Clinical Utility of Sleep Recordings During Presurgical Epilepsy Evaluation With Stereo-Electroencephalography: A Systematic Review.
Journal
Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society
ISSN: 1537-1603
Titre abrégé: J Clin Neurophysiol
Pays: United States
ID NLM: 8506708
Informations de publication
Date de publication:
01 Jul 2024
01 Jul 2024
Historique:
medline:
27
6
2024
pubmed:
27
6
2024
entrez:
27
6
2024
Statut:
ppublish
Résumé
Although the role of sleep in modulating epileptic activity is well established, many epileptologists overlook the significance of considering sleep during presurgical epilepsy evaluations in cases of drug-resistant epilepsy. Here, we conducted a comprehensive literature review from January 2000 to May 2023 using the PubMed electronic database and compiled evidence to highlight the need to revise the current clinical approach. All articles were assessed for eligibility by two independent reviewers. Our aim was to shed light on the clinical value of incorporating sleep monitoring into presurgical evaluations with stereo-electroencephalography. We present the latest developments on the important bidirectional interactions between sleep and various forms of epileptic activity observed in stereo-electroencephalography recordings. Specifically, epileptic activity is modulated by different sleep stages, peaking in non-rapid eye movement sleep, while being suppressed in rapid eye movement sleep. However, this modulation can vary across different brain regions, underlining the need to account for sleep to accurately pinpoint the epileptogenic zone during presurgical assessments. Finally, we offer practical solutions, such as automated sleep scoring algorithms using stereo-electroencephalography data alone, to seamlessly integrate sleep monitoring into routine clinical practice. It is hoped that this review will provide clinicians with a readily accessible roadmap to the latest evidence concerning the clinical utility of sleep monitoring in the context of stereo-electroencephalography and aid the development of therapeutic and diagnostic strategies to improve patient surgical outcomes.
Identifiants
pubmed: 38935657
doi: 10.1097/WNP.0000000000001057
pii: 00004691-202407000-00008
doi:
Types de publication
Journal Article
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
430-443Subventions
Organisme : Fonds de Recherche du Québec - Santé
ID : 2021-2023
Informations de copyright
Copyright © 2024 by the American Clinical Neurophysiology Society.
Déclaration de conflit d'intérêts
The authors have no funding or conflicts of interest to disclose.
Références
Grigg-Damberger M, Foldvary-Schaefer N. Bidirectional relationships of sleep and epilepsy in adults with epilepsy. Epilepsy Behav 2021;116:107735.
Dinkelacker V, El Helou J, Frauscher B. Interictal sleep recordings during presurgical evaluation: bidirectional perspectives on sleep related network functioning. Rev Neurol (Paris) 2022;178:703–713.
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.
Steriade M. Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 2005;28:317–324.
Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia 2016;57:879–888.
Shouse MN, Siegel JM, Wu MF, Szymusiak R, Morrison AR. Mechanisms of seizure suppression during rapid-eye-movement (REM) sleep in cats. Brain Res 1989;505:271–282.
Shouse MN, Farber PR, Staba RJ. Physiological basis: how NREM sleep components can promote and REM sleep components can suppress seizure discharge propagation. Clin Neurophysiol 2000;111(suppl 2):S9–S18.
Ramantani G, Maillard L, Koessler L. Correlation of invasive EEG and scalp EEG. Seizure 2016;41:196–200.
Nobili L, Frauscher B, Eriksson S, et al. Sleep and epilepsy: a snapshot of knowledge and future research lines. J Sleep Res 2022; 31:e13622.
Berry R, Quan S, Abreu A, et al. The AASM manual for the scoring of sleep and associated events, Version 2.6. Darien, IL: American Academy of Sleep Medicine; 2020.
Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. Scalp spindles are associated with widespread intracranial activity with unexpectedly low synchrony. Neuroimage 2015;105:1–12.
Campana C, Zubler F, Gibbs S, et al. Suppression of interictal spikes during phasic rapid eye movement sleep: a quantitative stereo-electroencephalography study. J Sleep Res 2017;26:606–613.
Markun LC, Sampat A. Clinician-focused overview and developments in polysomnography. Curr Sleep Med Rep 2020;6:309–321.
Loddo G, Baldassarri L, Zenesini C, et al. Seizures with paroxysmal arousals in sleep-related hypermotor epilepsy (SHE): dissecting epilepsy from NREM parasomnias. Epilepsia 2020;61:2194–2202.
McLeod GA, Ghassemi A, Ng MC. Can REM sleep localize the epileptogenic zone? A systematic review and analysis. Front Neurol 2020;11:584.
Klimes P, Cimbalnik J, Brazdil M, et al. NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram. Epilepsia 2019;60:2404–2415.
Lambert I, Roehri N, Giusiano B, et al. Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness. Epilepsia 2018;59:235–243.
Nguyen-Michel VH, Herlin B, Gales A, et al. Sleep scoring based on video-electroencephalography monitoring in an Epileptology Unit: comparison with polysomnography. J Sleep Res 2021;30:e13332.
Dasheiff RM, Kofke WA. Primarily generalized seizures are more effective than partial seizures in arousing patients from sleep. Neurol Res 2003;25:63–67.
Peter-Derex L, Klimes P, Latreille V, Bouhadoun S, Dubeau F, Frauscher B. Sleep disruption in epilepsy: ictal and interictal epileptic activity Matter. Ann Neurol 2020;88:907–920.
Dell KL, Payne DE, Kremen V, et al. Seizure likelihood varies with day-to-day variations in sleep duration in patients with refractory focal epilepsy: a longitudinal electroencephalography investigation. EClinicalMedicine 2021;37:100934.
Juan E, Gorska U, Kozma C, et al. Distinct signatures of loss of consciousness in focal impaired awareness versus tonic-clonic seizures. Brain 2023;146:109–123.
Malow A, Bowes RJ, Ross D. Relationship of temporal lobe seizures to sleep and arousal: a combined scalp-intracranial electrode study. Sleep 2000;23:231–234.
Kremen V, Duque JJ, Brinkmann BH, et al. Behavioral state classification in epileptic brain using intracranial electrophysiology. J Neural Eng 2017;14:026001.
Zubler F, Rubino A, Lo Russo G, Schindler K, Nobili L. Correlating interictal spikes with migma and delta dynamics during non-rapid-eye-movement-sleep. Front Neurol 2017;8:288.
Conrad EC, Revell AY, Greenblatt AS, et al. Spike patterns surrounding sleep and seizures localize the seizure-onset zone in focal epilepsy. Epilepsia 2023;64:754–768.
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.
Fouad A, Azizollahi H, Le Douget JE, et al. Interictal epileptiform discharges show distinct spatiotemporal and morphological patterns across wake and sleep. Brain Commun 2022;4:fcac183.
Conrad EC, Tomlinson SB, Wong JN, et al. Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset. Brain 2020;143:554–569.
Bower MR, Kucewicz MT, St Louis EK, et al. Reactivation of seizure-related changes to interictal spike shape and synchrony during postseizure sleep in patients. Epilepsia 2017;58:94–104.
Bagshaw AP, Jacobs J, LeVan P, Dubeau F, Gotman J. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia 2009;50:617–628.
Dumpelmann M, Jacobs J, Schulze-Bonhage A. Temporal and spatial characteristics of high frequency oscillations as a new biomarker in epilepsy. Epilepsia 2015;56:197–206.
Sakuraba R, Iwasaki M, Okumura E, et al. High frequency oscillations are less frequent but more specific to epileptogenicity during rapid eye movement sleep. Clin Neurophysiol 2016;127:179–186.
von Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. Neuroimage Clin 2017;14:566–573.
Klimes P, Duque JJ, Brinkmann B, et al. The functional organization of human epileptic hippocampus. J Neurophysiol 2016;115:3140–3145.
Chen C, Wang Y, Ye L, et al. A region-specific modulation of sleep slow waves on interictal epilepsy markers in focal epilepsy. Epilepsia 2023;64:973–985.
Song I, Orosz I, Chervoneva I, et al. Bimodal coupling of ripples and slower oscillations during sleep in patients with focal epilepsy. Epilepsia 2017;58:1972–1984.
Frauscher B, von Ellenrieder N, Ferrari-Marinho T, Avoli M, Dubeau F, Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain 2015;138:1629–1641.
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.
Menezes Cordeiro I, von Ellenrieder N, Zazubovits N, Dubeau F, Gotman J, Frauscher B. Sleep influences the intracerebral EEG pattern of focal cortical dysplasia. Epilepsy Res 2015;113:132–139.
Minthe A, Janzarik WG, Lachner-Piza D, et al. Stable high frequency background EEG activity distinguishes epileptic from healthy brain regions. Brain Commun 2020;2:fcaa107.
Weiss SA, Staba RJ, Sharan A, et al. Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions. Sci Rep 2021;11:21388.
Thomas J, Kahane P, Abdallah C, et al. A subpopulation of spikes predicts successful epilepsy surgery outcome. Ann Neurol 2023;93:522–535.
Sinha SR, Sullivan L, Sabau D, et al. American clinical Neurophysiology society guideline 1: pinimum technical sequirements for performing clinical electroencephalography. J Clin Neurophysiol 2016;33:303–307.
Brigham D, Shah Y, Singh K, Pavkovic I, Karkare S, Kothare SV. Comparison of artifacts between paste and collodion method of electrode application in pediatric EEG. Clin Neurophysiol Pract 2020;5:12–15.
Young GB, Ives JR, Chapman MG, Mirsattari SM. A comparison of subdermal wire electrodes with collodion-applied disk electrodes in long-term EEG recordings in ICU. Clin Neurophysiol 2006;117:1376–1379.
Ives JR. New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 2005;22:119–123.
von Ellenrieder N, Peter-Derex L, Gotman J, Frauscher B. SleepSEEG: automatic sleep scoring using intracranial EEG recordings only. J Neural Eng 2022;19:026057.
Kremen V, Brinkmann BH, Van Gompel JJ, Stead M, St Louis EK, Worrell GA. Automated unsupervised behavioral state classification using intracranial electrophysiology. J Neural Eng 2019;16:026004.
Reed CM, Birch KG, Kamiński J, et al. Automatic detection of periods of slow wave sleep based on intracranial depth electrode recordings. J Neurosci Methods 2017;282:1–8.