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Journal of Pediatric Epilepsy 2021; 10(04): 141-146
DOI: 10.1055/s-0041-1731412
Review Article

Electrical Status Epilepticus during Sleep and Evaluating the Electroencephalogram

Michael Drees 
1   Department of Pediatric Neurology, Nationwide Children's Hospital, Tipp City, Ohio, United States
,
Neil Kulkarni
2   Department of Pediatric Neurology, Nationwide Children's Hospital, The Ohio State University, Columbus, Ohio, United States
,
Jorge Vidaurre
2   Department of Pediatric Neurology, Nationwide Children's Hospital, The Ohio State University, Columbus, Ohio, United States
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Abstract

Electrical status epilepticus during sleep (ESES) is an age-related, self-limited epileptic encephalopathy characterized by heterogeneous clinical manifestations and a specific electroencephalographic pattern of continuous spikes and waves during slow sleep. The etiology of ESES is not completely clear, although structural brain lesions, abnormal immunological markers, and genetic mutations have been associated with the syndrome. ESES was first described in 1971 and since then, the diagnostic criteria have changed multiple times. Additionally, inconsistency between authors in how to record and evaluate the electroencephalogram also leads to variability between studies. These inconsistencies hamper objectivity, comparison, and generalization. Because of this, one of the first priorities of physicians treating this condition should be defining the parameters of this disease so that cooperative building can occur.

Keywords

electrical status epilepticus during sleep - epileptic encephalopathy - spike-wave index - epileptiform activity


Publication History

Received: 11 February 2021

Accepted: 06 May 2021

Article published online:
19 July 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Tassinari CA, Rubboli G, Volpi L. et al. Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia. Clin Neurophysiol 2000; 111 (Suppl. 02) S94-S102
    CrossrefPubMedGoogle Scholar
  • 2 Fernández IS, Chapman KE, Peters JM. et al. The tower of Babel: survey on concepts and terminology in electrical status epilepticus in sleep and continuous spikes and waves during sleep in North America. Epilepsia 2013; 54 (04) 741-750
    CrossrefPubMedGoogle Scholar
  • 3 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 (03) 242-252
    CrossrefPubMedGoogle Scholar
  • 4 Scheltens-de Boer M. Guidelines for EEG in encephalopathy related to ESES/CSWS in children. Epilepsia 2009; 50 (Suppl. 07) 13-17
    CrossrefPubMedGoogle Scholar
  • 5 Lee YJ, Hwang SK, Kwon S. The clinical spectrum of benign epilepsy with centro-temporal spikes: a challenge in categorization and predictability. J Epilepsy Res 2017; 7 (01) 1-6
    CrossrefPubMedGoogle Scholar
  • 6 Fejerman N. Atypical Rolandic epilepsy. Epilepsia 2009; 50 (Suppl. 07) 9-12
    CrossrefPubMedGoogle Scholar
  • 7 van den Munckhof B, van Dee V, Sagi L. et al. Treatment of electrical status epilepticus in sleep: a pooled analysis of 575 cases. Epilepsia 2015; 56 (11) 1738-1746
    CrossrefPubMedGoogle Scholar
  • 8 Morrell F, Whisler WW, Bleck TP. Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 1989; 70 (02) 231-239
    CrossrefPubMedGoogle Scholar
  • 9 Kotagal P. Current status of treatments for children with electrical status in slow-wave sleep (ESES/CSWS). Epilepsy Curr 2017; 17 (04) 214-216
    CrossrefPubMedGoogle Scholar
  • 10 Galanopoulou AS, Bojko A, Lado F, Moshé SL. The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev 2000; 22 (05) 279-295
    CrossrefPubMedGoogle Scholar
  • 11 Coppola G, Federico RR, Epifanio G, Tagliente F, Bravaccio C. Focal polymicrogyria, continuous spike-and-wave discharges during slow-wave sleep and Cohen syndrome: a case report. Brain Dev 2003; 25 (06) 446-449
    CrossrefPubMedGoogle Scholar
  • 12 Guerrini R, Genton P, Bureau M. et al. Multilobar polymicrogyria, intractable drop attack seizures, and sleep-related electrical status epilepticus. Neurology 1998; 51 (02) 504-512
    CrossrefPubMedGoogle Scholar
  • 13 Kobayashi K, Nishibayashi N, Ohtsuka Y, Oka E, Ohtahara S. Epilepsy with electrical status epilepticus during slow sleep and secondary bilateral synchrony. Epilepsia 1994; 35 (05) 1097-1103
    CrossrefPubMedGoogle Scholar
  • 14 Fejerman N, Caraballo R, Cersósimo R, Ferraro SM, Galicchio S, Amartino H. Sulthiame add-on therapy in children with focal epilepsies associated with encephalopathy related to electrical status epilepticus during slow sleep (ESES). Epilepsia 2012; 53 (07) 1156-1161
    CrossrefPubMedGoogle Scholar
  • 15 Veggiotti P, Beccaria F, Papalia G, Termine C, Piazza F, Lanzi G. Continuous spikes and waves during sleep in children with shunted hydrocephalus. Childs Nerv Syst 1998; 14 (4-5): 188-194
    CrossrefPubMedGoogle Scholar
  • 16 Kersbergen KJ, de Vries LS, Leijten FSS. et al. Neonatal thalamic hemorrhage is strongly associated with electrical status epilepticus in slow wave sleep. Epilepsia 2013; 54 (04) 733-740
    CrossrefPubMedGoogle Scholar
  • 17 Oliveira AR, Nunes RG, Figueiredo P, Dias AI, Leal A. Regional white matter atrophy correlates with spike activity in encephalopathy related to status epilepticus during slow sleep (ESES) after early thalamic lesions. Brain Topogr 2020; 33 (05) 571-585
    CrossrefPubMedGoogle Scholar
  • 18 Sánchez Fernández I, Takeoka M, Tas E. et al. Early thalamic lesions in patients with sleep-potentiated epileptiform activity. Neurology 2012; 78 (22) 1721-1727
    CrossrefPubMedGoogle Scholar
  • 19 van den Munckhof B, Zwart AF, Weeke LC. et al. Perinatal thalamic injury: MRI predictors of electrical status epilepticus in sleep and long-term neurodevelopment. Neuroimage Clin 2020; 26: 102227
    CrossrefPubMedGoogle Scholar
  • 20 Sánchez Fernández I, Peters JM, Akhondi-Asl A, Klehm J, Warfield SK, Loddenkemper T. Reduced thalamic volume in patients with electrical status epilepticus in sleep. Epilepsy Res 2017; 130: 74-80
    CrossrefPubMedGoogle Scholar
  • 21 Van Hirtum-Das M, Licht EA, Koh S, Wu JY, Shields WD, Sankar R. Children with ESES: variability in the syndrome. Epilepsy Res 2006; 70 (Suppl. 01) S248-S258
    CrossrefPubMedGoogle Scholar
  • 22 Buzatu M, Bulteau C, Altuzarra C, Dulac O, Van Bogaert P. Corticosteroids as treatment of epileptic syndromes with continuous spike-waves during slow-wave sleep. Epilepsia 2009; 50 (Suppl. 07) 68-72
    CrossrefPubMedGoogle Scholar
  • 23 Sánchez Fernández I, Loddenkemper T, Peters JM, Kothare SV. Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatr Neurol 2012; 47 (06) 390-410
    CrossrefPubMedGoogle Scholar
  • 24 Gardella E, Cantalupo G, Larsson PG. et al. EEG features in Encephalopathy related to Status Epilepticus during slow Sleep. Epileptic Disord 2019; 21 (S1): 22-30
    PubMedGoogle Scholar
  • 25 van den Munckhof B, de Vries EE, Braun KPJ. et al. Serum inflammatory mediators correlate with disease activity in electrical status epilepticus in sleep (ESES) syndrome. Epilepsia 2016; 57 (02) e45-e50
    CrossrefPubMedGoogle Scholar
  • 26 Kessi M, Peng J, Yang L. et al. Genetic etiologies of the electrical status epilepticus during slow wave sleep: systematic review. BMC Genet 2018; 19 (01) 40
    CrossrefPubMedGoogle Scholar
  • 27 Lesca G, Møller RS, Rudolf G, Hirsch E, Hjalgrim H, Szepetowski P. Update on the genetics of the epilepsy-aphasia spectrum and role of GRIN2A mutations. Epileptic Disord 2019; 21 (S1): 41-47
    Google Scholar
  • 28 Medline Plus. GRIN2A Gene. Bethesda: National Library of Medicine; 2020
    Google Scholar
  • 29 Yuan H, Hansen KB, Zhang J. et al. Functional analysis of a de novo GRIN2A missense mutation associated with early-onset epileptic encephalopathy. Nat Commun 2014; 5: 3251
    Google Scholar
  • 30 Sun Y, Liu YD, Xu ZF, Kong QX, Wang YL. CNKSR2 mutation causes the X-linked epilepsy-aphasia syndrome: a case report and review of literature. World J Clin Cases 2018; 6 (12) 570-576
    CrossrefPubMedGoogle Scholar
  • 31 Bonardi CM, Mignot C, Serratosa JM. et al. Expanding the clinical and EEG spectrum of CNKSR2-related encephalopathy with status epilepticus during slow sleep (ESES). Clin Neurophysiol 2020; 131 (05) 1030-1039
    CrossrefPubMedGoogle Scholar
  • 32 Vaags AK, Bowdin S, Smith ML. et al. Absent CNKSR2 causes seizures and intellectual, attention, and language deficits. Ann Neurol 2014; 76 (05) 758-764
    CrossrefPubMedGoogle Scholar
  • 33 Pavlidis E, Møller RS, Nikanorova M. et al. Idiopathic encephalopathy related to status epilepticus during slow sleep (ESES) as a “pure” model of epileptic encephalopathy. An electroclinical, genetic, and follow-up study. Epilepsy Behav 2019; 97: 244-252
    CrossrefPubMedGoogle Scholar
  • 34 Kramer U, Nevo Y, Neufeld MY, Fatal A, Leitner Y, Harel S. Epidemiology of epilepsy in childhood: a cohort of 440 consecutive patients. Pediatr Neurol 1998; 18 (01) 46-50
    CrossrefPubMedGoogle Scholar
  • 35 Gencpinar P, Dundar NO, Tekgul H. Electrical status epilepticus in sleep (ESES)/continuous spikes and waves during slow sleep (CSWS) syndrome in children: an electroclinical evaluation according to the EEG patterns. Epilepsy Behav 2016; 61: 107-111
    CrossrefPubMedGoogle Scholar
  • 36 van den Munckhof B, Alderweireld C, Davelaar S. et al. Treatment of electrical status epilepticus in sleep: clinical and EEG characteristics and response to 147 treatments in 47 patients. Eur J Paediatr Neurol 2018; 22 (01) 64-71
    CrossrefPubMedGoogle Scholar
  • 37 Arhan E, Serdaroglu A, Aydin K, Hırfanoglu T, Soysal AS. Epileptic encephalopathy with electrical status epilepticus: an electroclinical study of 59 patients. Seizure 2015; 26: 86-93
    CrossrefPubMedGoogle Scholar
  • 38 Landau WM, Kleffner FR. Syndrome of acquired aphasia with convulsive disorder in children. Neurology 1957; 7 (08) 523-530
    CrossrefPubMedGoogle Scholar
  • 39 Tassinari CA, Terzano G, Capocchi G. et al. Epileptic seizures during sleep in children. Paper presented at: Epilepsy, The 8th International Symposium; New York:
    Google Scholar
  • 40 Tassinari CA, Dravet C, Roger J. Encephalopathy related to electrical status epilepticus during slow sleep. Electroencephalogr Clin Neurophysiol 1977; 43: 529-530
    PubMedGoogle Scholar
  • 41 Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989; 30 (04) 389-399
    CrossrefPubMedGoogle Scholar
  • 42 Uliel-Sibony S, Kramer U. Benign childhood epilepsy with Centro-Temporal spikes (BCECTSs), electrical status epilepticus in sleep (ESES), and academic decline--how aggressive should we be?. Epilepsy Behav 2015; 44: 117-120
    CrossrefPubMedGoogle Scholar
  • 43 Beaumanoir A, Bureau M, Mira L. ‘Identification of the Syndrome.’ Continuous Spike and Waves during Slow Sleep. London, United KIngdom: Oxford; 1995: 243-249
    Google Scholar
  • 44 Raha S, Shah U, Udani V. Neurocognitive and neurobehavioral disabilities in epilepsy with electrical status epilepticus in slow sleep (ESES) and related syndromes. Epilepsy Behav 2012; 25 (03) 381-385
    CrossrefPubMedGoogle Scholar
  • 45 Bölsterli BK, Gardella E, Pavlidis E. et al. Remission of encephalopathy with status epilepticus (ESES) during sleep renormalizes regulation of slow wave sleep. Epilepsia 2017; 58 (11) 1892-1901
    CrossrefPubMedGoogle Scholar
  • 46 Inutsuka M, Kobayashi K, Oka M, Hattori J, Ohtsuka Y. Treatment of epilepsy with electrical status epilepticus during slow sleep and its related disorders. Brain Dev 2006; 28 (05) 281-286
    CrossrefPubMedGoogle Scholar
  • 47 Tassinari CA, Rubboli G. Encephalopathy related to status epilepticus during slow sleep: current concepts and future directions. Epileptic Disord 2019; 21 (S1) 82-87
    PubMedGoogle Scholar
  • 48 Hempel A, Frost M, Agarwal N. Language and behavioral outcomes of treatment with pulse-dose prednisone for electrical status epilepticus in sleep (ESES). Epilepsy Behav 2019; 94: 93-99
    CrossrefPubMedGoogle Scholar
  • 49 Yan Liu X, Wong V. Spectrum of epileptic syndromes with electrical status epilepticus during sleep in children. Pediatr Neurol 2000; 22 (05) 371-379
    CrossrefPubMedGoogle Scholar
  • 50 García-Peñas JJ. [Antiepileptic drugs in the treatment of autistic regression syndromes]. Rev Neurol 2005; 40 (Suppl. 01) S173-S176
    PubMedGoogle Scholar
  • 51 Teixeira KC, Montenegro MA, Cendes F, Guimarães CA, Guerreiro CA, Guerreiro MM. Clinical and electroencephalographic features of patients with polymicrogyria. J Clin Neurophysiol 2007; 24 (03) 244-251
    CrossrefPubMedGoogle Scholar
  • 52 Wang S, Weil AG, Ibrahim GM. et al. Surgical management of pediatric patients with encephalopathy due to electrical status epilepticus during sleep (ESES). Epileptic Disord 2020; 22 (01) 39-54
    PubMedGoogle Scholar
  • 53 Wiwattanadittakul N, Depositario-Cabacar D, Zelleke TG. Electrical status epilepticus in sleep (ESES) - treatment pattern and EEG outcome in children with very high spike-wave index. Epilepsy Behav 2020; 105: 106965
    CrossrefPubMedGoogle Scholar
  • 54 Liukkonen E, Kantola-Sorsa E, Paetau R, Gaily E, Peltola M, Granström ML. Long-term outcome of 32 children with encephalopathy with status epilepticus during sleep, or ESES syndrome. Epilepsia 2010; 51 (10) 2023-2032
    CrossrefPubMedGoogle Scholar
  • 55 Lewine JD, Andrews R, Chez M. et al. Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders. Pediatrics 1999; 104 (3 Pt 1): 405-418
    CrossrefPubMedGoogle Scholar
  • 56 Massa R, de Saint-Martin A, Hirsch E. et al. Landau-Kleffner syndrome: sleep EEG characteristics at onset. Clin Neurophysiol 2000; 111 (Suppl. 02) S87-S93
    CrossrefPubMedGoogle Scholar
  • 57 Aeby A, Poznanski N, Verheulpen D, Wetzburger C, Van Bogaert P. Levetiracetam efficacy in epileptic syndromes with continuous spikes and waves during slow sleep: experience in 12 cases. Epilepsia 2005; 46 (12) 1937-1942
    CrossrefPubMedGoogle Scholar
  • 58 Weber AB, Albert DV, Yin H, Held TP, Patel AD. Diagnosis of electrical status epilepticus during slow-wave sleep with 100 seconds of sleep. J Clin Neurophysiol 2017; 34 (01) 65-68
    CrossrefPubMedGoogle Scholar
  • 59 Fernández IS, Peters JM, Hadjiloizou S. et al. Clinical staging and electroencephalographic evolution of continuous spikes and waves during sleep. Epilepsia 2012; 53 (07) 1185-1195
    CrossrefPubMedGoogle Scholar
  • 60 Saltik S, Uluduz D, Cokar O, Demirbilek V, Dervent A. A clinical and EEG study on idiopathic partial epilepsies with evolution into ESES spectrum disorders. Epilepsia 2005; 46 (04) 524-533
    CrossrefPubMedGoogle Scholar
  • 61 Joshi CN, Chapman KE, Bear JJ, Wilson SB, Walleigh DJ, Scheuer ML. Semiautomated spike detection software Persyst 13 is noninferior to human readers when calculating the spike-wave index in electrical status epilepticus in sleep. J Clin Neurophysiol 2018; 35 (05) 370-374
    CrossrefPubMedGoogle Scholar
  • 62 Zhao X, Wang X, Chen C. et al. A knowledge-based approach for automatic quantification of epileptiform activity in children with electrical status epilepticus during sleep. J Neural Eng 2020; 17 (04) 046032
    CrossrefPubMedGoogle Scholar