Magnetoencephalography spike sources interrelate the extensive epileptogenic zone of tuberous sclerosis complex

Tohru Okanishi, Tomoyuki Akiyama, Ellen Mayo, Yasunori Honda, Chihiro Ueda-Kawada, Midori Nakajima, Yoichiro Homma, Ayako Ochi, Cristina Go, Elysa Widjaja, Sylvester H. Chuang, James T. Rutka, James Drake, O. Carter Snead, Hiroshi Otsubo

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Abstract

Objective We hypothesized that the extensive epileptic network in patients with tuberous sclerosis complex (TSC) manifests as clustered and scattered distributions of magnetoencephalography spike sources (MEGSS). Methods We retrospectively analyzed pre-surgical MEG in 15 patients with TSC. We performed single moving dipole analysis to localize and classify clustered and scattered MEGSS. We compared the number of electrodes within the resected area (RA) and the proportions of clustered and scattered MEGSS within RA with the seizure outcome. Results The number of electrodes within RA ranged from 29 to 83 (mean = 51). The MEGSS were distributed over multiple lobes (3–8; mean = 5.9) and bilaterally in 14 patients. Clusters of MEGSS ranged from 1 to 4 (mean = 1.4). The number of MEGSS ranged in total from 28 to 139 (mean = 70); in the clusters, 10–128 (mean = 49); and in the scatters, 0–45 (mean = 21). Four patients achieved an Engel class I surgical outcome, four, a class II outcome; five, a class III outcome; and two, a class IV outcome. The proportion of MEGSS ranged in total from 0 to 92% (mean = 57%) within RA; 0–100% (mean = 67%) in the resection hemisphere; 0–100% (mean = 63%) in the clusters; and 0–81% (mean = 28%) in the scatters. Univariate ordinal logistic regression analyses showed that the proportion of scattered MEGSS within RA (p = 0.049) significantly correlated with seizure outcomes. Multivariate analyses using three covariates (number of electrodes, proportions of clustered and scattered MEGSS within RA) showed that only the proportion of scattered MEGSS within RA significantly correlated with seizure outcomes (p = 0.016). Significance MEG data showed a wide distribution of multilobar MEGSS in patients with TSC. The seizure outcome was not related to the clustered MEGSS within RA, since the grids were essentially planned to cover and resect the clustered MEGSS surrounding tubers. The maximal possible resection of scattered MEGSS correlated with improved seizure outcome in TSC. Some parts of the epileptogenic zone disrupted by multiple tubers did not have a sufficiently large area to produce clustered MEGSS. Although the wide distribution of scattered MEGSS is not interpreted as epileptogenic, they might be interrelated with clustered MEGSS to project a complex epilepsy network and be part of the extensive epileptogenic zones found in TSC.

Original languageEnglish
Pages (from-to)302-310
Number of pages9
JournalEpilepsy Research
Volume127
DOIs
Publication statusPublished - Nov 1 2016

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Magnetoencephalography
Tuberous Sclerosis
Seizures
Electrodes

Keywords

  • Epilepsy surgery
  • Epileptic network
  • Intractable epilepsy
  • Magnetoencephalography
  • Seizure outcome
  • Tuberous sclerosis complex

ASJC Scopus subject areas

  • Neurology
  • Clinical Neurology

Cite this

Magnetoencephalography spike sources interrelate the extensive epileptogenic zone of tuberous sclerosis complex. / Okanishi, Tohru; Akiyama, Tomoyuki; Mayo, Ellen; Honda, Yasunori; Ueda-Kawada, Chihiro; Nakajima, Midori; Homma, Yoichiro; Ochi, Ayako; Go, Cristina; Widjaja, Elysa; Chuang, Sylvester H.; Rutka, James T.; Drake, James; Snead, O. Carter; Otsubo, Hiroshi.

In: Epilepsy Research, Vol. 127, 01.11.2016, p. 302-310.

Research output: Contribution to journalArticle

Okanishi, T, Akiyama, T, Mayo, E, Honda, Y, Ueda-Kawada, C, Nakajima, M, Homma, Y, Ochi, A, Go, C, Widjaja, E, Chuang, SH, Rutka, JT, Drake, J, Snead, OC & Otsubo, H 2016, 'Magnetoencephalography spike sources interrelate the extensive epileptogenic zone of tuberous sclerosis complex', Epilepsy Research, vol. 127, pp. 302-310. https://doi.org/10.1016/j.eplepsyres.2016.09.007
Okanishi, Tohru ; Akiyama, Tomoyuki ; Mayo, Ellen ; Honda, Yasunori ; Ueda-Kawada, Chihiro ; Nakajima, Midori ; Homma, Yoichiro ; Ochi, Ayako ; Go, Cristina ; Widjaja, Elysa ; Chuang, Sylvester H. ; Rutka, James T. ; Drake, James ; Snead, O. Carter ; Otsubo, Hiroshi. / Magnetoencephalography spike sources interrelate the extensive epileptogenic zone of tuberous sclerosis complex. In: Epilepsy Research. 2016 ; Vol. 127. pp. 302-310.
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abstract = "Objective We hypothesized that the extensive epileptic network in patients with tuberous sclerosis complex (TSC) manifests as clustered and scattered distributions of magnetoencephalography spike sources (MEGSS). Methods We retrospectively analyzed pre-surgical MEG in 15 patients with TSC. We performed single moving dipole analysis to localize and classify clustered and scattered MEGSS. We compared the number of electrodes within the resected area (RA) and the proportions of clustered and scattered MEGSS within RA with the seizure outcome. Results The number of electrodes within RA ranged from 29 to 83 (mean = 51). The MEGSS were distributed over multiple lobes (3–8; mean = 5.9) and bilaterally in 14 patients. Clusters of MEGSS ranged from 1 to 4 (mean = 1.4). The number of MEGSS ranged in total from 28 to 139 (mean = 70); in the clusters, 10–128 (mean = 49); and in the scatters, 0–45 (mean = 21). Four patients achieved an Engel class I surgical outcome, four, a class II outcome; five, a class III outcome; and two, a class IV outcome. The proportion of MEGSS ranged in total from 0 to 92{\%} (mean = 57{\%}) within RA; 0–100{\%} (mean = 67{\%}) in the resection hemisphere; 0–100{\%} (mean = 63{\%}) in the clusters; and 0–81{\%} (mean = 28{\%}) in the scatters. Univariate ordinal logistic regression analyses showed that the proportion of scattered MEGSS within RA (p = 0.049) significantly correlated with seizure outcomes. Multivariate analyses using three covariates (number of electrodes, proportions of clustered and scattered MEGSS within RA) showed that only the proportion of scattered MEGSS within RA significantly correlated with seizure outcomes (p = 0.016). Significance MEG data showed a wide distribution of multilobar MEGSS in patients with TSC. The seizure outcome was not related to the clustered MEGSS within RA, since the grids were essentially planned to cover and resect the clustered MEGSS surrounding tubers. The maximal possible resection of scattered MEGSS correlated with improved seizure outcome in TSC. Some parts of the epileptogenic zone disrupted by multiple tubers did not have a sufficiently large area to produce clustered MEGSS. Although the wide distribution of scattered MEGSS is not interpreted as epileptogenic, they might be interrelated with clustered MEGSS to project a complex epilepsy network and be part of the extensive epileptogenic zones found in TSC.",
keywords = "Epilepsy surgery, Epileptic network, Intractable epilepsy, Magnetoencephalography, Seizure outcome, Tuberous sclerosis complex",
author = "Tohru Okanishi and Tomoyuki Akiyama and Ellen Mayo and Yasunori Honda and Chihiro Ueda-Kawada and Midori Nakajima and Yoichiro Homma and Ayako Ochi and Cristina Go and Elysa Widjaja and Chuang, {Sylvester H.} and Rutka, {James T.} and James Drake and Snead, {O. Carter} and Hiroshi Otsubo",
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T1 - Magnetoencephalography spike sources interrelate the extensive epileptogenic zone of tuberous sclerosis complex

AU - Okanishi, Tohru

AU - Akiyama, Tomoyuki

AU - Mayo, Ellen

AU - Honda, Yasunori

AU - Ueda-Kawada, Chihiro

AU - Nakajima, Midori

AU - Homma, Yoichiro

AU - Ochi, Ayako

AU - Go, Cristina

AU - Widjaja, Elysa

AU - Chuang, Sylvester H.

AU - Rutka, James T.

AU - Drake, James

AU - Snead, O. Carter

AU - Otsubo, Hiroshi

PY - 2016/11/1

Y1 - 2016/11/1

N2 - Objective We hypothesized that the extensive epileptic network in patients with tuberous sclerosis complex (TSC) manifests as clustered and scattered distributions of magnetoencephalography spike sources (MEGSS). Methods We retrospectively analyzed pre-surgical MEG in 15 patients with TSC. We performed single moving dipole analysis to localize and classify clustered and scattered MEGSS. We compared the number of electrodes within the resected area (RA) and the proportions of clustered and scattered MEGSS within RA with the seizure outcome. Results The number of electrodes within RA ranged from 29 to 83 (mean = 51). The MEGSS were distributed over multiple lobes (3–8; mean = 5.9) and bilaterally in 14 patients. Clusters of MEGSS ranged from 1 to 4 (mean = 1.4). The number of MEGSS ranged in total from 28 to 139 (mean = 70); in the clusters, 10–128 (mean = 49); and in the scatters, 0–45 (mean = 21). Four patients achieved an Engel class I surgical outcome, four, a class II outcome; five, a class III outcome; and two, a class IV outcome. The proportion of MEGSS ranged in total from 0 to 92% (mean = 57%) within RA; 0–100% (mean = 67%) in the resection hemisphere; 0–100% (mean = 63%) in the clusters; and 0–81% (mean = 28%) in the scatters. Univariate ordinal logistic regression analyses showed that the proportion of scattered MEGSS within RA (p = 0.049) significantly correlated with seizure outcomes. Multivariate analyses using three covariates (number of electrodes, proportions of clustered and scattered MEGSS within RA) showed that only the proportion of scattered MEGSS within RA significantly correlated with seizure outcomes (p = 0.016). Significance MEG data showed a wide distribution of multilobar MEGSS in patients with TSC. The seizure outcome was not related to the clustered MEGSS within RA, since the grids were essentially planned to cover and resect the clustered MEGSS surrounding tubers. The maximal possible resection of scattered MEGSS correlated with improved seizure outcome in TSC. Some parts of the epileptogenic zone disrupted by multiple tubers did not have a sufficiently large area to produce clustered MEGSS. Although the wide distribution of scattered MEGSS is not interpreted as epileptogenic, they might be interrelated with clustered MEGSS to project a complex epilepsy network and be part of the extensive epileptogenic zones found in TSC.

AB - Objective We hypothesized that the extensive epileptic network in patients with tuberous sclerosis complex (TSC) manifests as clustered and scattered distributions of magnetoencephalography spike sources (MEGSS). Methods We retrospectively analyzed pre-surgical MEG in 15 patients with TSC. We performed single moving dipole analysis to localize and classify clustered and scattered MEGSS. We compared the number of electrodes within the resected area (RA) and the proportions of clustered and scattered MEGSS within RA with the seizure outcome. Results The number of electrodes within RA ranged from 29 to 83 (mean = 51). The MEGSS were distributed over multiple lobes (3–8; mean = 5.9) and bilaterally in 14 patients. Clusters of MEGSS ranged from 1 to 4 (mean = 1.4). The number of MEGSS ranged in total from 28 to 139 (mean = 70); in the clusters, 10–128 (mean = 49); and in the scatters, 0–45 (mean = 21). Four patients achieved an Engel class I surgical outcome, four, a class II outcome; five, a class III outcome; and two, a class IV outcome. The proportion of MEGSS ranged in total from 0 to 92% (mean = 57%) within RA; 0–100% (mean = 67%) in the resection hemisphere; 0–100% (mean = 63%) in the clusters; and 0–81% (mean = 28%) in the scatters. Univariate ordinal logistic regression analyses showed that the proportion of scattered MEGSS within RA (p = 0.049) significantly correlated with seizure outcomes. Multivariate analyses using three covariates (number of electrodes, proportions of clustered and scattered MEGSS within RA) showed that only the proportion of scattered MEGSS within RA significantly correlated with seizure outcomes (p = 0.016). Significance MEG data showed a wide distribution of multilobar MEGSS in patients with TSC. The seizure outcome was not related to the clustered MEGSS within RA, since the grids were essentially planned to cover and resect the clustered MEGSS surrounding tubers. The maximal possible resection of scattered MEGSS correlated with improved seizure outcome in TSC. Some parts of the epileptogenic zone disrupted by multiple tubers did not have a sufficiently large area to produce clustered MEGSS. Although the wide distribution of scattered MEGSS is not interpreted as epileptogenic, they might be interrelated with clustered MEGSS to project a complex epilepsy network and be part of the extensive epileptogenic zones found in TSC.

KW - Epilepsy surgery

KW - Epileptic network

KW - Intractable epilepsy

KW - Magnetoencephalography

KW - Seizure outcome

KW - Tuberous sclerosis complex

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