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Surgical strategy for focal cortical dysplasia based on the analysis of the spike onset and peak zones on magnetoencephalography

Hiroshi Shirozu, Akira Hashizume, Hiroshi Masuda, Akiyoshi Kakita, Hiroshi Otsubo, and Shigeki Kameyama

OBJECTIVE

The aim of this study was to elucidate the surgical strategy for focal cortical dysplasia (FCD) based on the interictal analysis on magnetoencephalography (MEG). For this purpose, the correlation between the spike onset zone (Sp-OZ) and the spike peak zone (Sp-PZ) on MEG was evaluated to clarify the differences in the Sp-OZ and its correlation with Sp-PZ in FCD subtypes to develop an appropriate surgical strategy.

METHODS

Forty-one FCD patients (n = 17 type I, n = 13 type IIa, and n = 11 type IIb) were included. The Sp-OZ was identified by the summation of gradient magnetic-field topography (GMFT) magnitudes at interictal MEG spike onset, and Sp-PZ was defined as the distribution of the equivalent current dipole (ECD) at spike peak. Correlations between Sp-OZ and Sp-PZ distributions were evaluated and compared with clinical factors and seizure outcomes retrospectively.

RESULTS

Good seizure outcomes (Engel class I) were obtained significantly more often in patients with FCD type IIb (10/11, 90.9%) than those with type IIa (4/13, 30.8%; p = 0.003) and type I (6/17, 35.3%; p = 0.004). The Sp-OZ was significantly smaller (1 or 2 gyri) in type IIb (10, 90.9%) than in type IIa (4, 30.8%; p = 0.003) or type I (9, 53.0%; p = 0.036). Concordant correlations between the Sp-OZ and Sp-PZ were significantly more frequent in type IIb (7, 63.6%) than in type IIa (1, 7.7%; p = 0.015) or type I (1, 5.8%; p = 0.004). Complete resection of the Sp-OZ achieved significantly better seizure outcomes (Engel class I: 9/10, 90%) than incomplete resection (11/31, 35.5%) (p = 0.003). In contrast, complete resection of the Sp-PZ showed no significant difference in good seizure outcomes (9/13, 69.2%) compared with incomplete resection (11/28, 39.3%).

CONCLUSIONS

The Sp-OZ detected by MEG using GMFT and its correlation with Sp-PZ were related to FCD subtypes. A discordant distribution between Sp-OZ and Sp-PZ in type I and IIa FCD indicated an extensive epileptogenic zone and a complex epileptic network. Type IIb showed a restricted epileptogenic zone with the smaller Sp-OZ and concordance between Sp-OZ and Sp-PZ. Complete resection of the Sp-OZ provided significantly better seizure outcomes than incomplete resection. Complete resection of the Sp-PZ was not related to seizure outcomes. There was a definite difference in the epileptogenic zone among FCD subtypes; hence, an individual surgical strategy taking into account the correlation between the Sp-OZ and Sp-PZ should be considered.

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The role of magnetoencephalography in epilepsy surgery

Zulma S. Tovar-Spinoza, Ayako Ochi, James T. Rutka, Cristina Go, and Hiroshi Otsubo

Epilepsy surgery requires the precise localization of the epileptogenic zone and the anatomical localization of eloquent cortex so that these areas can be preserved during cortical resection. Magnetoencephalography (MEG) is a technique that maps interictal magnetic dipole sources onto MR imaging to produce a magnetic source image. Magneto-encephalographic spike sources can be used to localize the epileptogenic zone and be part of the workup of the patient for epilepsy surgery in conjunction with data derived from an analysis of seizure semiology, scalp video electroencephalography, PET, functional MR imaging, and neuropsychological testing. In addition, magnetoencephalographic spike sources can be linked to neuronavigation platforms for use in the neurosurgical field. Finally, paradigms have been developed so that MEG can be used to identify functional areas of the cerebral cortex including the somatosensory, motor, language, and visual evoked fields.

The authors review the basic principles of MEG and the utility of MEG for presurgical planning as well as intra-operative mapping and discuss future applications of MEG technology.

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Surgical outcomes in children with bottom-of-sulcus dysplasia and drug-resistant epilepsy: a retrospective cohort study

Puneet Jain, Ayako Ochi, Carter McInnis, Hiroshi Otsubo, O. Carter Snead III, George M. Ibrahim, Elizabeth Donner, and Elysa Widjaja

OBJECTIVE

Bottom-of-sulcus dysplasia (BOSD) is challenging to identify radiologically. The aim of this study was to explore seizure outcomes after resective surgery or MR-guided laser interstitial thermal therapy (MRgLITT) in children with BOSD.

METHODS

Children with radiologically defined BOSD who underwent resective surgery or MRgLITT, with at least 1 year of follow-up were included. Clinical, radiological, neurophysiological, and histological data were extracted from medical records. Invasive video EEG (IVEEG) was used to evaluate the ictal onset zone or motor/language mapping, wherever appropriate. Histology of MRI-visible BOSD, including the overlying and adjacent cortex, was also evaluated.

RESULTS

Forty-one children with BOSD underwent surgical treatment. The lesion was initially overlooked on MRI in 20 patients (48.8%). Of 34 patients who underwent IVEEG and who had available ictal data, the ictal onset zone extended beyond the MRI-visible BOSD in 23 patients (67.6%). Surgical treatment included lesionectomy (24 patients), extended lesionectomy (12 patients), lobectomy (1 patient), and ablation of BOSD (4 patients). The pathology in 37 patients who underwent resection showed focal cortical dysplasia type IIB and type IIA in 21 (53.8%) and 16 patients (41%), respectively. Seizure freedom was achieved in 32 patients (78.1%) after a mean follow-up of 4.3 years.

CONCLUSIONS

Seizure outcomes after resective surgery or MRgLITT in children with BOSD were generally favorable. The authors found that the neurophysiological abnormality and pathology often extended beyond the MRI-visible BOSD.

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Detection of epileptogenic focus using advanced dynamic statistical parametric mapping with magnetoencephalography in a patient with MRI-negative focal cortical dysplasia type IIB

Won Seok Chang, Midori Nakajima, Ayako Ochi, Elysa Widjaja, James T. Rutka, Ivanna Yau, Shiro Baba, and Hiroshi Otsubo

Advanced dynamic statistical parametric mapping (AdSPM) with magnetoencephalography (MEG) was used to identify MRI-negative epileptogenic lesions in this report. A 15-year-old girl had MRI-negative and pharmacology-resistant focal-onset epilepsy. She experienced two types of seizures. Type I consisted of her arousal from sleep, staring, and a forced head-turning movement to the left, followed by secondary generalization. Type II began with an aura of dizziness followed by staring and postictal headache with fatigue. Scalp video-electroencephalography (EEG) captured two type I seizures originating from the right frontocentral region. MEG showed scattered dipoles over the right frontal region. AdSPM identified the spike source at the bottom of the right inferior frontal sulcus. Intracranial video-EEG captured one type I seizure, which originated from the depth electrode at the bottom of the sulcus and correlated with the AdSPM spike source. Accordingly, the patient underwent resection of the middle and inferior frontal gyri, including the AdSPM-identified spike source. Histopathological examination revealed that the patient had focal cortical dysplasia type IIB. To date, the patient has been seizure free for 2 years while receiving topiramate treatment. This is the first preliminary report to identify MRI-negative epilepsy using AdSPM. Further investigation of AdSPM would be valuable for cases of MRI-negative focal epilepsy.

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Phase-amplitude coupling of interictal fast activities modulated by slow waves on scalp EEG and its correlation with seizure outcomes of disconnection surgery in children with intractable nonlesional epileptic spasms

Takehiro Uda, Ichiro Kuki, Takeshi Inoue, Noritsugu Kunihiro, Hiroharu Suzuki, Hiroshi Uda, Toshiyuki Kawashima, Kosuke Nakajo, Yoko Nakanishi, Shinsuke Maruyama, Takashi Shibata, Hiroshi Ogawa, Shin Okazaki, Hisashi Kawawaki, Kenji Ohata, Takeo Goto, and Hiroshi Otsubo

OBJECTIVE

Epileptic spasms (ESs) are classified as focal, generalized, or unknown onset ESs. The classification of ESs and surgery in patients without lesions apparent on MRI is challenging. Total corpus callosotomy (TCC) is a surgical option for diagnosis of the lateralization and possible treatment for ESs. This study investigated phase-amplitude coupling (PAC) of fast activity modulated by slow waves on scalp electroencephalography (EEG) to evaluate the strength of the modulation index (MI) before and after disconnection surgery in children with intractable nonlesional ESs. The authors hypothesize that a decreased MI due to surgery correlates with good seizure outcomes.

METHODS

The authors studied 10 children with ESs without lesions on MRI who underwent disconnection surgeries. Scalp EEG was obtained before and after surgery. The authors collected 20 epochs of 3 minutes each during non–rapid eye movement sleep. The MI of the gamma (30–70 Hz) amplitude and delta (0.5–4 Hz) phase was obtained in each electrode. MIs for each electrode were averaged in 4 brain areas (left/right, anterior/posterior quadrants) and evaluated to determine the correlation with seizure outcomes.

RESULTS

The median age at first surgery was 2.3 years (range 10 months–9.1 years). Two patients with focal onset ESs underwent anterior quadrant disconnection (AQD). TCC alone was performed in 5 patients with generalized or unknown onset ESs. Two patients achieved seizure freedom. Three patients had residual generalized onset ESs. Disconnection surgeries in addition to TCC consisted of TCC + posterior quadrant disconnection (PQD) (1 patient); TCC + AQD + PQD (1 patient); and TCC + AQD + hemispherotomy (1 patient). Seven patients became seizure free with a mean follow-up period of 28 months (range 5–54 months). After TCC, MIs in 4 quadrants were significantly lower in the 2 seizure-free patients than in the 6 patients with residual ESs (p < 0.001). After all 15 disconnection surgeries in 10 patients, MIs in the 13 target quadrants for each disconnection surgery that resulted in freedom from seizures were significantly lower than in the 26 target quadrants in patients with residual ESs (p < 0.001).

CONCLUSIONS

In children with nonlesional ESs, PAC for scalp EEG before and after disconnection surgery may be a surrogate marker for control of ESs. The MI may indicate epileptogenic neuronal modulation of the interhemispheric corpus callosum and intrahemispheric subcortical network for ESs. TCC may be a therapeutic option to disconnect the interhemispheric modulation of epileptic networks.

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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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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