Temporal Lobe Epilepsy with Bitemporal Interictal Epileptiform Discharges: Effects of Sleep and Wakefulness
- Authors: Broutian A.G.1, Glazova M.A.1, Maksimova M.Y.1, Belyakova-Bodina A.I.1
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Affiliations:
- Research Center of Neurology
- Issue: Vol 18, No 3 (2024)
- Pages: 35-41
- Section: Original articles
- URL: https://journals.rcsi.science/2075-5473/article/view/269313
- DOI: https://doi.org/10.17816/ACEN.1150
- ID: 269313
Cite item
Abstract
Introduction. Independent bitemporal interictal discharges are often found in patients with temporal lobe epilepsy. The likelihood of registering epileptiform activity (EA) is higher during sleep. Assessment of bitemporal interictal epileptiform discharges (BIEDs) with various discharge predominance ratio is used for presurgical evaluation of epilepsy patients and prediction of surgical outcomes.
Our objective was to determine the predominant side (PS) in patients with bitemporal epilepsy using the incidence of epileptiform discharges for each sleep stage.
Materials and methods. We analyzed 45 recordings of 10–24 h long-term video-EEG monitoring (LTM) in patients with bitemporal EA. For each recording, the total incidence of EA (IEA) and EA incidence for wakefulness and for each sleep stage were calculated individually. We also assessed the discharge predominance index (DPI) as a ratio of IEA in the predominant and contralateral sides for the entire recording and for each sleep stage.
Results. We observed an IEA increase with sleep deepening, with maximum values observed during N2 and N3 sleep stages. The minimum IEA values were recorded during REM sleep; nevertheless, most of the REM sleep discharges were detected on the PS. DPI values were the highest and the most stable during N2 and N3 stages.
Conclusion. The findings of our study demonstrate an increase in DPI values with non-rapid eye movement (NREM) sleep deepening in patients with bitemporal localization of EA. Despite the protective effects of REM sleep (i.e., reducing the likelihood of EA), it may be pivotal in lateralization of EA in patients with BIEDs. The PS is generally determined by a higher DPI during N2 and N3 stages.
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##article.viewOnOriginalSite##About the authors
Amayak G. Broutian
Research Center of Neurology
Email: ncnmaximova@mail.ru
ORCID iD: 0000-0002-6381-2925
Cand. Sci. (Med.), Head, Laboratory of clinical neurophysiology, Institute of Clinical and Preventive Neurology
Russian Federation, MoscowMariya A. Glazova
Research Center of Neurology
Email: ncnmaximova@mail.ru
ostgraduate student, 2nd Neurological department, Institute of Clinical and Preventive Neurology
Russian Federation, MoscowMarina Yu. Maksimova
Research Center of Neurology
Author for correspondence.
Email: ncnmaximova@mail.ru
ORCID iD: 0000-0002-7682-6672
D. Sci. (Med), Prof., Head, 2nd Neurological department, Institute of Clinical and Preventive Neurology
Russian Federation, MoscowAlexandra I. Belyakova-Bodina
Research Center of Neurology
Email: ncnmaximova@mail.ru
ORCID iD: 0000-0002-2339-8483
junior researcher, Laboratory of clinical neurophysiology, Institute of Clinical and Preventive Neurology
Russian Federation, MoscowReferences
- Hauser W.A., Kurland L.T. The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia. 1975;16(1):1–66. doi: 10.1111/j.1528-1157.1975.tb04721.x
- Wiebe S., Jette N. Pharmacoresistance and the role of surgery in difficult to treat epilepsy. Nat. Rev. Neurol. 2012;8(12):669–677. doi: 10.1038/nrneurol.2012.181
- Ergene E., Shih J.J., Blum D.E., So N.K. Frequency of bitemporal independent interictal epileptiform discharges in temporal lobe epilepsy. Epilepsia. 2000;41(2):213–218. doi: 10.1111/j.1528-1157.2000.tb00142.x
- Gollwitzer S., Scott C.A., Farrell F. et al. The long-term course of temporal lobe epilepsy: From unilateral to bilateral interictal epileptiform discharges in repeated video-EEG monitorings. Epilepsy Behav. 2017;68:17–21. doi: 10.1016/j.yebeh.2016.12.027
- Chung M.Y., Walczak T.S., Lewis D.V. et al. Temporal lobectomy and independent bitemporal interictal activity: what degree of lateralization is sufficient? Epilepsia. 1991;32(2):195–201. doi: 10.1111/j.1528-1157.1991.tb05244.x
- Blume W.T., Borghesi J.L., Lemieux J.F. Interictal indices of temporal seizure origin. Ann. Neurol. 1993;34(5):703–709. doi: 10.1002/ana.410340513
- Malow B.A., Lin X., Kushwaha R., Aldrich M.S. Interictal spiking increases with sleep depth in temporal lobe epilepsy. Epilepsia. 1998;39(12):1309–1316. doi: 10.1111/j.1528-1157.1998.tb01329.x
- Clemens Z., Janszky J., Szucs A. et al. Interictal epileptic spiking during sleep and wakefulness in mesial temporal lobe epilepsy: a comparative study of scalp and foramen ovale electrodes. Epilepsia. 2003;44(2):186–192. doi: 10.1046/j.1528-1157.2003.27302.x
- Брутян А.Г., Белякова-Бодина А.И., Долгова С.М. и др. Интериктальная эпилептиформная активность во сне и в бодрствовании у пациентов с височной эпилепсией. Вестник РГМУ. 2019;(6):22–27. Broutian A.G., Belyakova-Bodina A.I., Dolgova S.M. et al. Interictal epileptiform activity in sleep and wakefulness in patients with temporal lobe epilepsy. Vestnik RGMU. 2019;(6):22–27. doi: 10.24075/vrgmu.2019.073
- Berry R.B., Brooks R., Gamaldo C. et al. AASM Scoring Manual Updates for 2017 (Version 2.4). J. Clin. Sleep. Med. 2017;13(5):665–666. doi: 10.5664/jcsm.6576
- Lieb J.P., Joseph J.P., Engel J. Jr. et al. Sleep state and seizure foci related to depth spike activity in patients with temporal lobe epilepsy. Electroencephalogr. Clin. Neurophysiol. 1980;49(5-6):538–557. doi: 10.1016/0013-4694(80)90396-x
- Sammaritano M., Gigli G.L., Gotman J. Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy. Neurology. 1991;41(2(Pt 1)):290–297. doi: 10.1212/wnl.41.2_part_1.290
- Clemens Z., Janszky J., Clemens B. et al. Factors affecting spiking related to sleep and wake states in temporal lobe epilepsy (TLE). Seizure. 2005;14(1):52–57. doi: 10.1016/j.seizure.2004.09.003
- Singh S., Shukla G., Goyal V. et al. Impact of sleep on the localizing value of video EEG in patients with refractory focal seizures — a prospective video-EEG with EOG and submental EMG study. Clin. Neurophysiol. 2014;125(12):2337–2243. doi: 10.1016/j.clinph.2014.03.021
- Ferrillo F., Beelke M., Nobili L. Sleep EEG synchronization mechanisms and activation of interictal epileptic spikes. Clin. Neurophysiol. 2000;111 Suppl 2:S65–S73. doi: 10.1016/s1388-2457(00)00404-1
- Frauscher B., von Ellenrieder N., Ferrari-Marinho T. et al. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain. 2015;138(Pt 6):1629–1641. doi: 10.1093/brain/awv073
- Garg D., Charlesworth L., Shukla G. Sleep and temporal lobe epilepsy — associations, mechanisms and treatment implications. Front. Hum. Neurosci. 2022;16:849899. doi: 10.3389/fnhum.2022.849899
- Frauscher B., von Ellenrieder N., Dubeau F., Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia. 2016;57(6):879–888. doi: 10.1111/epi.13389
- Ng M., Pavlova M. Why are seizures rare in rapid eye movement sleep? Review of the frequency of seizures in different sleep stages. Epilepsy Res. Treat. 2013;2013:932790. doi: 10.1155/2013/932790
- Yuan X., Sun M. The value of rapid eye movement sleep in the localization of epileptogenic foci for patients with focal epilepsy. Seizure. 2020;81:192–197. doi: 10.1016/j.seizure.2020.06.009
- Копачев Д.Н., Шишкина Л.В., Быченко В.Г. и др. Склероз гиппокампа: патогенез, клиника, диагностика, лечение. Вопросы нейрохирургии имени Н.Н. Бурденко. 2016;80(4):109–116. Kopachev D.N., Shishkina L.V., Bychenko V.G. et al. Hippocampal sclerosis: pathogenesis, clinical features, diagnosis, and treatment. Burdenko's Journal of Neurosurgery. 2016;80(4):109–116. doi: 10.17116/neiro2016804109-116
- Asadi-Pooya A.A., Farazdaghi M., Shahpari M. Clinical significance of bilateral epileptiform discharges in temporal lobe epilepsy. Acta Neurol. Scand. 2021;143(6):608–613. doi: 10.1111/ane.13402
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