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The role of magnetoencephalography in children undergoing hemispherectomy

Clinical article

Cristina V. Torres, Aria Fallah, George M. Ibrahim, Samuel Cheshier, Hiroshi Otsubo, Ayako Ochi, Sylvester Chuang, O. Carter Snead, Stephanie Holowka, and James T. Rutka

Object

Hemispherectomy is an established neurosurgical procedure for medication-resistant epilepsy in children. Despite the effectiveness of this technique, there are patients who do not achieve an optimum outcome after surgery; possible causes of suboptimal results include the presence of bilateral independent epileptogenic foci. Magnetoencephalography (MEG) is an emerging tool that has been found to be useful in the management of lesional and nonlesional epilepsy. The authors analyzed the relative contribution of MEG in patient selection for hemispherectomy.

Methods

The medical records of children undergoing hemispherectomy at the Hospital for Sick Children were reviewed. Those patients who underwent MEG as part of the presurgical evaluation were selected.

Results

Thirteen patients were included in the study. Nine patients were boys. The mean age at the time of surgery was 66 months (range 10–149 months). Seizure etiology was Rasmussen encephalitis in 6 patients, hemimegalencephaly in 2 patients, and cortical dysplasia in 4 patients. In 8 patients, video-EEG and MEG results were consistent to localize the primary epileptogenic hemisphere. In 2 patients, video-EEG lateralized the ictal onset, but MEG showed bilateral spikes. Two patients had bilateral video-EEG and MEG spikes. Engel Class I, II, and IV outcomes were seen in 10, 2, and 1 patients, respectively. In 2 of the patients who had an outcome other than Engel Class I, the MEG clusters were concentrated in the disconnected hemisphere. The third patient had bilateral clusters and potentially independent epileptogenic foci from bilateral cortical dysplasia.

Conclusions

The presence of unilateral MEG spike waves correlated with good outcomes following hemispherectomy. In some cases, MEG provides information that differs from that obtained from video-EEG and conventional MR imaging studies. Further studies with a greater number of patients are needed to assess the role of MEG in the preoperative assessment of candidates for hemispherectomy.

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Utility of depth electrode placement in the neurosurgical management of bottom-of-sulcus lesions: technical note

Eisha A. Christian, Elysa Widjaja, Ayako Ochi, Hiroshi Otsubo, Stephanie Holowka, Elizabeth Donner, Shelly K. Weiss, Cristina Go, James Drake, O. Carter Snead, and James T. Rutka

OBJECTIVE

Small lesions at the depth of the sulcus, such as with bottom-of-sulcus focal cortical dysplasia, are not visible from the surface of the brain and can therefore be technically challenging to resect. In this technical note, the authors describe their method of using depth electrodes as landmarks for the subsequent resection of these exacting lesions.

METHODS

A retrospective review was performed on pediatric patients who had undergone invasive electroencephalography with depth electrodes that were subsequently used as guides for resection in the period between July 2015 and June 2017.

RESULTS

Ten patients (3–15 years old) met the criteria for this study. At the same time as invasive subdural grid and/or strip insertion, between 2 and 4 depth electrodes were placed using a hand-held frameless neuronavigation technique. Of the total 28 depth electrodes inserted, all were found within the targeted locations on postoperative imaging. There was 1 patient in whom an asymptomatic subarachnoid hemorrhage was demonstrated on postprocedural imaging. Depth electrodes aided in target identification in all 10 cases.

CONCLUSIONS

Depth electrodes placed at the time of invasive intracranial electrode implantation can be used to help localize, target, and resect primary zones of epileptogenesis caused by bottom-of-sulcus lesions.

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Preoperative simulation of intracerebral epileptiform discharges: synthetic aperture magnetometry virtual sensor analysis of interictal magnetoencephalography data

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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Neurosurgical management of intractable rolandic epilepsy in children: role of resection in eloquent cortex

Clinical article

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.

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Localization of epileptic foci in children with intractable epilepsy secondary to multiple cortical tubers by using synthetic aperture magnetometry kurtosis

Clinical article

Ichiro Sugiyama, Katsumi Imai, Yu Yamaguchi, Ayako Ochi, Yoko Akizuki, Cristina Go, Tomoyuki Akiyama, O. Carter Snead III, James T. Rutka, James M. Drake, Elysa Widjaja, Sylvester H. Chuang, Doug Cheyne, and Hiroshi Otsubo

Object

Magnetoencephalography (MEG) has been typically used to localize epileptic activity by modeling interictal activity as equivalent current dipoles (ECDs). Synthetic aperture magnetometry (SAM) is a recently developed adaptive spatial filtering algorithm for MEG that provides some advantages over the ECD approach. The SAM-kurtosis algorithm (also known as SAM[g2]) additionally provides automated temporal detection of spike sources by using excess kurtosis value (steepness of epileptic spike on virtual sensors). To evaluate the efficacy of the SAM(g2) method, the authors applied it to readings obtained in children with intractable epilepsy secondary to tuberous sclerosis complex (TSC), and compared them to localizations obtained with ECDs.

Methods

The authors studied 13 children with TSC (7 girls) whose ages ranged from 13 months to 16.3 years (mean 7.3 years). Video electroencephalography, MR imaging, and MEG studies were analyzed. A single ECD model was applied to localize ECD clusters. The SAM(g2) value was calculated at each SAM(g2) virtual voxel in the patient's MR imaging–defined brain volume. The authors defined the epileptic voxels of SAM(g2) (evSAM[g2]) as those with local peak kurtosis values higher than half of the maximum. A clustering of ECDs had to contain ≥ 6 ECDs within 1 cm of each other, and a grouping of evSAM(g2)s had to contain ≥ 3 evSAM(g2)s within 1 cm of each other. The authors then compared both ECD clusters and evSAM(g2) groups with the resection area and correlated these data with seizure outcome.

Results

Seizures started when patients were between 6 weeks and 8 years of age (median 6 months), and became intractable secondary to multiple tubers in all cases. Ictal onset on scalp video electroencephalography was lateralized in 8 patients (62%). The MEG studies showed multiple ECD clusters in 7 patients (54%). The SAM(g2) method showed multiple groups of epileptic voxels in 8 patients (62%). Colocalization of grouped evSAM(g2) with ECD clusters ranged from 20 to 100%, with a mean of 82%. Eight patients underwent resection of single (1 patient) and multiple (7 patients) lobes, with 6 patients achieving freedom from seizures. Of 8 patients who underwent surgery, in 7 the resection area covered ECD clusters and grouped evSAM(g2)s. In the remaining patient the resection area partially included the ECD cluster and grouped evSAM(g2)s. Six of the 7 patients became seizure free.

Conclusions

The combination of SAM(g2) and ECD analyses succeeded in localizing the complex epileptic zones in children with TSC who had intractable epilepsy secondary to multiple cortical tubers. For the subset of children with TSC who present with early-onset and nonlateralized seizures, MEG studies in which SAM(g2) and ECD are used might identify suitable candidates for resection to control seizures.

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Abstracts for the 2013 Annual Meeting of The American Society of Pediatric Neurosurgeons

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Oral Presentations 2015 AANS Annual Scientific Meeting Washington, DC • May 2–6, 2015

Published online August 1, 2015; DOI: 10.3171/2015.8.JNS.AANS2015abstracts