Sleep and epilepsy: A snapshot of knowledge and future research lines

Nobili, Lino; Frauscher, Birgit; Eriksson, Sofia; Gibbs, Steve A.; Halász, Péter; Lambert, Isabelle; Manni, Raffaele; Peter‐Derex, Laure; Proserpio, Paola; Provini, Federica; Weerd, Al de; Parrino, Liborio

doi:10.1111/jsr.13622

Cited by 38 publications

(31 citation statements)

References 136 publications

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“…Besides the risks accompanied by nightly seizures, the effects of these seizures on sleep quality are substantial. A rising amount of literature exists on the vicious cycle between sleep disturbance and epilepsy 30 . Better control of nightly seizures could improve daytime sleepiness and overall well‐being in children with severe epilepsies.…”

Section: Discussionmentioning

confidence: 99%

Wearable detection of tonic seizures in childhood epilepsy: An exploratory cohort study

Proost,

Macea,

Lagae

et al. 2023

Epilepsia

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ObjectiveTo investigate the performance of a multimodal wearable device for the offline detection of tonic seizures (TS) in a pediatric childhood epilepsy cohort, with a focus on patients with Lennox–Gastaut syndrome.MethodsParallel with prolonged video‐electroencephalography (EEG), the Plug 'n Patch system, a multimodal wearable device using the Sensor Dot and replaceable electrode adhesives, was used to detect TS. Multiple biosignals were recorded: behind‐the‐ear EEG, surface electromyography, electrocardiography, and accelerometer/gyroscope. Biosignals were annotated blindly by a neurologist. Seizure characteristics were described, and performance was assessed by sensitivity, positive predictive value (PPV), F1 score, and false alarm rate (FAR) per hour. Performance was compared to seizure diaries kept by the caretaker.ResultsNinety‐nine TS were detected in 13 patients. Seven patients (54%) had Lennox–Gastaut syndrome and six patients (46%) had other forms of (developmental) epileptic encephalopathies or drug‐resistant epilepsy. All but one patient had intellectual disability. Overall sensitivity was 41%, with a PPV of 9%, an F1 score of 14%, and a median FAR per hour of 0.75. Performance increased to an F1 score of 66% for nightly seizures lasting at least 10 s (sensitivity 66%, PPV 66%) and 71% for nightly seizures lasting at least 20 s (sensitivity 62%, PPV 82%). For these seizures there were no false alarms in 10 of 13 patients. Sensitivity of seizure diaries reached a maximum of 52% for prolonged (≥20 s) nightly seizures, even though caretakers slept in the same room.SignificanceWe showed that it is feasible to use a multimodal wearable device with multiple adhesive sites in children with epilepsy and intellectual disability. For prolonged nightly seizures, offline manual detection of TS outperformed seizure diaries. The recognition of seizure‐specific signatures using multiple modalities can help in the development of automated TS detection algorithms.

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Section: Discussionmentioning

confidence: 99%

Wearable detection of tonic seizures in childhood epilepsy: An exploratory cohort study

Proost,

Macea,

Lagae

et al. 2023

Epilepsia

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“…[4][5][6] Therefore, the bidirectional link between epilepsy and sleep is known, and the mutual modulating effects have been widely described in clinical studies. [7][8][9] Consistently, seizures and sleep disorders have an interdependent relation, where the occurrence of one can exacerbate the other. Sleep deprivation, also restricted to rapid eye movement (REM) sleep, and chronic sleep loss or insufficient sleep have been associated with worsening of seizure frequency and severity, thus possibly causing drug-resistant epilepsy.…”

Section: Introductionmentioning

confidence: 99%

“…Sleep impairment, in particular sleep deprivation, has been associated with the increased risk of seizures in people with epilepsy (PWE) 4–6 . Therefore, the bidirectional link between epilepsy and sleep is known, and the mutual modulating effects have been widely described in clinical studies 7–9 . Consistently, seizures and sleep disorders have an interdependent relation, where the occurrence of one can exacerbate the other.…”

Section: Introductionmentioning

confidence: 99%

Role of the orexin system in the bidirectional relation between sleep and epilepsy: New chances for patients with epilepsy by the antagonism to orexin receptors?

2023

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Epilepsy is a common neurological disorder, affecting patients of all ages, reducing the quality of life, and associated with several comorbidities. Sleep impairment is a frequent condition in patients with epilepsy (PWE), and the relation between sleep and epilepsy has been considered bidirectional, as one can significantly influence the other, and vice versa. The orexin system was described more than 20 years ago and is implicated in several neurobiological functions other than in controlling the sleep–wake cycle. Considering the relation between epilepsy and sleep, and the significant contribution of the orexin system in regulating the sleep–wake cycle, it is conceivable that the orexin system may be affected in PWE. Preclinical studies investigated the impact of the orexin system on epileptogenesis and the effect of orexin antagonism on seizures in animal models. Conversely, clinical studies are few and propose heterogeneous results also considering the different methodological approaches to orexin levels quantification (cerebrospinal‐fluid or blood samples). Because orexin system activity can be modulated by sleep, and considering the sleep impairment documented in PWE, the recently approved dual orexin receptor antagonists (DORAs) have been suggested for treating sleep impairment and insomnia in PWE. Accordingly, sleep improvement can be a therapeutic strategy for reducing seizures and better managing epilepsy. The present review analyzes the preclinical and clinical evidence linking the orexin system to epilepsy, and hypothesizes a model in which the antagonism to the orexin system by DORAs can improve epilepsy by both a direct and a sleep‐mediated (indirect) effect.

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“…As such, there is an urgent need to improve understanding of the pathophysiology of this devastating disease to pave the way for novel diagnostic and therapeutic strategies. One promising avenue toward this goal is studying the effects of sleep, given that is known to be an important modulating factor in epilepsy 5–12 …”

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confidence: 99%

The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy

Hannan,

Thomas,

Jaber

et al. 2023

Annals of Neurology

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ObjectiveSleep has important influences on focal interictal epileptiform discharges (IEDs), and the rates and spatial extent of IEDs are increased in non‐rapid eye movement (NREM) sleep. In contrast, the influence of sleep on seizures is less clear and its effects on seizure topography are poorly documented. We evaluated the influences of NREM sleep on ictal spatiotemporal dynamics and contrasted these with interictal network dynamics.MethodsWe included patients with drug‐resistant focal epilepsy who underwent continuous intracranial EEG with depth electrodes. Patients were selected if they had 1‐3 seizures from each vigilance state, wakefulness and NREM sleep, within a 48‐hour window and under the same anti‐seizure medication. A 10‐min epoch of the interictal iEEG was selected per state, and IEDs were detected automatically. Twenty‐five patients (13 females; 32.5±7.1 years) were included.ResultsThe seizure onset pattern, duration, spatiotemporal propagation and latency of ictal high‐frequency activity did not differ significantly between wakefulness and NREM sleep (all p>0.05). In contrast, IED rates and spatial distribution were increased in NREM compared to wakefulness (p<0.001, Cliff's d=0.48 and 0.49). The spatial overlap between vigilance states was higher for seizures (57.1±40.1%) than IEDs (41.7±46.2%) (p=0.001, Cliff's d=0.51).InterpretationIn contrast to its effects on IEDs, NREM sleep does not affect ictal spatiotemporal dynamics. This suggests that once the brain surpasses the seizure threshold, it will follow the underlying epileptic network irrespective of the vigilance state. These findings offer valuable insights into neural network dynamics in epilepsy and have important clinical implications for localizing seizure foci.This article is protected by copyright. All rights reserved.

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Sleep and epilepsy: A snapshot of knowledge and future research lines

Cited by 38 publications

References 136 publications

Wearable detection of tonic seizures in childhood epilepsy: An exploratory cohort study

Wearable detection of tonic seizures in childhood epilepsy: An exploratory cohort study

Role of the orexin system in the bidirectional relation between sleep and epilepsy: New chances for patients with epilepsy by the antagonism to orexin receptors?

The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy

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