrospective analysis of hospital charts at the Hospital for Sick Children was performed for all patients who had undergone iEEG monitoring between 2000 and 2016. Univariate and multivariate analyses were performed to look for statistically significant variables in relation to SSI.

RESULTS

Among 199 patients eligible for analysis, 8 (4.0%) developed SSIs within a period ranging from 21 to 51 days postoperatively. Univariate analysis yielded 4 factors related to SSI: number of people present in the operating room on electrode insertion (p = 0.02), length of insertion surgery (p = 0.04), previous operation at the same surgical site (p = 0.04), and number of depth electrodes inserted (p = 0.01). Multivariate analysis revealed that both the number of people present during the implant operation (OR 0.08, 95% CI 0.01–0.70) and the number of depth electrodes inserted (OR 3.52, 95% CI 1.44–8.59) independently contributed to SSI.

CONCLUSIONS

This is the largest case series and the first comprehensive review of both patient and operative risk factors in the development of SSI from iEEG monitoring in a pediatric population. The authors’ institution had a lower rate of infection than those in most other studies, which could be explained by their protocol of administering intravenous antibiotics perioperatively and post–implant removal antibiotics for 14 days. The authors found a correlation between SSI and the number of people present during the implant operation, as well as the number of depth electrodes; both may contribute to breaks in sterility.

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Koji Iida, Hiroshi Otsubo, Yuuri Matsumoto, Ayako Ochi, Makoto Oishi, Stephanie Holowka, Elizabeth Pang, Irene Elliott, Shelly K. Weiss, Sylvester H. Chuang, O. Carter Snead III and James T. Rutka

Object

The authors sought to validate magnetoencephalography spike sources (MEGSSs) in neuronavigation during epilepsy surgery in pediatric patients.

Methods

The distributions of MEGSSs in 16 children were defined and classified as clusters (Class I), greater than or equal to 20 MEGSSs with 1 cm or less between MEGSSs; small clusters (Class II), 6 to 19 with 1 cm or less between; and scatters (Class III), less than 6 or greater than 1 cm between spike sources. Using neuronavigation, the MEGSSs were correlated to epileptic zones from intra- and extraoperative electrocorticography (ECoG), surgical procedures, disease entities, and seizure outcomes.

Thirteen patients underwent MEGSSs: nine had clusters; two had small clusters, one with and one without clusters; and three had scatters alone. All 13 had scatters. Clusters localized within and extended from areas of cortical dysplasia and at margins of tumors or cystic lesions. All clusters were colocalized to ECoG-defined epileptic zones. Four of six patients with clusters and/or small clusters underwent complete excisions, and two underwent partial excision with or without multiple subpial transections. In the three patients with scatters alone, ECoG revealed epileptic zones buried within MEGSS areas; these regions of scatters were completely excised and treated with multiple subpial transections. Coexisting scatters were left untreated in nine of 10 patients. Postoperatively, nine of 13 patients were seizure free; the four patients with residual seizures had clusters in unresected eloquent cortex. Three patients in whom no MEGSSs were demonstrated underwent lesionectomies and were seizure free.

Conclusions

Magnetoencephalography spike source clusters indicate an epileptic zone requiring complete excision. Coexisting scatters remote from clusters are nonepileptogenic and do not require excision. Scatters alone, however, should be examined by ECoG; an epileptic zone may exist within these distributions.

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Makoto Oishi, Hiroshi Otsubo, Koji Iida, Yasuhiro Suyama, Ayako Ochi, Shelly K. Weiss, Jing Xiang, William Gaetz, Douglas Cheyne, Sylvester H. Chuang, James T. Rutka and O. Carter Snead III

Object

Magnetoencephalography (MEG) has been used for the preoperative localization of epileptic equivalent current dipoles (ECDs) in neocortical epilepsy. Spatial filtering can be applied to MEG data by means of synthetic aperture magnetometry (SAM), and SAM virtual sensor analysis can be used to estimate the strength and temporal course of the epileptic source in the region of interest. To evaluate the clinical usefulness of this approach, the authors compare the results of SAM virtual sensor analysis to the results of ECD analysis, subdural electroencephalography (EEG) findings, and surgical outcomes in pediatric patients with neocortical epilepsy.

Methods

Ten pediatric patients underwent MEG, invasive subdural EEG, and cortical resection for neocortical epilepsy. The authors compared the morphological characteristics, quantity, location, and distribution of the epileptiform discharges assessed using SAM and ECD analysis, and subdural EEG findings (interictal discharges and ictal onset zones).

In nine patients, MEG revealed clustered ECDs. The region exhibiting the maximum percentage (≥ 70%) of spikes/sharp waves on SAM was colocalized to clustered ECDs in seven patients. In six patients, SAM demonstrated focal spikes; in two, diffuse spikes; and in two others, focal rhythmic sharp waves. These epileptiform discharges were similar to those recorded on subdural EEG. In nine patients, concordant regions containing the maximum percentage of spikes/sharp waves were revealed by SAM and subdural EEG data. The region of the maximum percentage of spikes/sharp waves as demonstrated by SAM was colocalized to the ictal onset zone identified by subdural EEG findings in seven patients and partially colocalized in two.

Conclusions

The SAM virtual sensor analysis revealed morphological characteristics, location, and distribution of epileptiform discharges similar to those shown by subdural EEG recordings. By using SAM it is possible to predict intracerebral interictal epileptiform discharges in the region of interest from noninvasively collected preoperative MEG data. The maximum interictal discharge zone identified by SAM virtual sensors correlated to clustered ECDs and the ictal onset zone on subdural EEG findings. Complementary analyses of ECDs and SAM on three-dimensional MR images can improve delineation of epileptogenic zones and lesions in neocortical epilepsy.

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Mony Benifla, Francesco Sala, John Jane Jr., Hiroshi Otsubo, Ayako Ochi, James Drake, Shelly Weiss, Elizabeth Donner, Ayataka Fujimoto, Stephanie Holowka, Elysa Widjaja, O. Carter Snead III, Mary Lou Smith, Mandeep S. Tamber and James T. Rutka

Object

The authors undertook this study to review their experience with cortical resections in the rolandic region in children with intractable epilepsy.

Methods

The authors retrospectively reviewed the medical records obtained in 22 children with intractable epilepsy arising from the rolandic region. All patients underwent preoperative electroencephalography (EEG), MR imaging, prolonged video-EEG recordings, functional MR imaging, magnetoencephalography, and in some instances PET/SPECT studies. In 21 patients invasive subdural grid and depth electrode monitoring was performed. Resection of the epileptogenic zones in the rolandic region was undertaken in all cases. Seizure outcome was graded according to the Engel classification. Functional outcome was determined using validated outcome scores.

Results

There were 10 girls and 12 boys, whose mean age at seizure onset was 3.2 years. The mean age at surgery was 10 years. Seizure duration prior to surgery was a mean of 7.4 years. Nine patients had preoperative hemiparesis. Neuropsychological testing revealed impairment in some domains in 19 patients in whom evaluation was possible. Magnetic resonance imaging abnormalities were identified in 19 patients. Magnetoencephalography was performed in all patients and showed perirolandic spike clusters on the affected side in 20 patients. The mean duration of invasive monitoring was 4.2 days. The mean number of seizures during the period of invasive monitoring was 17. All patients underwent resection that involved primary motor and/or sensory cortex. The most common pathological entity encountered was cortical dysplasia, in 13 children. Immediately postoperatively, 20 patients had differing degrees of hemiparesis, from mild to severe. The hemiparesis improved in all affected patients by 3–6 months postoperatively. With a mean follow-up of 4.1 years (minimum 2 years), seizure outcome in 14 children (64%) was Engel Class I and seizure outcome in 4 (18%) was Engel Class II. In this series, seizure outcome following perirolandic resection was intimately related to the child's age at the time of surgery. By univariate logistic regression analysis, age at surgery was a statistically significant factor predicting seizure outcome (p < 0.024).

Conclusions

Resection of rolandic cortex for intractable epilepsy is possible with expected morbidity. Accurate mapping of regions of functional cortex and epileptogenic zones may lead to improved seizure outcome in children with intractable rolandic epilepsy. It is important to counsel patients and families preoperatively to prepare them for possible worsened functional outcome involving motor, sensory and/or language pathways.