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Pathology of temporal lobectomy for refractory seizures in children

Review of 20 cases including some unique malformative lesions

Venita Jay, Laurence E. Becker, Hiroshi Otsubo, Paul A. Hwang, Harold J. Hoffman and Derek Harwood-Nash

✓ Significant pathological abnormalities were encountered in a series of 20 temporal lobectomies in children with intractable complex partial seizures. In particular, “dual pathology” (mesial temporal sclerosis with other lesions) was found rather than mesial temporal sclerosis as the only lesion. Unusual pathological findings included capillary penetration of neurons in a neuronal heterotopia in one patient, and foci of extensive cortical disorganization in some cases of mixed tumors and gangliogliomas. A high proportion of neuronal migration disorders was also seen with overlapping pathological features between cortical dysplasia and tuberous sclerosis. In this correlative clinical, radiological, electroencephalographic, and pathological study, some of the pathological lesions in children did not fit the classical categories of neoplasia and malformation and transitional forms were rarely encountered.

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Venita Jay, Laurence E. Becker, Hiroshi Otsubo, Paul Hwang, Harold J. Hoffman and Derek C. Armstrong

✓ Unusual pathological findings were encountered in a temporal lobectomy specimen from a 9-year-old boy with intractable complex partial seizures. Magnetic resonance imaging revealed an enlarged left temporal lobe, with diffuse high signal intensity over the cortex and poor gray-white differentiation on T2-weighted imaging; single-photon emission computerized tomography showed decreased blood flow. Active epileptiform discharges were identified in the left temporal lobe with focal slow waves and generalized epileptiform paroxysms. Pathologically, the cortex revealed changes of focal cortical dysplasia with extensive disorganization of neuronal morphology, layering, and orientation as well as focal polymicrogyria. The cortical-white matter junction was indistinct with extensive neuronal heterotopias in the white matter. Large pale balloon cells akin to those seen in tuberous sclerosis were found scattered within the cortex and white matter. The most striking finding was that of a heterotopic nodule in the white matter, which revealed abnormal neurons with penetration of cell bodies by capillaries. Ultrastructurally, there were no degenerative changes in these neurons, and this unusual phenomenon is attributed to a developmental disturbance affecting neuronal, glial, and vascular elements.

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Hiroshi Otsubo, Atsushi Shirasawa, Shiro Chitoku, James T. Rutka, Scott B. Wilson and O. Carter Snead III

✓ The purpose of this paper is to describe the use of computerized brain-surface voltage topographic mapping to localize and identify epileptic discharges recorded on electrocorticographic (ECoG) studies in which a subdural grid was used during intracranial video electroencephalographic (IVEEG) monitoring. The authors studied 12 children who underwent surgery for intractable extrahippocampal epilepsy. Cortical surfaces and subdural grid electrodes were photographed during the initial surgery to create an electrode map that could be superimposed onto a picture of the brain surface. Spikes were selected from ictal discharges recorded at the beginning of clinically confirmed seizures and from interictal discharges seen on ECoG studies during IVEEG recording. A computer program was used to calculate the sequential amplitude of the spikes by using squared interpolation, and they were then superimposed onto the electrode map. Interictal discharges and high-amplitude spike complexes at seizure onset were plotted on the map. This mapping procedure depicted the ictal zone in nine patients and the interictal zone in 12, and proved to be an accurate and useful source of information for planning corrective surgery.

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Chusak Limotai, Cristina Y. Go, Shiro Baba, Kazuo Okanari, Ayako Ochi, James T. Rutka, O. Carter Snead III and Hiroshi Otsubo

Infants with Sturge-Weber syndrome (SWS) are considered for surgery if they develop seizures and the seizures prove medically refractory. The authors report on 2 infants (15 and 19 months old) with SWS who underwent scalp video electroencephalography (EEG) and subsequent functional hemispherotomy for intractable partial motor seizures due to extensive left hemispheric angiomatosis. They presented with similar interictal and ictal EEG findings. Ictal EEG showed abrupt high-amplitude delta slow waves, without evolution on the contralateral hemisphere before the build-up of ictal EEG changes on the lesional hemisphere. The patients became seizure free after hemispherotomy. The ictal contralateral slow waves were not a sign of an ictal hemisphere and may indicate prominent ischemic changes resulting from a steal phenomenon of hemispheric angiomatosis during seizure.

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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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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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Harold J. Hoffman, Hiroshi Otsubo, E. Bruce Hendrick, Robin P. Humphreys, James M. Drake, Laurence E. Becker, Mark Greenberg and Derek Jenkin

✓ All patients with confirmed intracranial germ-cell tumors treated at the Hospital of Sick Children during the period January, 1952, to December, 1989, were reviewed. Of the 51 tumors reviewed, 16 were located in the suprasellar region, 32 in the pineal region, and three in both the pineal and the suprasellar regions. Forty-nine patients underwent surgical resection which was total in seven and partial in 20, and consisted of a biopsy in 22. Two patients were managed on the basis of serum and cerebrospinal fluid markers. Surgical tools such as the operating microscope, the ultrasonic surgical aspirator, and the laser beam allowed safe debulking and removal of the deep-seated tumors in the pineal region. There were no operative deaths in the 36 patients treated since 1972, who included 23 with pineal tumors. Twenty-five patients with germinomas received radiotherapy and had a 5-year survival rate of 85.1%. Thirteen patients with non-germinoma germ-cell tumors received radiotherapy and had a 5-year survival rate of 45.5%. On the basis of this review, the authors recommend resection of pineal and suprasellar germ-cell tumors in order to firmly establish an accurate histological diagnosis to guide the extent of adjuvant therapy. In the case of a pure germinoma without evidence of dissemination, adjuvant therapy consists only of local radiotherapy. On the other hand, for malignant non-germinoma germ-cell tumors, adjuvant therapy must include chemotherapy as well as craniospinal axis radiotherapy.

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Gregory W. Albert, George M. Ibrahim, Hiroshi Otsubo, Ayako Ochi, Cristina Y. Go, O. Carter Snead III, James M. Drake and James T. Rutka

Object

Resective surgery is increasingly used in the management of pediatric epilepsy. Frequently, invasive monitoring with subdural electrodes is required to adequately map the epileptogenic focus. The risks of invasive monitoring include the need for 2 operations, infection, and CSF leak. The aim of this study was to evaluate the feasibility and outcomes of resective epilepsy surgery guided by magnetoencephalography (MEG) in children who would have otherwise been candidates for electrode implantation.

Methods

The authors reviewed the records of patients undergoing resective epilepsy surgery at the Hospital for Sick Children between 2001 and 2010. They identified cases in which resections were based on MEG data and no intracranial recordings were performed. Each patient's chart was reviewed for presentation, MRI findings, MEG findings, surgical procedure, pathology, and surgical outcome.

Results

Sixteen patients qualified for the study. All patients had localized spike clusters on MEG and most had abnormal findings on MRI. Resection was carried out in each case based on the MEG data linked to neuronavigation and supplemented with intraoperative neuromonitoring. Overall, 62.5% of patients were seizure free following surgery, and 20% of patients experienced an improvement in seizures without attaining seizure freedom. In 2 cases, additional surgery was performed subsequently with intracranial monitoring in attempts to obtain seizure control.

Conclusions

MEG is a viable alternative to invasive monitoring with intracranial electrodes for planning of resective surgery in carefully selected pediatric patients with localization-related epilepsy. Good candidates for this approach include patients who have a well-delineated, localized spike cluster on MEG that is concordant with findings of other preoperative evaluations and patients with prior brain pathologies that make the implantation of subdural and depth electrodes somewhat problematic.

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Odeya Bennett-Back, Ayako Ochi, Elysa Widjaja, Shohei Nambu, Akio Kamiya, Cristina Go, Sylvester Chuang, James T. Rutka, James Drake, O. Carter Snead III and Hiroshi Otsubo

Object

Porencephalic cyst/encephalomalacia (PC/E) is a brain lesion caused by ischemic insult or hemorrhage. The authors evaluated magnetoencephalography (MEG) spike sources (MEGSS) to localize the epileptogenic zone in children with intractable epilepsy secondary to PC/E.

Methods

The authors retrospectively studied 13 children with intractable epilepsy secondary to PC/E (5 girls and 8 boys, age range 1.8–15 years), who underwent prolonged scalp video-electroencephalography (EEG), MRI, and MEG. Interictal MEGSS locations were compared with the ictal and interictal zones as determined from scalp video-EEG.

Results

Magnetic resonance imaging showed PC/E in extratemporal lobes in 3 patients, within the temporal lobe in 2 patients, and in both temporal and extratemporal lobes in 8 patients. Magnetoencephalographic spike sources were asymmetrically clustered at the margin of PC/E in all 13 patients. One cluster of MEGSS was observed in 11 patients, 2 clusters in 1 patient, and 3 clusters in 1 patient. Ictal EEG discharges were lateralized and concordant with MEGSS in 8 patients (62%). Interictal EEG discharges were lateralized and concordant with MEGSS hemisphere in 9 patients (69%). Seven patients underwent lesionectomy in addition to MEGSS clusterectomy with (2 patients) and without (5 patients) intracranial video-EEG. Temporal lobectomy was performed in 1 patient and hemispherectomy in another. Eight of 9 patients achieved seizure freedom following surgery.

Conclusions

Magnetoencephalography delineated the extent of the epileptogenic zone adjacent to PC/E in patients with intractable epilepsy. Complete resection of the MEGSS cluster along with PC/E can provide favorable seizure outcomes.

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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.