Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy

Yasushi Iimura, Kevin Jones, Kyoko Hattori, Yushi Okazawa, Atsuko Noda, Kana Hoashi, Yutaka Nonoda, Eishi Asano, Tomoyuki Akiyama, Cristina Go, Ayako Ochi, O. Carter Snead, Elizabeth J. Donner, James T. Rutka, James M. Drake, Hiroshi Otsubo

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Objective Subtotal hemispherectomy involves the resection of multiple lobes in children with drug-resistant epilepsy, skipping the motor area (MA). We determined epileptogenicity using the occurrence rate (OR) of high-frequency oscillations (HFOs) and the modulation index (MI), demonstrating strength of coupling between HFO and slow wave. We hypothesized that epileptogenicity increased over the multiple lobes but skipped the MA. Methods We analyzed 23 children (14 subtotal hemispherectomy; 9 multilobar resections). Scalp video-EEG and magnetoencephalography were performed before surgery. We analyzed the OR(HFO) and MI(5 phases=0.5–8 Hz) on electrodes of total area, resection areas, and MA. We compared the data between good [International League Against Epilepsy (ILAE) class I–II] and poor (III–VI) seizure outcome groups. Results ILAE class Ia outcome was achieved in 18 children. Among the MI(5 phases) in the resection areas, MI(3–4 Hz) was the highest. The OR(HFO) and MI(3–4 Hz) in both total area and resection areas were significantly higher in the good seizure outcome group than in the poor outcome group. The OR(HFO) and MI(3–4 Hz) in resection areas were significantly higher than in the MA. Conclusions Our patients with multilobar drug-resistant epilepsy showed evidence of multifocal epileptogenicity that specifically skipped the MA. Significance This is the first study demonstrating that the electrophysiological phenotype of multifocal epilepsy specifically skips the MA using OR(HFO) and MI(3–4 Hz).

Original languageEnglish
Pages (from-to)1197-1205
Number of pages9
JournalClinical Neurophysiology
Volume128
Issue number7
DOIs
Publication statusPublished - Jul 1 2017

Fingerprint

Motor Cortex
Hemispherectomy
Epilepsy
Seizures
Magnetoencephalography
Scalp
Drug Resistant Epilepsy
Electroencephalography
Electrodes
Phenotype

Keywords

  • Epileptic spasms
  • Modulation index (MI)
  • Motor area
  • Pathological high-frequency oscillations
  • Phase-amplitude coupling
  • Subtotal hemispherectomy

ASJC Scopus subject areas

  • Sensory Systems
  • Neurology
  • Clinical Neurology
  • Physiology (medical)

Cite this

Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy. / Iimura, Yasushi; Jones, Kevin; Hattori, Kyoko; Okazawa, Yushi; Noda, Atsuko; Hoashi, Kana; Nonoda, Yutaka; Asano, Eishi; Akiyama, Tomoyuki; Go, Cristina; Ochi, Ayako; Snead, O. Carter; Donner, Elizabeth J.; Rutka, James T.; Drake, James M.; Otsubo, Hiroshi.

In: Clinical Neurophysiology, Vol. 128, No. 7, 01.07.2017, p. 1197-1205.

Research output: Contribution to journalArticle

Iimura, Y, Jones, K, Hattori, K, Okazawa, Y, Noda, A, Hoashi, K, Nonoda, Y, Asano, E, Akiyama, T, Go, C, Ochi, A, Snead, OC, Donner, EJ, Rutka, JT, Drake, JM & Otsubo, H 2017, 'Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy', Clinical Neurophysiology, vol. 128, no. 7, pp. 1197-1205. https://doi.org/10.1016/j.clinph.2017.03.031
Iimura, Yasushi ; Jones, Kevin ; Hattori, Kyoko ; Okazawa, Yushi ; Noda, Atsuko ; Hoashi, Kana ; Nonoda, Yutaka ; Asano, Eishi ; Akiyama, Tomoyuki ; Go, Cristina ; Ochi, Ayako ; Snead, O. Carter ; Donner, Elizabeth J. ; Rutka, James T. ; Drake, James M. ; Otsubo, Hiroshi. / Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy. In: Clinical Neurophysiology. 2017 ; Vol. 128, No. 7. pp. 1197-1205.
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abstract = "Objective Subtotal hemispherectomy involves the resection of multiple lobes in children with drug-resistant epilepsy, skipping the motor area (MA). We determined epileptogenicity using the occurrence rate (OR) of high-frequency oscillations (HFOs) and the modulation index (MI), demonstrating strength of coupling between HFO and slow wave. We hypothesized that epileptogenicity increased over the multiple lobes but skipped the MA. Methods We analyzed 23 children (14 subtotal hemispherectomy; 9 multilobar resections). Scalp video-EEG and magnetoencephalography were performed before surgery. We analyzed the OR(HFO) and MI(5 phases=0.5–8 Hz) on electrodes of total area, resection areas, and MA. We compared the data between good [International League Against Epilepsy (ILAE) class I–II] and poor (III–VI) seizure outcome groups. Results ILAE class Ia outcome was achieved in 18 children. Among the MI(5 phases) in the resection areas, MI(3–4 Hz) was the highest. The OR(HFO) and MI(3–4 Hz) in both total area and resection areas were significantly higher in the good seizure outcome group than in the poor outcome group. The OR(HFO) and MI(3–4 Hz) in resection areas were significantly higher than in the MA. Conclusions Our patients with multilobar drug-resistant epilepsy showed evidence of multifocal epileptogenicity that specifically skipped the MA. Significance This is the first study demonstrating that the electrophysiological phenotype of multifocal epilepsy specifically skips the MA using OR(HFO) and MI(3–4 Hz).",
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author = "Yasushi Iimura and Kevin Jones and Kyoko Hattori and Yushi Okazawa and Atsuko Noda and Kana Hoashi and Yutaka Nonoda and Eishi Asano and Tomoyuki Akiyama and Cristina Go and Ayako Ochi and Snead, {O. Carter} and Donner, {Elizabeth J.} and Rutka, {James T.} and Drake, {James M.} and Hiroshi Otsubo",
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T1 - Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy

AU - Iimura, Yasushi

AU - Jones, Kevin

AU - Hattori, Kyoko

AU - Okazawa, Yushi

AU - Noda, Atsuko

AU - Hoashi, Kana

AU - Nonoda, Yutaka

AU - Asano, Eishi

AU - Akiyama, Tomoyuki

AU - Go, Cristina

AU - Ochi, Ayako

AU - Snead, O. Carter

AU - Donner, Elizabeth J.

AU - Rutka, James T.

AU - Drake, James M.

AU - Otsubo, Hiroshi

PY - 2017/7/1

Y1 - 2017/7/1

N2 - Objective Subtotal hemispherectomy involves the resection of multiple lobes in children with drug-resistant epilepsy, skipping the motor area (MA). We determined epileptogenicity using the occurrence rate (OR) of high-frequency oscillations (HFOs) and the modulation index (MI), demonstrating strength of coupling between HFO and slow wave. We hypothesized that epileptogenicity increased over the multiple lobes but skipped the MA. Methods We analyzed 23 children (14 subtotal hemispherectomy; 9 multilobar resections). Scalp video-EEG and magnetoencephalography were performed before surgery. We analyzed the OR(HFO) and MI(5 phases=0.5–8 Hz) on electrodes of total area, resection areas, and MA. We compared the data between good [International League Against Epilepsy (ILAE) class I–II] and poor (III–VI) seizure outcome groups. Results ILAE class Ia outcome was achieved in 18 children. Among the MI(5 phases) in the resection areas, MI(3–4 Hz) was the highest. The OR(HFO) and MI(3–4 Hz) in both total area and resection areas were significantly higher in the good seizure outcome group than in the poor outcome group. The OR(HFO) and MI(3–4 Hz) in resection areas were significantly higher than in the MA. Conclusions Our patients with multilobar drug-resistant epilepsy showed evidence of multifocal epileptogenicity that specifically skipped the MA. Significance This is the first study demonstrating that the electrophysiological phenotype of multifocal epilepsy specifically skips the MA using OR(HFO) and MI(3–4 Hz).

AB - Objective Subtotal hemispherectomy involves the resection of multiple lobes in children with drug-resistant epilepsy, skipping the motor area (MA). We determined epileptogenicity using the occurrence rate (OR) of high-frequency oscillations (HFOs) and the modulation index (MI), demonstrating strength of coupling between HFO and slow wave. We hypothesized that epileptogenicity increased over the multiple lobes but skipped the MA. Methods We analyzed 23 children (14 subtotal hemispherectomy; 9 multilobar resections). Scalp video-EEG and magnetoencephalography were performed before surgery. We analyzed the OR(HFO) and MI(5 phases=0.5–8 Hz) on electrodes of total area, resection areas, and MA. We compared the data between good [International League Against Epilepsy (ILAE) class I–II] and poor (III–VI) seizure outcome groups. Results ILAE class Ia outcome was achieved in 18 children. Among the MI(5 phases) in the resection areas, MI(3–4 Hz) was the highest. The OR(HFO) and MI(3–4 Hz) in both total area and resection areas were significantly higher in the good seizure outcome group than in the poor outcome group. The OR(HFO) and MI(3–4 Hz) in resection areas were significantly higher than in the MA. Conclusions Our patients with multilobar drug-resistant epilepsy showed evidence of multifocal epileptogenicity that specifically skipped the MA. Significance This is the first study demonstrating that the electrophysiological phenotype of multifocal epilepsy specifically skips the MA using OR(HFO) and MI(3–4 Hz).

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KW - Modulation index (MI)

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KW - Pathological high-frequency oscillations

KW - Phase-amplitude coupling

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