NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram

KLIMES, Petr, Jan CIMBÁLNÍK, Milan BRÁZDIL, Jeffery HALL, Francois DUBEAU, Jean GOTMAN and Brigit FRAUSCHER. NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram. Epilepsia. Blackwell Science, 2019, vol. 60, No 12, p. 2404-2415. ISSN 0013-9580. Available from: https://dx.doi.org/10.1111/epi.16377.

Basic information

• Original name: NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram
• Authors: KLIMES, Petr (203 Czech Republic), Jan CIMBÁLNÍK (203 Czech Republic), Milan BRÁZDIL (203 Czech Republic, belonging to the institution), Jeffery HALL (124 Canada), Francois DUBEAU (124 Canada), Jean GOTMAN (124 Canada) and Brigit FRAUSCHER (124 Canada, guarantor).
• Edition: Epilepsia, Blackwell Science, 2019, 0013-9580.

Other information

• Original language: English
• Type of outcome: Article in a journal
• Field of Study: 30210 Clinical neurology
• Country of publisher: United States of America
• Confidentiality degree: is not subject to a state or trade secret
• WWW: URL
• Impact factor: Impact factor: 6.040
• RIV identification code: RIV/00216224:14110/19:00113177
• Organization unit: Faculty of Medicine
• Doi: http://dx.doi.org/10.1111/epi.16377
• UT WoS: 000545973100008
• Keywords in English: connectivity; drug-resistant epilepsy; high-frequency oscillations; machine learning; sleep-wake cycle
• Tags: 14110127, podil, rivok
• Tags: International impact

Abstract

OBJECTIVE: Interictal epileptiform anomalies such as epileptiform discharges or high-frequency oscillations show marked variations across the sleep-wake cycle. This study investigates which state of vigilance is the best to localize the epileptogenic zone (EZ) in interictal intracranial electroencephalography (EEG). METHODS: Thirty patients with drug-resistant epilepsy undergoing stereo-EEG (SEEG)/sleep recording and subsequent open surgery were included; 13 patients (43.3%) had good surgical outcome (Engel class I). Sleep was scored following standard criteria. Multiple features based on the interictal EEG (interictal epileptiform discharges, high-frequency oscillations, univariate and bivariate features) were used to train a support vector machine (SVM) model to classify SEEG contacts placed in the EZ. The performance of the algorithm was evaluated by the mean area under the receiver-operating characteristic (ROC) curves (AUCs) and positive predictive values (PPVs) across 10-minute sections of wake, non-rapid eye movement sleep (NREM) stages N2 and N3, REM sleep, and their combination. RESULTS: Highest AUCs were achieved in NREM sleep stages N2 and N3 compared to wakefulness and REM (P < .01). There was no improvement when using a combination of all four states (P > .05); the best performing features in the combined state were selected from NREM sleep. There were differences between good (Engel I) and poor (Engel II-IV) outcomes in PPV (P < .05) and AUC (P < .01) across all states. The SVM multifeature approach outperformed spikes and high-frequency oscillations (P < .01) and resulted in results similar to those of the seizure-onset zone (SOZ; P > .05). SIGNIFICANCE: Sleep improves the localization of the EZ with best identification obtained in NREM sleep stages N2 and N3. Results based on the multifeature classification in 10 minutes of NREM sleep were not different from the results achieved by the SOZ based on 12.7 days of seizure monitoring. This finding might ultimately result in a more time-efficient intracranial presurgical investigation of focal epilepsy.