Encephalopathy with Electrical Status Epilepticus in Slow Wave Sleep – a review with an emphasis on regional (perisylvian) aspects

• Authors: Peter Halász , Márta Hegyi , Zsuzsa Siegler , András Fogarasi
• Languages of publication: EN

Abstracts

EN

Aim. The aim of this article is to review criticaly the Electrical Status Epilepticus in Slow Sleep (ESES) phenomenon from a neurophysiological mechanisms aspect as well as terminological and classification issues.Methods. The review includes all the relevant papers published during the last 43 years on the subject of ESES and Continous Spike – Wave in Sleep (CSWS).These papers were identified in various large databases via the internet.Rewiev and remarks. ESES/CSWS phenomena can be held as a common final pathway originating from different etiologies, including patients with early brain damage (probably involving thalamic structures), but also patients without structural pathology as in atypical evolution of idiopathic regional childhood hyperexcitability syndromes (with Rolandic epilepsy as a prototype). There are hints that genetic predisposition might be an important factor in the development of this process. The two large patient groups (lesional and non-lesional) show the same EEG evolution and encephalopathic cognitive consequences. The sleep EEG activation can be held as a common endophenotype. ESES represents an extreme sleep activation/potentiation of the local/regional interictal discharges, enhancing them in frequency, territorial extension, intra and trans-hemispherial propagation, synchrony and continuity. This process is most probably not identical with the development of bilateral spike-wave pattern in „generalized” epilepsies which involves primarily or secondarily the thalamocortical system as it had been explored by Gloor (1979) for idiopathic generalized rpilepsy and Steriade and Amzica (2003) for different types of generalized spike and wave discharges.Conclusions and syndromological embedding of ESES. In an overwhelming majority of the investigated cases, the maps of the single discharges constituting sleep activation are identical; with focal/regional interictal spikes followed by slow closing wave, as it is seen in childhood regional age dependent hyperexcitability syndromes (prototype of the centro-temporal spikes of Rolandic epilepsy). The main mechanism of the developing cognitive impairment is most probably the consequence of interference with plastic function of slow wave sleep by obliterating synaptic decline during sleep. Presently, the consensus and co-operative research is highly obstacled by the terminological chaos, the controversial definitions and views around this still striking and enigmatic phenomenon.

Keywords

EN

Electrical Status Epilepticus in Slow Sleep; Continuous Spike-Wave in slow Sleep; perisylvian epileptic network; cognitive impairment; sleep plastic functions; synaptic decline during slow wave sleep; atypical Rolandic epilepsy; early thalamic lesions

• Publisher: De Gruyter Open
• Journal: Journal of Epileptology
• Year: 2014
• Volume: 22
• Issue: 2
• Pages: 71-87

Dates

published

1 - 12 - 2014

online

1 - 3 - 2015

received

16 - 9 - 2014

accepted

3 - 12 - 2014

Contributors

author

Peter Halász

• National Institute of Clinical Neurosciences, Budapest

author

Márta Hegyi

• Bethesda Children Hospital Epilepsy Center, Budapest

author

Zsuzsa Siegler

• Bethesda Children Hospital Epilepsy Center, Budapest

author

András Fogarasi

• Bethesda Children Hospital Epilepsy Center, Budapest

References

• 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: 1937–1942.[PubMed][Crossref]
• Andrade-Machado R.:Early thalamic lesions in patients with sleep-potentiated pileptiform activity. Neurology, 2012, 79: 2218; author reply 2218–2219.[Crossref]
• Beaumanoir A.:Continuous spike-waves during slow wave sleep. Electrical status epilepticus during slow wave sleep. London John Libey, 1995, 217–223.
• Beelke M., Nobili L., Baglietto M.G., De Carli F., Robert A., De Negri E. et al.:Relationship of sigma activity to sleep interictal epileptic discharges: a study in children affected by benign epilepsy with occipital paroxysms. Epilepsy Res., 2000, 40: 179–186.[PubMed][Crossref]
• Berg A.T., Berkovic S.F., Brodie M.J., Buchhalter J., Cross J.H., van Emde Boas W. 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: 676–685.[Crossref]
• Bersagliere A., Achermann P.:Slow oscillations in human non-rapid eye movement sleep electroencephalogram: effects of increased sleep pressure. J. Sleep. Res., 2010, 19: 228–237.[Crossref]
• Bigna K., Bölsterli H., Fattinger S., Kurth S., LeBourgeois M.K., Ringli M. et al.:Spike wave location and density disturb sleep slow waves in patients with CSWS (continuous spike waves during sleep). Epilepsia, 2014, 55: 584–591.[Crossref]
• Boel M., Casaer P.:Continuous spikes and waves during slow sleep: a 30 months follow-up study of neuropsychological recovery and EEG findings. Neuropediatrics, 1989, 20: 176–180.[Crossref][PubMed]
• Borbély A.A.:A two process model of sleep regulation. Hum. Neurobiol., 1982, 1: 195–204.[PubMed]
• Bölsterli B.K., Schmitt B., Bast T., Critelli H., Heinzle J., Jenni O.G. et al.:Impaired slow wave sleep downscaling in encephalopathy with status epilepticus during sleep (ESES). Clin. Neurophysiol., 2011, 122: 1779–1787.[PubMed][Crossref]
• Bureau M.:Outstanding cases of CSWS and LKS: analysis of the data sheets provided by the participants. In: A. Beaumanoir, M. Bureau, T. Deonna et al. (eds.), Continuous Spikes and Waves During Slow Sleep. Electrical Status Epilepticus During Slow Sleep: Acquired Epileptic Aphasia and Related Conditions. John Libbey, London 1995, 213–216.
• Cantalupo G., Rubboli G., Tassinari C.A.:Night-time unravelling of the brain web: impaired synaptic downscaling in ESES – the Penelope syndrome. Clin. Neurophysiol., 2011, 122: 1691–1692.[Crossref][PubMed]
• Caraballo R.H., Bongiorni L., Cersósimo R., Semprino M., Espeche A., Fejerman N.:Epileptic encephalopathy with continuous spikes and waves during sleep inchildren with shunted hydrocephalus: a study of nine cases. Epilepsia, 2008, 49: 1520–1527.
• Clemens B., Majoros E.:Sleep studies in benign epilepsy of childhood with rolandic spikes. II. Analysis of discharge frequency and its relation to sleep dynamics. Epilepsia, 1987, 28: 24–27.[Crossref][PubMed]
• Dalla Bernardina B., Tassinari C.A., Dravet C., Bureau M., Beghini G., Roger J.:Benign focal epilepsy and “electrical status epilepticus” during sleep Rev Electroencephalogr. Neurophysiol. Clin., 1978, 8: 350–353.
• Dalla Bernardina B., Sgrò V., Caraballo R., Fontana E., Colamaria V., Zullini E. et al.:Sleep and benign partial epilepsies of childhood: EEG and evoked potentials study. Epilepsy Res., Suppl. 1991, 2: 83–96.
• De Negri M.:Electrical status epilepticus during sleep (ESES). Different clinical syndromes: towards a unifying view? Brain Dev., 1997, 19: 447–551.[Crossref][PubMed]
• De Tiège X., Goldman S., Laureys S., Verheulpen D., Chiron C., Wetzburger C. et al.:Regional cerebral glucose metabolism in epilepsies with continuous spikes and waves during sleep. Neurology, 2004, 63: 853–857.[PubMed][Crossref]
• De Tiège X., Trotta N., Op de Beeck M., Bourguignon M., Marty B., Wens V. et al.:Neurophysiological activity underlying altered brain metabolism in epileptic encephalopathies with CSWS. Epilepsy Res., 2013, 105: 316–325.[Crossref]
• Deonna T., Roulet-Perez E.:Early-onset acquired epileptic aphasia (Landau-Kleffner syndrome, LKS) and regressive autistic disorders with epileptic EEG abnormalities: the continuing debate. Brain Dev., 2010, 32: 746–752.[Crossref][PubMed]
• Doose H., Baier W.K.:Benign partial epilepsy and related conditions: multifactoral pathogenesis with hereditary impairment of brain maturation. Eur. J. Pediatr., 1989, 149: 152–158.[Crossref]
• Dulac O., Billard C., Arthuis M.:Electroclinical and developmental aspects of epilepsy in the aphasia-epilepsy syndrome. Arch. Fr. Pediatr., 1983, 40: 299–308.[PubMed]
• Galanopoulou A.S., Bojko A., Lado F., Moshé S.L.:The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev., 2000, 22: 279–295.[Crossref][PubMed]
• Echlin F.A., Battista A.:Epileptiform Seizures From Chronic Isolated Cortex. Arch. Neurol., 1963, 9: 154–170[Crossref][PubMed]
• Engel J. Jr.:ILAE classification of epilepsy syndromes. Epilepsy Res., 2006, 70, Suppl. 1: S5–S10.[Crossref]
• Fejerman N.:Atypical rolandic epilepsy. Epilepsia, 2009, 50 Suppl. 7: 9–12.[Crossref][PubMed]
• Foldvary-Schaefer N., Grigg-Damberger M.:Sleep and epilepsy: what we know, don't know, and need to know. J. Clin. Neurophysiol., 2006, 23: 4–20.[Crossref]
• Fueki N., Iinuma K., Kojima A., Haginoya K., Yanai K., Tada K. et al.:Alteration of regional cerebral metabolic rate for glucose at interictal and ictal stages in a case of epilepsy with electrical status epilepticus during slow sleep. Jpn. J. Psychiatry Neurol., 1988, 42: 611–612.
• Gaggero R., Caputo M., Fiorio P., Pessagno A., Baglietto M.G., Muttini P. et al.:SPECT and epilepsy with continuous spike waves during slow-wave sleep. Childs. Nerv. Syst., 1995, 11: 154–160.[Crossref][PubMed]
• García-Peñas J.J.:Neurocognitive dysfunction in electrical status epilepticus during slow-wave sleep syndrome: Can the natural course of the syndrome be modified with early pharmacological treatment? Rev. Neurol., 2010, 3, 50, Suppl. 3: S37–S47.
• Gloor P.:Generalized epilepsy with spike-and-wave discharge: a reinterpretation of its electrographic and clinical manifestations. The 1977 William G. Lennox Lecture, American Epilepsy Society. Epilepsia, 1979, 20: 571–588.[Crossref]
• Guerrini R., Genton P., Bureau M., Parmeggiani A., Salas-Puig X., Santucci M. et al.:Clinical and electroencephalographicfeatures of patients with polymicrogyria. J. Clin. Neurophysiol., 2007, 24: 244–251.[Crossref]
• Guzzetta F., Battaglia D., Veredice C., Donvito V., Pane M., Lettori D. et al.:Early thalamic injury associated with epilepsy and continuous spike-wave during slow sleep. Epilepsia, 2005, 46: 889–900.[PubMed][Crossref]
• Halász P., Kelemen A., Clemens B., Saracz J., Rosdy B., Rásonyi G. et al.:The perisylvian epileptic network. A unifying concept. Ideggyogy Sz. 2005, 20, 58: 21–31.
• Hegyi M., Siegler Z., Barsi P., Rudas G., Lengyel Z., Szakáll S. et al.:Surgical treatment of resistant epilepsy, caused by hemi-spherical dysgenesis – case report. Ideggyogy Sz., 2009, 62: 185–189 (Hungarian).
• Hegyi M., Siegler Zs., Fogarasi A., Barsi P., Halász P.:Age dependent features of lesional and non-lesional patients with Electrical Status Epilepticus in slow Sleep. Accepted in “Clinical Neuroscience”, 2014.
• Huber R., Ghilardi M.F., Massimini M., Tononi G.:Local sleep and learning. Nature, 2004, 1, 430: 78–81.[Crossref]
• Huber R., Ghilardi M.F., Massimini M., Ferrarelli F., Riedner B.A., Peterson M.J. et al.:Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci., 2006, 9: 1169–1176.[Crossref][PubMed]
• Huber R., Esser S.K., Ferrarelli F., Massimini M., Peterson M.J., Tononi G.:TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS One, 2007, 7: 2.
• Hirsch E., Marescaux C., Maquet P., Metz-Lutz M.N., Kiesmann M., Salmon E. et al.:Landau-Kleffner syndrome: a clinical and EEG study of five cases. Epilepsia, 1990, 1: 756–767.[Crossref]
• 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: 281–286.[Crossref][PubMed]
• Kelemen A., Barsi P., Gyorsok Z., Sarac J., Szucs A., Halász P.:Thalamic lesion and epilepsy with generalized seizures, ESES and spike-wave paroxysms – report of three cases. Seizure, 2006, 15: 454–458.[Crossref][PubMed]
• Kellaway P.:The electroencephalographic features of benign centrotemporal (rolandic) epilepsy of childhood. Epilepsia, 2000, 41: 1053–1056.[PubMed][Crossref]
• Kellermann K.:Recurrent aphasia with subclinical bioelectric status epilepticus during sleep. Eur. J. Pediatr., 1978, 128: 207–212.[PubMed][Crossref]
• Kevelam S.H., Jansen F.E., Binsbergen Ev., Braun K.P., Verbeek N.E., Lindhout D. et al.:Copy number variations in patients with electrical status epilepticus in sleep. J. Child. Neurol., 2012, 27: 178–182.[Crossref]
• 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: 1097–1103.[Crossref][PubMed]
• Kramer U., Sagi L., Goldberg-Stern H., Zelnik N., Nissenkorn A., Ben-Zeev B.:Clinical spectrum and medical treatment of children with electrical status epilepticus in sleep (ESES). Epilepsia, 2009, 50: 1517–1524.[PubMed][Crossref]
• Laurette G., Arfel G.:Electrographic “status epilepticus” during afternoon sleep. Rev. Electroencephalogr. Neurophysiol. Clin., 1976, 6: 137–139.[Crossref][PubMed]
• Lemke J.R., Lal D., Reinthaler E.M., Steiner I., Nothnagel M., Alber M. et al.:Mutations in GRIN2A cause idiopathic focal epilepsy with rolandic spikes. Nat. Genet., 2013, 45: 1067–1072.[Crossref]
• Lerman P., Kivity S.:The benign partial nonrolandic epilepsies (review). J. Clin. Neurophysiol., 1991, 8: 275–287.[Crossref]
• Lesca G., Rudolf G., Labalme A., Hirsch E., Arzimanoglou A. et al.:Epileptic encephalopathies of the Landau-Kleffner and continuous spike and waves during slow-wave sleep types: genomic dissection makes the link with autism. Epilepsia, 2012, 53: 1526–1538.[Crossref][PubMed]
• Liukkonen E., Kantola-Sorsa E., Paetau R., Gaily E., Peltola M., Granström. M.L.:Long-term outcome of 32 children with encephalopathy with status epilepticus during sleep, or ESES syndrome. Epilepsia, 2010, 51: 2023–2032.[PubMed][Crossref]
• Loddenkemper T., Cosmo G., Kotagal P., Haut J., Klaas P., Gupta A.:Epilepsy surgery in children with electrical status epilepticus in sleep. Neurosurgery, 2009, 64: 328–337.[Crossref][PubMed]
• Loddenkemper T., Sánchez Fernández J., Peters J.M.:Continuous spike and waves during sleep and electrical status epilepticus in sleep. J. Clin. Neurophysiol., 2011, 28: 154–164.[Crossref]
• Loddenkemper T.:Early thalamic lesions in patients with sleep-potentiated epileptiform activity. Neurology, 2012, 78: 1721–1727.[PubMed][Crossref]
• Majkowski J.:Kindling and Memory. In: T.G. Bolwig and M.R. Trimble (Eds), The Clinical Relevance of Kindling. John Wiley, Chichester – New York – Brisbane – Toronto – Singapore 1989, 87–102.
• Massimini M., Ferrarelli F., Esser S.K., Riedner B.A., Huber R., Murphy M. et al.:Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl. Acad. Sci., USA, 2007, 104: 8496–8501.[Crossref]
• Maquet P., Hirsch E., Metz-Lutz M.N., Motte J., Dive D., Marescaux C. et al.:Regional cerebral glucose metabolism in children with deterioration of one or more cognitive functions and continuous spike-and-wave discharges during sleep. Brain, 1995, 118: 1497–1520.[PubMed][Crossref]
• Maquet P., Metz-Lutz M.N., de Saint-Martin A., Marescaux C., Hirsch E.:Isotope tracer-techniques in rolandic epilepsy and its variants. Epileptic Disord., 2000, 2 Suppl. 1: S55–S57.
• Maquet P., Hirsch E., Metz-Lutz M.N., Motte J., Dive D., Marescaux C. et al.:Regional cerebral glucose metabolism in children with deterioration of one or more cognitive functions and continuous spike-and-wave discharges during sleep. Brain, 1995, 118: 1497–1520.[PubMed][Crossref]
• Moeller F., Moehring J., Ick I., Steinmann E., Wolff S., Jansen O. et al.:EEG-fMRI in atypical benign partial epilepsy. Epilepsia, 2013, 54: 103–108.[Crossref]
• Metz-Lutz M.N., Filippini M.:Neuropsychological findings in Rolandic epilepsy and Landau-Kleffner syndrome. Epilepsia, 2006, 47 Suppl. 2: 71–5.[Crossref]
• Monteiro J.P., Roulet-Perez E., Davidoff V., Deonna T.:Primary neonatal thalamic haemorrhage and epilepsy with continuous spike-wave during sleep: a longitudinal follow-up of a possible significant relation. Eur. J. Paediatr. Neurol., 2001, 5: 41–47.
• Morikawa T., Seino M., Watanabe M.:Long-term outcome of ESES syndrome. In: A. Beaumanoir, M. Bureau, T. Deonna, L. Mira, C.A. Tassinari (eds), Continuous Spikes and Waves during Slow Wave Sleep. Electrical status epilepticus during Slow Sleep. John Libey, London 1995, 27–36.
• Morrell F., Whisler W.W., Smith M.C., Hoeppner T.J., de Toledo-Morrell L., Pierre-Louis S.J. et al.:Landau-Kleffner syndrome. Treatment with subpial intracortical transection. Brain, 1995, 118: 1529–1546.[Crossref]
• Nickels K., Wirrell E.:Electrical status epilepticus in sleep. Semin. Pediatr. Neurol., 2008, 15: 50–60.[Crossref][PubMed]
• Nobili L., Ferrillo F., Baglietto M.G., Beelke M., De Carli F., De Negri E. et al.:Relationship of sleep interictal epileptiform discharges to sigma activity (12–16 Hz) in benign epilepsy of childhood with rolandic spikes. Clin. Neurophysiol., 1999, 110: 39–46.[Crossref]
• Overvliet G.M., Besseling R.M., Vles J.S., Hofman P.A., Backes W.H., van Hall M.H. et al.:Nocturnal epileptiform EEG discharges, nocturnal epileptic seizures, and language impairments in children: review of the literature. Epilepsy Behav., 2010, 19: 550–558.[Crossref][PubMed]
• Panayiotopoulos C.P.:Early onset benign childhood occipital seizures: Panayiotopoulos syndrome. In: C.P. Panayiotopoulos (ed.), Benign childhood partial seizures and related epileptic syndromes. John Libbey, London 1999, 133–147.
• Patry G., Lyagoubi S., Tassinari C.A.:Subclinical electrical status epilepticus induced by sleep in children. Arch. Neurol., 1971, 24: 242–252.[Crossref][PubMed]
• Penfield W. and Jasper H.:Epilepsy and the functional anatomy of the human brain. Little, Brown & Co., Oxford 1954, 605–614.
• Praline J., Barthez M.A., Casteniau P., Debiais S., Lucas B., Billard C. et al:Atypical language impairment in two siblings: relationship with electrical status epilepticus in sleep. J. Neurol. Sci., 2006, 249: 166–171.[Crossref]
• Quigg M., Noachtar S.:Sleep-potentiated epileptic discharges, language regression, and pediatric thalamic lesions. Neurology, 2012, 78: 1708–1709.[Crossref][PubMed]
• Rovó Z., Ulbert I., Acsády L.:Drivers of the primate thalamus. J. Neurosci., 2012, 32: 17894–17908.[Crossref]
• Rudolf G., Valenti M.P., Hirsch E., Szepetowski P.:From rolandic epilepsy to continuous spike-and-waves during sleep and Landau-Kleffner syndromes: insights into possible genetic factors. Epilepsia, 2009, 50 (suppl. 7): 25–28.[Crossref][PubMed]
• 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: 524–533.[PubMed][Crossref]
• Sánchez Fernández I., Loddenkemper T., Peters J.M., Kothare S.V.:Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatr. Neurol., 2012, 47: 390–410.[Crossref][PubMed]
• Sánchez Fernández I., Peters J.M., Hadjiloizou S., Prabhu S.P., Zarowski M., Stannard K.M. et al.:Clinical staging and electroencephalographic evolution of continuous spikes and waves during sleep. Epilepsia, 2012b, 53: 1185–1195.[Crossref]
• Sánchez Fernández I., Chapman K.E., Peters J.M., Kothare S.V., Nordli D.R. Jr, Jensen F.E. 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: 741–750.[Crossref]
• Schaul N.:The fundamental neural mechanisms of electroencephalography. Electroencephalography and Clinical Neurophysiology, 1998, 106: 101–107.
• Siniatchkin M., Groening K., Moehring J., Moeller F., Boor R., Brodbeck V. et al.:Neuronal networks in children with continuous spikes and waves during slow sleep. Brain, 2010, 133: 2798–2813.[Crossref][PubMed]
• Steriade M., Amzica F.:Sleep oscillations developing into seizures in corticothalamic systems. Epilepsia, 2003, 44 Suppl. 12: 9–20.[PubMed][Crossref]
• Stickgold R., James L., Hobson J.A.:Visual discrimination learning requires sleep after training. Nat. Neurosci., 2000, 3: 1237–1238.[Crossref][PubMed]
• Tas E., Takeoka M., Molino J., Gregas M., Eksioglu Y.Z., Rotenberg A. et al.:Thalamic lesion increase the frequency of spiking during sleep (abstract). Epilepsia, 2009, 50 (suppl. 11): 479.
• Tassinari C.A., Dravet C., Roger J.:Encephalopathy related to electrical status epilepticus during slow sleep. Electroenceph. Clin. Neurophysiol., 1977, 43: 529–530.
• Tassinari C.A., Bureau M., Dravet C., Dalla Bernardina B., Roger J.:Epilepsy with continuous spike and waves during slow sleep. In: J. Roger, C. Dravet, M. Bureau, F.E. Dreifuss, P. Wolf (eds.), Epileptic Syndromes in Infancy, Childhood and Adolescence. John Libbey, London 1985, 194–204.
• Tassinari C.A, Rubboli G., Volpi L., Meletti S., d'Orsi G., Franca M. et al.:Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia. Clin. Neurophysiol., 2000, 111 Suppl. 2: S94–S102.[Crossref]
• Tassinari C.A., Cantalupo G., Rios-Pohl L., Giustina E.D., Rubboli G.:Encephalopathy with status epilepticus during slow sleep: “the Penelope syndrome”. Epilepsia, 2009, 50 Suppl. 7: 4–8.[PubMed][Crossref]
• Tassinari C.A., Cantaplupo G., DallaBernardina B., Darra F., Bureau M., Cirelli C. et al.:Encephalopathy related to Status Epilepticus during Slow Sleep (ESES) including Landau-Kleffner Syndrome. In: Bureau et al. (Eds.), Epileptic Syndromes in Infancy and Adolescence, 5th Ed. John Libbey Eurotext Ltd. 2012, 255–275.
• Teixeira K.C., Cendes F., Guerreiro C.A., Guerreiro M.M.:Focal electrical status (FES): a new finding associated with polymicrogyria. J. Clin. Neurophysiol., 2009, 26: 155–159.[Crossref]
• Tononi G., Cirelli C.:Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull., 2003, 62: 143–150.[Crossref][PubMed]
• Tovia E., Goldberg-Stern H., Ben Zeev B., Heyman E., Watemberg N., Fattal-Valevski Kramer U.:The prevalence of atypical presentations and comorbidities of benign childhood epilepsy with centrotemporal spikes. Epilepsia, 2011, 52: 1483–1488.[Crossref][PubMed]
• Tükel K., Jasper H.:The electroencephalogram in parasagittal lesions. Electroencephalogr. Clin. Neurophysiol., 1952, 4: 481–494.[PubMed][Crossref]
• Van Bogaert P., Aeby A., De Borchgrave V., De Cocq C., Deprez M., De Tiège X. et al.:The epileptic syndromes with continuous spikes and waves during slow sleep: definition and management guidelines. Acta Neurol. Belg., 2006, 106: 52–60.[PubMed]
• Van Hirtum-Das M., Licht E.A., Koh S., Wu J.Y., Shields W.D., Sankar R.:Children with ESES: variability in the syndrome. Epilepsy Res., 2006, 70 Suppl. 1: S248–S258.[Crossref]
• Veggiotti P., Beccaria F., Guerrini R., Capovilla G., Lanzi G.:Continuous spike-and-wave activity during slow-wave sleep: syndrome or EEG pattern? Epilepsia, 1999, 40: 1593–1601.[PubMed][Crossref]
• Vyazovskiy V.V., Cirelli C., Pfister-Genskow M., Faraguna U., Tononi G.:Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci., 2008, 11: 200–208.[PubMed][Crossref]
• Yan Liu X., Wong V.:Spectrum of epileptic syndromes with electrical status epilepticus during sleep in children. Pediatr. Neurol., 2000, 22: 371–379.[Crossref][PubMed]
• Yasuhara A., Yoshida H., Hatanaka T., Sugimoto T., Kobayashi Y., Dyken E.:Epilepsy with continuous spike-waves during slow sleep and its treatment. Epilepsia, 1991, 32: 59–62.[PubMed][Crossref]

Identifiers

DOI

10.1515/joepi-2015-0015