Interictal High Gamma Oscillation Regularity as a Marker for Presurgical Epileptogenic Zone Localization.
Journal
Operative neurosurgery (Hagerstown, Md.)
ISSN: 2332-4260
Titre abrégé: Oper Neurosurg (Hagerstown)
Pays: United States
ID NLM: 101635417
Informations de publication
Date de publication:
01 08 2022
01 08 2022
Historique:
received:
04
11
2021
accepted:
12
02
2022
pubmed:
30
4
2022
medline:
20
7
2022
entrez:
29
4
2022
Statut:
ppublish
Résumé
To ensure that epilepsy surgery is effective, accurate presurgical localization of the epileptogenic zone is essential. Our previous reports demonstrated that interictal high gamma oscillation (30-70 Hz) regularity (GOR) on intracranial electroencephalograms is related to epileptogenicity. To examine whether preoperative GOR analysis with interictal high-density electroencephalography (HD-EEG) improves the accuracy of epileptogenic focus localization and enhances postoperative seizure control. We calculated GOR from 20 seconds of HD-EEG data for 21 patients with refractory focal epilepsy (4 with nonlesional temporal lobe epilepsy) scheduled for epilepsy surgery. Low-resolution brain electromagnetic tomography was used to analyze the high GOR source. To validate our findings, we made comparisons with other conventional localization methods and postoperative seizure outcomes. In all patients, the areas of interictal high GOR were identified and resected. All patients were seizure-free after the operation. The concordance between the results of interictal high GOR on HD-EEG and those of source estimation of interictal discharge was fully overlapping in 10 cases, partially overlapping in 8 cases, and discordant in 3 cases. The concordance between the results of interictal high GOR on HD-EEG and those of interictal 123 I-iomazenil single-photon emission computed tomography was fully overlapping in 8 cases, partially overlapping in 11 cases, and discordant in 2 cases. In 4 patients with nonlesional temporal lobe epilepsy, the interictal high GOR on HD-EEG was useful in confirming the epileptogenic zone. The interictal high GOR on HD-EEG is an excellent marker for presurgical epileptogenic zone localization.
Sections du résumé
BACKGROUND
To ensure that epilepsy surgery is effective, accurate presurgical localization of the epileptogenic zone is essential. Our previous reports demonstrated that interictal high gamma oscillation (30-70 Hz) regularity (GOR) on intracranial electroencephalograms is related to epileptogenicity.
OBJECTIVE
To examine whether preoperative GOR analysis with interictal high-density electroencephalography (HD-EEG) improves the accuracy of epileptogenic focus localization and enhances postoperative seizure control.
METHODS
We calculated GOR from 20 seconds of HD-EEG data for 21 patients with refractory focal epilepsy (4 with nonlesional temporal lobe epilepsy) scheduled for epilepsy surgery. Low-resolution brain electromagnetic tomography was used to analyze the high GOR source. To validate our findings, we made comparisons with other conventional localization methods and postoperative seizure outcomes.
RESULTS
In all patients, the areas of interictal high GOR were identified and resected. All patients were seizure-free after the operation. The concordance between the results of interictal high GOR on HD-EEG and those of source estimation of interictal discharge was fully overlapping in 10 cases, partially overlapping in 8 cases, and discordant in 3 cases. The concordance between the results of interictal high GOR on HD-EEG and those of interictal 123 I-iomazenil single-photon emission computed tomography was fully overlapping in 8 cases, partially overlapping in 11 cases, and discordant in 2 cases. In 4 patients with nonlesional temporal lobe epilepsy, the interictal high GOR on HD-EEG was useful in confirming the epileptogenic zone.
CONCLUSION
The interictal high GOR on HD-EEG is an excellent marker for presurgical epileptogenic zone localization.
Identifiants
pubmed: 35486873
doi: 10.1227/ons.0000000000000245
pii: 01787389-202208000-00008
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
164-173Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © Congress of Neurological Surgeons 2022. All rights reserved.
Références
Lüders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: general principles [published correction appears in Epileptic Disord. 2008;10(2):191]. Epileptic Disord. 2006;8(suppl 2):S1-S9.
Smith SJ. EEG in the diagnosis, classification, and management of patients with epilepsy. J Neurol Neurosurg Psychiatry. 2005;76(suppl 2):ii2-ii7.
Rosenow F, Lüders H. Presurgical evaluation of epilepsy. Brain. 2001;124(pt 9):1683-1700.
Lantz G, Grave de Peralta R, Spinelli L, Seeck M, Michel CM. Epileptic source localization with high density EEG: how many electrodes are needed? Clin Neurophysiol. 2003;114(1):63-69.
Brodbeck V, Lascano AM, Spinelli L, Seeck M, Michel CM. Accuracy of EEG source imaging of epileptic spikes in patients with large brain lesions. Clin Neurophysiol. 2009;120(4):679-685.
Yamazaki M, Tucker DM, Terrill M, Fujimoto A, Yamamoto T. Dense array EEG source estimation in neocortical epilepsy [published correction appears in Front Neurol . 2013;4:132]. Front Neurol. 2013;4:42.
Mégevand P, Spinelli L, Genetti M, et al. Electric source imaging of interictal activity accurately localises the seizure onset zone. J Neurol Neurosurg Psychiatry. 2014;85(1):38-43.
Nemtsas P, Birot G, Pittau F, et al. Source localization of ictal epileptic activity based on high-density scalp EEG data. Epilepsia. 2017;58(6):1027-1036.
Serafini R. Similarities and differences between the interictal epileptiform discharges of green-spikes and red-spikes zones of human neocortex. Clin Neurophysiol. 2019;130(3):396-405.
Bazhenov M, Rulkov NF, Timofeev I. Effect of synaptic connectivity on long-range synchronization of fast cortical oscillations [published correction appears in J Neurophysiol. 2008;100(6):3460]. J Neurophysiol. 2008;100(3):1562-1575.
Avoli M, de Curtis M. GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity. Prog Neurobiol. 2011;95(2):104-132.
Huberfeld G, Menendez de la Prida L, Pallud J, et al. Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy. Nat Neurosci. 2011;14(5):627-634.
Matsumoto A, Brinkmann BH, Matthew Stead S, et al. Pathological and physiological high-frequency oscillations in focal human epilepsy. J Neurophysiol. 2013;110(8):1958-1964.
de Curtis M, Avoli M. Initiation, propagation, and termination of partial (focal) seizures. Cold Spring Harb Perspect Med. 2015;5(7):a022368.
Sato Y, Wong SM, Iimura Y, Ochi A, Doesburg SM, Otsubo H. Spatiotemporal changes in regularity of gamma oscillations contribute to focal ictogenesis. Sci Rep. 2017;7(1):9362.
Sato Y, Ochi A, Mizutani T, Otsubo H. Low entropy of interictal gamma oscillations is a biomarker of the seizure onset zone in focal cortical dysplasia type II. Epilepsy Behav. 2019;96:155-159.
Sato Y, Tsuji Y, Kawauchi Y, et al. Epileptogenic zone localization using intraoperative gamma oscillation regularity analysis in epilepsy surgery for cavernomas: patient series. J Neurosurg Case Lessons. 2021;1(4):CASE20121.
Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R. EEG source imaging. Clin Neurophysiol. 2004;115(10):2195-2222.
Plummer C, Harvey AS, Cook M. EEG source localization in focal epilepsy: where are we now? Epilepsia. 2008;49(2):201-218.
Brodbeck V, Spinelli L, Lascano AM, et al. Electrical source imaging for presurgical focus localization in epilepsy patients with normal MRI. Epilepsia. 2010;51(4):583-591.
Lamusuo S, Ruottinen HM, Knuuti J, et al. Comparison of [ 18 F]FDG-PET, [ 99 mTc]-HMPAO-SPECT, and [ 123 I]-iomazenil-SPECT in localising the epileptogenic cortex. J Neurol Neurosurg Psychiatry. 1997;63(6):743-748.
Fujimoto A, Okanishi T, Kanai S, et al. Double match of 18 F-fluorodeoxyglucose-PET and iomazenil-SPECT improves outcomes of focus resection surgery. Acta Neurochir (Wien). 2018;160(9):1875-1882.
Wieser HG, Blume WT, Fish D, et al. ILAE Commission report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282-286.
Burioka N, Miyata M, Cornélissen G, et al. Approximate entropy in the electroencephalogram during wake and sleep. Clin EEG Neurosci. 2005;36(1):21-24.
Pascual-Marqui RD, Michel CM, Lehmann D. Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol. 1994;18(1):49-65.
Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D. Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. Methods Find Exp Clin Pharmacol. 2002;24(suppl C):91-95.
Grave de Peralta Menendez RG, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL. Electrical neuroimaging based on biophysical constraints. Neuroimage. 2004;21(2):527-539.
Rulkov NF, Timofeev I, Bazhenov M. Oscillations in large-scale cortical networks: map-based model. J Comput Neurosci. 2004;17(2):203-223.
Tanaka T, Ihara M. Post-stroke epilepsy. Neurochem Int. 2017;107:219-228.
Singh R, Pathak DN. Lipid peroxidation and glutathione peroxidase, glutathione reductase, superoxide dismutase, catalase, and glucose-6-phosphate dehydrogenase activities in FeC l3 -induced epileptogenic foci in the rat brain. Epilepsia. 1990;31(1):15-26.
Beaumont A, Whittle IR. The pathogenesis of tumour associated epilepsy. Acta Neurochir (Wien). 2000;142(1):1-15.