Generalized quasiperiodic epileptiform activity in sleep is associated with cognitive impairment in children with drug-resistant focal lesional epilepsy
Language English Country United States Media print-electronic
Document type Journal Article, Observational Study, Research Support, Non-U.S. Gov't
Grant support
NV19-04-00369
Czech Health Research Council AZV ČR - International
PubMed
31612465
DOI
10.1111/epi.16362
Knihovny.cz E-resources
- Keywords
- ESES, cognition, epilepsy surgery, epileptic encephalopathy, non-REM sleep,
- MeSH
- Wakefulness physiology MeSH
- Child MeSH
- Electroencephalography trends MeSH
- Epilepsies, Partial diagnosis physiopathology psychology MeSH
- Cognitive Dysfunction diagnosis physiopathology psychology MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Child, Preschool MeSH
- Drug Resistant Epilepsy diagnosis physiopathology psychology MeSH
- Retrospective Studies MeSH
- Sleep physiology MeSH
- Case-Control Studies MeSH
- Check Tag
- Child MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Male MeSH
- Child, Preschool MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Observational Study MeSH
- Research Support, Non-U.S. Gov't MeSH
OBJECTIVE: To evaluate the impact of generalized quasiperiodic epileptiform discharges ("hurdles") observed in non-rapid eye movement (NREM) sleep on cognitive function in children with intractable focal epilepsy. "Hurdles" pattern does not meet the criteria of the electrical status epilepticus in slow-wave sleep (ESES). METHODS: In a retrospective analysis, 24 patients with "hurdles" and their 24 peers matched for demographic and epilepsy-related variables were compared in terms of neuropsychological domains and electroencephalography (EEG)-derived quantifiers. Both "hurdles" and controls were children between 2 and 19 years of age who had intractable focal epilepsy evaluated as candidates of resective epilepsy surgery. RESULTS: Full-scale intelligence quotient/developmental quotient (FSIQ/DQ) (P = .002) and visuoconstructional skills (P = .004) were significantly lower in children with "hurdles" compared to controls. Patients with "hurdles" presented with higher interictal spike indexes in sleep (P < .001, median difference -0.9, 95% confidence interval [CI] -1.4, -0.6) and wakefulness (P < .001, median difference -0.3, 95% CI -0.5, -1). Relative time of sleep spindles in NREM sleep was significantly reduced (P < .001, median difference 0.1, 95% CI 0.0, 0.1) in the "hurdles" group. The time proportion of sleep spindles represented a significant positive (P = .008) and spike index of generalized spikes in sleep a significant negative explanatory variable (P = .004) of FSIQ/DQ scores. The proportion of seizure-free patients 2 years after epilepsy surgery did not differ significantly between the two groups (P = .19). SIGNIFICANCE: Although the "hurdles" pattern does not fulfill the criteria of ESES, it is associated with a pronounced cognitive dysfunction. Disturbed sleep structure marked by reduced sleep spindles and generalized spiking in sleep is associated with worse cognitive performance. Despite having a generalized nature, we did not find a lower probability of postsurgical seizure freedom in patients with "hurdles" pattern.
2nd Faculty of Medicine Charles University Prague Prague Czech Republic
Department of Clinical Psychology Motol University Hospital Prague Czech Republic
Department of Paediatric Neurology Motol University Hospital Prague Czech Republic
Department of Paediatric Neurology Ostrava Faculty Hospital Ostrava Czech Republic
See more in PubMed
Berg AT, Langfitt JT, Testa FM, Levy SR, DiMario F, Westerveld M, et al. Global cognitive function in children with epilepsy: a community-based study. Epilepsia. 2008;49:608-14.
Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, van Emde BW, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia. 2010;51:676-85.
Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512-21.
Binnie CD, Kasteleijn-Nolst Trenite DG, Smit AM, Wilkins AJ. Interactions of epileptiform EEG discharges and cognition. Epilepsy Res. 1987;1(4):239-45.
Tassinari CA, Rubboli G. Cognition and paroxysmal EEG activities: from a single spike to electrical status epilepticus during sleep. Epilepsia. 2006;47(Suppl 2):40-3.
Peigneux P, Smith C. Memory processing in relation to sleep. In: Kryger M, Roth T, Dement WC, ed. Principles and Practice of Sleep Medicine. Amsterdam, the Netherlands: Elsevier; 2010. p. 335-47.
Rasch B, Born J. About sleep's role in memory. Physiol Rev. 2013;93:681-766.
Chan S, Pressler R, Boyd SG, Baldeweg T, Cross JH. Does sleep benefit memory consolidation in children with focal epilepsy? Epilepsia. 2017;58:456-66.
Garside P, Arizpe J, Lau CI, Goh C, Walsh V. Cross-hemispheric alternating current stimulation during a nap disrupts slow wave activity and associated memory consolidation. Brain Stimul 2015;8(3):520-7.
Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430:78-81.
Cox R, Hofman WF, Talamini LM. Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem. 2012;19:264-7.
Fogel SM, Nader R, Cote KA, Smith CT. Sleep spindles and learning potential. Behav Neurosci. 2007;121:1-10.
Gruber G, Anderer P, Parapatics S, Saletu B, Schabus M, Klimesch W, et al. Involvement of sleep spindles in overnight declarative memory stabilization. Somnologie - Schlafforschung und Schlafmedizin. 2015;19:30-7.
Van Bogaert P, Aeby A, De Borchgrave V, De Cocq C, Deprez M, De Tiege X, et al. The epileptic syndromes with continuous spikes and waves during slow sleep: definition and management guidelines. Acta neurologica Belg. 2006;106:52-60.
Peltola ME, Liukkonen E, Granstrom ML, Paetau R, Kantola-Sorsa E, Valanne L, et al. The effect of surgery in encephalopathy with electrical status epilepticus during sleep. Epilepsia. 2011;52:602-9.
Groppel G, Dorfer C, Dressler A, Muhlebner A, Porsche B, Hainfellner JA, et al. Immediate termination of electrical status epilepticus in sleep after hemispherotomy is associated with significant progress in language development. Dev Med Child Neurol. 2017;59:89-97.
Patry G, Lyagoubi S, Tassinari CA. Subclinical “electrical status epilepticus” induced by sleep in children. A clinical and electroencephalographic study of six cases. Arch Neurol. 1971;24:242-52.
Kane N, Acharya J, Benickzy S, Caboclo L, Finnigan S, Kaplan PW, et al. A revised glossary of terms most commonly used by clinical electroencephalographers and updated proposal for the report format of the EEG findings. Revision 2017. Clin Neurophysiol Pract. 2017;2:170-85.
Current KP. Current status of treatments for children with electrical status in slow-wave sleep (ESES/CSWS). Epilepsy Curr. 2017;17:214-6.
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;28:172-83.
Janca R, Krsek P, Jezdik P, Cmejla R, Tomasek M, Komarek V, et al. The sub-regional functional organization of neocortical irritative epileptic networks in pediatric epilepsy. Front Neurol. 2018;9:184.
Wendt SL, Christensen JA, Kempfner J, Leonthin HL, Jennum P, Sorensen HB. Validation of a novel automatic sleep spindle detector with high performance during sleep in middle aged subjects. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:4250-3.
Fastenau PS, Johnson CS, Perkins SM, Byars AW, deGrauw TJ, Austin JK, et al. Neuropsychological status at seizure onset in children: risk factors for early cognitive deficits. Neurology. 2009;73:526-34.
Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat Commun. 2017;8:15930.
Sanchez Fernandez I, Loddenkemper T, Peters JM, Kothare SV. Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatr Neurol. 2012;47:390-410.
De Giorgis V, Filippini M, Macasaet JA, Masnada S, Veggiotti P. Neurobehavioral consequences of continuous spike and waves during slow sleep (CSWS) in a pediatric population: a pattern of developmental hindrance. Epilepsy Behav. 2017 Sep;74:1-9.
Shaw P. Intelligence and the developing human brain. BioEssays. 2007;29:962-73.
Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387:167-78.
Vendrame M, Zarowski M, Alexopoulos AV, Wyllie E, Kothare SV, Loddenkemper T. Localization of pediatric seizure semiology. Clin Neurophysiol. 2011;122:1924-8.
Wyllie E, Lachhwani DK, Gupta A, Chirla A, Cosmo G, Worley S, et al. Successful surgery for epilepsy due to early brain lesions despite generalized EEG findings. Neurology. 2007;24(69):389-97.
Gupta A, Chirla A, Wyllie E, Lachhwani DK, Kotagal P, Bingaman WE. Pediatric epilepsy surgery in focal lesions and generalized electroencephalogram abnormalities. Pediatr Neurol. 2007;37:8-15.
van den Munckhof B, van Dee V, Sagi L, Caraballo RH, Veggiotti P, Liukkonen E, et al. Treatment of electrical status epilepticus in sleep: a pooled analysis of 575 cases. Epilepsia. 2015;56:1738-46.
Duchowny M, Jayakar P, Resnick T, Harvey AS, Alvarez L, Dean P, et al. Epilepsy surgery in the first three years of life. Epilepsia. 1998;39:737-43.
Freitag H, Tuxhorn I. Cognitive function in preschool children after epilepsy surgery: rationale for early intervention. Epilepsia. 2005;46:561-7.
Lamberink HJ, Boshuisen K, van RP, Gosselaar PH, Braun KP. Changing profiles of pediatric epilepsy surgery candidates over time: a nationwide single-center experience from 1990 to 2011. Epilepsia 2015;56:717-25.
Liava A, Francione S, Tassi L, Lo Russo G, Cossu M, Mai R, et al. Individually tailored extratemporal epilepsy surgery in children: anatomo-electro-clinical features and outcome predictors in a population of 53 cases. Epilepsy Behav. 2012;25:68-80.
Moosa ANV, Wyllie E. Cognitive outcome after epilepsy surgery in children. Semin Peadiatr Neurol. 2017;24(4):331-9.
Sibilia V, Barba C, Metitieri T, Michelini G, Giordano F, Genitori L, et al. Cognitive outcome after epilepsy surgery in children: a controlled longitudinal study. Epilepsy Behav. 2017;73:23-30.
