Interictal stereo-electroencephalography features below 45 Hz are sufficient for correct localization of the epileptogenic zone and postsurgical outcome prediction
Language English Country United States Media print-electronic
Document type Journal Article
Grant support
22-28784S
Grantová Agentura České Republiky
RVO:68081731
The Czech Academy of Sciences
NU22-08-00278
Ministerstvo Zdravotnictví Ceské Republiky
LM2023053
Ministerstvo Školství, Mládeže a Tělovýchovy
LX22NPO5107
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
39180407
DOI
10.1111/epi.18081
Knihovny.cz E-resources
- Keywords
- EEG, epilepsy, high‐frequency oscillations, interictal epileptoform discharges, machine learning,
- MeSH
- Child MeSH
- Adult MeSH
- Electroencephalography * methods MeSH
- Epilepsy surgery physiopathology diagnosis MeSH
- Middle Aged MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Drug Resistant Epilepsy surgery physiopathology diagnosis MeSH
- Stereotaxic Techniques MeSH
- Treatment Outcome MeSH
- Check Tag
- Child MeSH
- Adult MeSH
- Middle Aged MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
OBJECTIVE: Evidence suggests that the most promising results in interictal localization of the epileptogenic zone (EZ) are achieved by a combination of multiple stereo-electroencephalography (SEEG) biomarkers in machine learning models. These biomarkers usually include SEEG features calculated in standard frequency bands, but also high-frequency (HF) bands. Unfortunately, HF features require extra effort to record, store, and process. Here we investigate the added value of these HF features for EZ localization and postsurgical outcome prediction. METHODS: In 50 patients we analyzed 30 min of SEEG recorded during non-rapid eye movement sleep and tested a logistic regression model with three different sets of features. The first model used broadband features (1-500 Hz); the second model used low-frequency features up to 45 Hz; and the third model used HF features above 65 Hz. The EZ localization by each model was evaluated by various metrics including the area under the precision-recall curve (AUPRC) and the positive predictive value (PPV). The differences between the models were tested by the Wilcoxon signed-rank tests and Cliff's Delta effect size. The differences in outcome predictions based on PPV values were further tested by the McNemar test. RESULTS: The AUPRC score of the random chance classifier was .098. The models (broad-band, low-frequency, high-frequency) achieved median AUPRCs of .608, .582, and .522, respectively, and correctly predicted outcomes in 38, 38, and 33 patients. There were no statistically significant differences in AUPRC or any other metric between the three models. Adding HF features to the model did not have any additional contribution. SIGNIFICANCE: Low-frequency features are sufficient for correct localization of the EZ and outcome prediction with no additional value when considering HF features. This finding allows significant simplification of the feature calculation process and opens the possibility of using these models in SEEG recordings with lower sampling rates, as commonly performed in clinical routines.
Department of Biomedical Engineering Duke Pratt School of Engineering Durham North Carolina USA
Department of Neurology Duke University Medical Center Durham North Carolina USA
Institute of Scientific Instruments of the CAS Brno Czech Republic
International Clinical Research Center St Anne's University Hospital Brno Czech Republic
Lyon Neuroscience Research Center INSERM U1028 CNRS UMR5292 Lyon France
Montreal Neurological Hospital McGill University Montreal Quebec Canada
See more in PubMed
Thijs RD, Surges R, O'Brien TJ, Sander JW. Epilepsy in adults. Lancet. 2019;393:689–701.
Jehi L. The epileptogenic zone: concept and definition. Epilepsy Curr. 2018;18:12–16.
Chen Z, Brodie MJ, Liew D, Kwan P. Treatment outcomes in patients with newly diagnosed epilepsy treated with established and new antiepileptic drugs: a 30‐year longitudinal cohort study. JAMA Neurol. 2018;75:279–286.
Rosenow F, Lüders H. Presurgical evaluation of epilepsy. Brain. 2001;124:1683–1700.
Travnicek V, Klimes P, Cimbalnik J, Halamek J, Jurak P, Brinkmann B, et al. Relative entropy is an easy‐to‐use invasive electroencephalographic biomarker of the epileptogenic zone. Epilepsia. 2023;64:962–972.
Dellavale D, Bonini F, Pizzo F, Makhalova J, Wendling F, Badier JM, et al. Spontaneous fast‐ultradian dynamics of polymorphic interictal events in drug‐resistant focal epilepsy. Epilepsia. 2023;64:2027–2043.
Thomas J, Kahane P, Abdallah C, Avigdor T, Zweiphenning WJEM, Chabardes S, et al. A subpopulation of spikes predicts successful epilepsy surgery outcome. Ann Neurol. 2023;93:522–535.
Krucoff MO, Chan AY, Harward SC, Rahimpour S, Rolston JD, Muh C, et al. Rates and predictors of success and failure in repeat epilepsy surgery: a meta‐analysis and systematic review. Epilepsia. 2017;58:2133–2142.
Bernabei JM, Li A, Revell AY, Smith RJ, Gunnarsdottir KM, Ong IZ, et al. Quantitative approaches to guide epilepsy surgery from intracranial EEG. Brain. 2023;146:2248–2258.
van Mierlo P, Papadopoulou M, Carrette E, Boon P, Vandenberghe S, Vonck K, et al. Functional brain connectivity from EEG in epilepsy: seizure prediction and epileptogenic focus localization. Prog Neurobiol. 2014;121:19–35.
Lagarde S, Roehri N, Lambert I, Trebuchon A, McGonigal A, Carron R, et al. Interictal stereotactic‐EEG functional connectivity in refractory focal epilepsies. Brain. 2018;141:2966–2980.
Ren L, Kucewicz MT, Cimbalnik J, Matsumoto JY, Brinkmann BH, Hu W, et al. Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone. Neurology. 2015;84:602–608.
Shi W, Shaw D, Walsh KG, Han X, Eden UT, Richardson RM, et al. Spike ripples localize the epileptogenic zone best: an international intracranial study. Brain. 2024;147(7):2496–2506. https://doi.org/10.1093/brain/awae037
Frauscher B, Bartolomei F, Kobayashi K, Cimbalnik J, van ‘t Klooster MA, Rampp S, et al. High‐frequency oscillations: the state of clinical research. Epilepsia. 2017;58:1316–1329.
Warren CP, Hu S, Stead M, Brinkmann BH, Bower MR, Worrell GA. Synchrony in normal and focal epileptic brain: the seizure onset zone is functionally disconnected. J Neurophysiol. 2010;104:3530–3539.
Klimes P, Duque JJ, Brinkmann B, van Gompel J, Stead M, St. Louis EK, et al. The functional organization of human epileptic hippocampus. J Neurophysiol. 2016;115:3140–3145.
Shannon C, Weaver W. The Mathematical Theory of Communication.
Gliske SV, Irwin ZT, Chestek C, Stacey WC. Effect of sampling rate and filter settings on high frequency oscillation detections. Clin Neurophysiol. 2016;127:3042–3050.
Bénar CG, Chauvière L, Bartolomei F, Wendling F. Pitfalls of high‐pass filtering for detecting epileptic oscillations: a technical note on ‘false’ ripples. Clin Neurophysiol. 2010;121:301–310.
Cimbalnik J, Klimes P, Sladky V, Nejedly P, Jurak P, Pail M, et al. Multi‐feature localization of epileptic foci from interictal, intracranial EEG. Clin Neurophysiol. 2019;130:1945–1953.
Varatharajah Y, Berry B, Cimbalnik J, Kremen V, van Gompel J, Stead M, et al. Integrating artificial intelligence with real‐time intracranial EEG monitoring to automate interictal identification of seizure onset zones in focal epilepsy. J Neural Eng. 2018;15:046035.
Klimes P, Cimbalnik J, Brazdil M, Hall J, Dubeau F, Gotman J, et al. NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram. Epilepsia. 2019;60:2404–2415.
Chybowski B, Klimes P, Cimbalnik J, Travnicek V, Nejedly P, Pail M, et al. Timing matters for accurate identification of the epileptogenic zone. Clin Neurophysiol. 2024;161:1–9.
Ives JR. New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol. 2005;22:119–123.
Berry RB, Brooks R, Gamaldo C, Harding SM, Lloyd RM, Quan SF, et al. AASM scoring manual updates for 2017 (Version 2.4). J Clin Sleep Med. 2017;13:665–666.
Frauscher B, von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain. 2018;141:1130–1144.
Zelmann R, Frauscher B, Aro RP, Gueziri H‐E, Collins DL. SEEGAtlas: a framework for the identification and classification of depth electrodes using clinical images. J Neural Eng. 2023;20:036021.
Spanedda F, Cendes F, Gotman J. Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in Bitemporal epilepsy. Epilepsia. 1997;38:1300–1314.
Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain. 2008;131:1818–1830.
Cuello Oderiz C, von Ellenrieder N, Dubeau F, Eisenberg A, Gotman J, Hall J, et al. Association of cortical stimulation‐induced seizure with surgical outcome in patients with focal drug‐resistant epilepsy. JAMA Neurol. 2019;76:1070–1078.
Janca R, Jezdik P, Cmejla R, Tomasek M, Worrell GA, Stead M, et al. Detection of Interictal Epileptiform discharges using signal envelope distribution modelling: application to epileptic and non‐epileptic intracranial recordings. Brain Topogr. 2015;28:172–183.
von Ellenrieder N, Frauscher B, Dubeau F, Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high‐frequency oscillations (80‐500 Hz). Epilepsia. 2016;57:869–878.
Nevalainen P, von Ellenrieder N, Klimeš P, Dubeau F, Frauscher B, Gotman J. Association of fast ripples on intracranial EEG and outcomes after epilepsy surgery. Neurology. 2020;95:e2235–e2245.
Cliff N. Dominance statistics: ordinal analyses to answer ordinal questions. Psychol Bull. 1993;114:494–509.
McNemar Q. Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika. 1947;12:153–157.
Miettinen OS. The matched pairs design in the case of all‐or‐none responses. Biometrics. 1968;24:339–352.
Brázdil M, Pail M, Halámek J, Plešinger F, Cimbálník J, Roman R, et al. Very high‐frequency oscillations: novel biomarkers of the epileptogenic zone. Ann Neurol. 2017;82:299–310.
Lundstrom BN, Brinkmann BH, Worrell GA. Low frequency novel interictal EEG biomarker for localizing seizures and predicting outcomes. Brain Commun. 2021;3:fcab231.
Gliske SV, Stacey WC. The BEST conceivable way to talk about epilepsy biomarkers. Epilepsy Curr. 2023;23:175–178.
Klimes P, Peter‐Derex L, Hall J, Dubeau F, Frauscher B. Spatio‐temporal spike dynamics predict surgical outcome in adult focal epilepsy. Clin Neurophysiol. 2022;134:88–99.
Tomlinson SB, Porter BE, Marsh ED. Interictal network synchrony and local heterogeneity predict epilepsy surgery outcome among pediatric patients. Epilepsia. 2017;58:402–411.
Azeem A, von Ellenrieder N, Hall J, Dubeau F, Frauscher B, Gotman J. Interictal spike networks predict surgical outcome in patients with drug‐resistant focal epilepsy. Ann Clin Transl Neurol. 2021;8:1212–1223.
Karoly PJ, Freestone DR, Boston R, Grayden DB, Himes D, Leyde K, et al. Interictal spikes and epileptic seizures: their relationship and underlying rhythmicity. Brain. 2016;139:1066–1078.
Conrad EC, Revell AY, Greenblatt AS, Gallagher RS, Pattnaik AR, Hartmann N, et al. Spike patterns surrounding sleep and seizures localize the seizure‐onset zone in focal epilepsy. Epilepsia. 2023;64:754–768.
Vasickova Z, Klimes P, Cimbalnik J, Travnicek V, Pail M, Halamek J, et al. Shadows of very high‐frequency oscillations can be detected in lower frequency bands of routine stereoelectroencephalography. Sci Rep. 2023;13:1065.
Roehri N, Pizzo F, Lagarde S, Lambert I, Nica A, McGonigal A, et al. High‐frequency oscillations are not better biomarkers of epileptogenic tissues than spikes. Ann Neurol. 2018;83:84–97.
Zweiphenning W, Klooster MAV', van Klink NEC, et al. Intraoperative electrocorticography using high‐frequency oscillations or spikes to tailor epilepsy surgery in The Netherlands (the HFO trial): a randomised, single‐blind, adaptive non‐inferiority trial. Lancet Neurol. 2022;21:982–993.
Brázdil M, Worrell GA, Trávníček V, Pail M, Roman R, Plešinger F, et al. Ultra fast oscillations in the human brain and their functional significance. medRxiv. 2023. https://doi.org/10.1101/2023.02.23.23285962
Jiruska P, Alvarado‐Rojas C, Schevon CA, Staba R, Stacey W, Wendling F, et al. Update on the mechanisms and roles of high‐frequency oscillations in seizures and epileptic disorders. Epilepsia. 2017;58:1330–1339.
Sklenarova B, Zatloukalova E, Cimbalnik J, Klimes P, Dolezalova I, Pail M, et al. Interictal high‐frequency oscillations, spikes, and connectivity profiles: a fingerprint of epileptogenic brain pathologies. Epilepsia. 2023;64:3049–3060.
Přibylová L, Ševčík J, Eclerová V, Klimeš P, Brázdil M, Meijer HGE. Weak coupling of neurons enables very high‐frequency and ultra‐fast oscillations through the interplay of synchronized phase shifts. Netw Neurosci. 2024;8:293–318. https://doi.org/10.1162/netn_a_00351
Di Giacomo R, Uribe‐San‐Martin R, Mai R, et al. Stereo‐EEG ictal/interictal patterns and underlying pathologies. Seizure. 2019;72:54–60.
Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain. 2019;142:2688–2704.