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Journal of Pediatric Epilepsy 2016; 05(03): 133-138
DOI: 10.1055/s-0036-1585066
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Physiopathology of Atypical Evolutions of Idiopathic Focal Epilepsies in Childhood

Patrick Van Bogaert
1   Laboratoire de Cartographie Fonctionnelle du Cerveau, ULB Neuroscience Institute, Université libre de Bruxelles, Brussels, Belgium
2   Department of Pediatric Neurology, Hôpital Erasme, Université libre de Bruxelles, Brussels, Belgium
› Author Affiliations
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Publication History

Publication Date:
01 July 2016 (online)

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Abstract

This article aims to discuss if the underlying etiology is an important determinant of atypical evolution of idiopathic focal epilepsy (IFE) in childhood and if there might be biomarkers that would predict atypical evolution. It appears that the determinants of atypical evolution remain largely unknown but that both genetic and epigenetic factors are likely to be involved. The analysis of scalp electroencephalography remains the best biomarker of atypical evolution. However, functional neuroimaging methods of investigation are helpful to better understand how epileptic activity affects brain functioning at rest and during goal-directed tasks and to delineate the extent of brain networks that are impaired by epileptic activity. Moreover, neuroimaging bring new arguments favoring the idea that typical and atypical IFE should not be viewed as distinct entities but as a unique syndrome with various degrees of severity that should be treated using tailored strategies and robust biomarkers of efficacy.

Keywords

epilepsy - focal - genetics - childhood - physiopathology - functional neuroimaging
 

  • References

  • 1 Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989; 30 (4) 389-399
    CrossrefPubMedGoogle Scholar
  • 2 Engel Jr J. Report of the ILAE classification core group. Epilepsia 2006; 47 (9) 1558-1568
    CrossrefPubMedGoogle Scholar
  • 3 Berg AT, Berkovic SF, Brodie MJ , 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 (4) 676-685
    CrossrefPubMedGoogle Scholar
  • 4 Ferrie C, Caraballo R, Covanis A , et al. Panayiotopoulos syndrome: a consensus view. Dev Med Child Neurol 2006; 48 (3) 236-240
    CrossrefPubMedGoogle Scholar
  • 5 Aicardi J, Chevrie JJ. Atypical benign partial epilepsy of childhood. Dev Med Child Neurol 1982; 24 (3) 281-292
    PubMedGoogle Scholar
  • 6 Hahn A, Pistohl J, Neubauer BA, Stephani U. Atypical “benign” partial epilepsy or pseudo-Lennox syndrome. Part I: symptomatology and long-term prognosis. Neuropediatrics 2001; 32 (1) 1-8
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Fejerman N. Atypical rolandic epilepsy. Epilepsia 2009; 50 (Suppl. 07) 9-12
    PubMedGoogle Scholar
  • 8 Fujii A, Oguni H, Hirano Y, Osawa M. Atypical benign partial epilepsy: recognition can prevent pseudocatastrophe. Pediatr Neurol 2010; 43 (6) 411-419
    CrossrefPubMedGoogle Scholar
  • 9 Van Bogaert P. Epileptic encephalopathy with continuous spike-waves during slow-wave sleep including Landau-Kleffner syndrome. Handb Clin Neurol 2013; 111: 635-640
    PubMedGoogle Scholar
  • 10 Fernández IS, Peters JM, Hadjiloizou S , et al. Clinical staging and electroencephalographic evolution of continuous spikes and waves during sleep. Epilepsia 2012; 53 (7) 1185-1195
    CrossrefPubMedGoogle Scholar
  • 11 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
  • 12 Eriksson K, Kylliäinen A, Hirvonen K, Nieminen P, Koivikko M. Visual agnosia in a child with non-lesional occipito-temporal CSWS. Brain Dev 2003; 25 (4) 262-267
    CrossrefPubMedGoogle Scholar
  • 13 Ferrie CD, Koutroumanidis M, Rowlinson S, Sanders S, Panayiotopoulos CP. Atypical evolution of Panayiotopoulos syndrome: a case report. Epileptic Disord 2002; 4 (1) 35-42
    PubMedGoogle Scholar
  • 14 Caraballo RH, Astorino F, Cersósimo R, Soprano AM, Fejerman N. Atypical evolution in childhood epilepsy with occipital paroxysms (Panayiotopoulos type). Epileptic Disord 2001; 3 (3) 157-162
    PubMedGoogle Scholar
  • 15 Tovia E, Goldberg-Stern H, Ben Zeev B , et al. The prevalence of atypical presentations and comorbidities of benign childhood epilepsy with centrotemporal spikes. Epilepsia 2011; 52 (8) 1483-1488
    CrossrefPubMedGoogle Scholar
  • 16 De Tiège X, Goldman S, Verheulpen D, Aeby A, Poznanski N, Van Bogaert P. Coexistence of idiopathic rolandic epilepsy and CSWS in two families. Epilepsia 2006; 47 (10) 1723-1727
    CrossrefPubMedGoogle Scholar
  • 17 Stephani U, Carlsson G. The spectrum from BCECTS to LKS: the rolandic EEG trait-impact on cognition. Epilepsia 2006; 47 (Suppl. 02) 67-70
    CrossrefPubMedGoogle Scholar
  • 18 Tassinari CA, Cantalupo G, Rios-Pohl L, Giustina ED, Rubboli G. Encephalopathy with status epilepticus during slow sleep: “the Penelope syndrome.”. Epilepsia 2009; 50 (Suppl. 07) 4-8
    PubMedGoogle Scholar
  • 19 Vears DF, Tsai MH, Sadleir LG , et al. Clinical genetic studies in benign childhood epilepsy with centrotemporal spikes. Epilepsia 2012; 53 (2) 319-324
    CrossrefPubMedGoogle Scholar
  • 20 Lemke JR, Lal D, Reinthaler EM , et al. Mutations in GRIN2A cause idiopathic focal epilepsy with rolandic spikes. Nat Genet 2013; 45 (9) 1067-1072
    CrossrefPubMedGoogle Scholar
  • 21 Lal D, Reinthaler EM, Schubert J , et al. DEPDC5 mutations in genetic focal epilepsies of childhood. Ann Neurol 2014; 75 (5) 788-792
    CrossrefPubMedGoogle Scholar
  • 22 Carvill GL, Regan BM, Yendle SC , et al. GRIN2A mutations cause epilepsy-aphasia spectrum disorders. Nat Genet 2013; 45 (9) 1073-1076
    CrossrefPubMedGoogle Scholar
  • 23 Lesca G, Rudolf G, Bruneau N , et al. GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction. Nat Genet 2013; 45 (9) 1061-1066
    CrossrefPubMedGoogle Scholar
  • 24 Lal D, Reinthaler EM, Altmüller J , et al. RBFOX1 and RBFOX3 mutations in rolandic epilepsy. PLoS ONE 2013; 8 (9) e73323
    CrossrefPubMedGoogle Scholar
  • 25 Turner SJ, Mayes AK, Verhoeven A, Mandelstam SA, Morgan AT, Scheffer IE. GRIN2A: an aptly named gene for speech dysfunction. Neurology 2015; 84 (6) 586-593
    CrossrefPubMedGoogle Scholar
  • 26 Marescaux C, Hirsch E, Finck S , et al. Landau-Kleffner syndrome: a pharmacologic study of five cases. Epilepsia 1990; 31 (6) 768-777
    CrossrefPubMedGoogle Scholar
  • 27 Guerrini R, Belmonte A, Genton P. Antiepileptic drug-induced worsening of seizures in children. Epilepsia 1998; 39 (Suppl. 03) S2-S10
    PubMedGoogle Scholar
  • 28 Catania S, Cross H, de Sousa C, Boyd S. Paradoxic reaction to lamotrigine in a child with benign focal epilepsy of childhood with centrotemporal spikes. Epilepsia 1999; 40 (11) 1657-1660
    CrossrefPubMedGoogle Scholar
  • 29 Cerminara C, Montanaro ML, Curatolo P, Seri S. Lamotrigine-induced seizure aggravation and negative myoclonus in idiopathic rolandic epilepsy. Neurology 2004; 63 (2) 373-375
    CrossrefPubMedGoogle Scholar
  • 30 Montenegro MA, Guerreiro MM. Electrical status epilepticus of sleep in association with topiramate. Epilepsia 2002; 43 (11) 1436-1440
    PubMedGoogle Scholar
  • 31 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 (4) 524-533
    CrossrefPubMedGoogle Scholar
  • 32 Rakhade SN, Jensen FE. Epileptogenesis in the immature brain: emerging mechanisms. Nat Rev Neurol 2009; 5 (7) 380-391
    CrossrefPubMedGoogle Scholar
  • 33 Sánchez Fernández I, Loddenkemper T, Peters JM, Kothare SV. Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatr Neurol 2012; 47 (6) 390-410
    CrossrefPubMedGoogle Scholar
  • 34 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
  • 35 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
  • 36 Scholtes FB, Hendriks MP, Renier WO. Cognitive deterioration and electrical status epilepticus during slow sleep. Epilepsy Behav 2005; 6 (2) 167-173
    CrossrefPubMedGoogle Scholar
  • 37 Veggiotti P, Termine C, Granocchio E, Bova S, Papalia G, Lanzi G. Long-term neuropsychological follow-up and nosological considerations in five patients with continuous spikes and waves during slow sleep. Epileptic Disord 2002; 4 (4) 243-249
    PubMedGoogle Scholar
  • 38 Paquier PF, Van Dongen HR, Loonen CB. The Landau-Kleffner syndrome or ‘acquired aphasia with convulsive disorder’. Long-term follow-up of six children and a review of the recent literature. Arch Neurol 1992; 49 (4) 354-359
    CrossrefPubMedGoogle Scholar
  • 39 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 (6) 1517-1524
    CrossrefPubMedGoogle Scholar
  • 40 Seegmüller C, Deonna T, Dubois CM , et al. Long-term outcome after cognitive and behavioral regression in nonlesional epilepsy with continuous spike-waves during slow-wave sleep. Epilepsia 2012; 53 (6) 1067-1076
    CrossrefPubMedGoogle Scholar
  • 41 Robinson RO, Baird G, Robinson G, Simonoff E. Landau-Kleffner syndrome: course and correlates with outcome. Dev Med Child Neurol 2001; 43 (4) 243-247
    CrossrefPubMedGoogle Scholar
  • 42 Massa R, de Saint-Martin A, Carcangiu R , et al. EEG criteria predictive of complicated evolution in idiopathic rolandic epilepsy. Neurology 2001; 57 (6) 1071-1079
    CrossrefPubMedGoogle Scholar
  • 43 Maquet P, Hirsch E, Metz-Lutz MN , 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 (Pt 6): 1497-1520
    CrossrefPubMedGoogle Scholar
  • 44 Gaillard WD, Weinstein S, Conry J , et al. Prognosis of children with partial epilepsy: MRI and serial 18FDG-PET. Neurology 2007; 68 (9) 655-659
    CrossrefPubMedGoogle Scholar
  • 45 Tepmongkol S, Srikijvilaikul T, Vasavid P. Factors affecting bilateral temporal lobe hypometabolism on 18F-FDG PET brain scan in unilateral medial temporal lobe epilepsy. Epilepsy Behav 2013; 29 (2) 386-389
    CrossrefPubMedGoogle Scholar
  • 46 Van Bogaert P, Wikler D, Damhaut P, Szliwowski HB, Goldman S. Cerebral glucose metabolism and centrotemporal spikes. Epilepsy Res 1998; 29 (2) 123-127
    CrossrefPubMedGoogle Scholar
  • 47 De Tiège X, Goldman S, Laureys S , et al. Regional cerebral glucose metabolism in epilepsies with continuous spikes and waves during sleep. Neurology 2004; 63 (5) 853-857
    CrossrefPubMedGoogle Scholar
  • 48 Witte OW, Bruehl C. Distant functional and metabolic disturbances in focal epilepsy. Adv Neurol 1999; 81: 383-388
    PubMedGoogle Scholar
  • 49 De Tiège X, Ligot N, Goldman S, Poznanski N, de Saint Martin A, Van Bogaert P. Metabolic evidence for remote inhibition in epilepsies with continuous spike-waves during sleep. Neuroimage 2008; 40 (2) 802-810
    CrossrefPubMedGoogle Scholar
  • 50 De Tiège X, Trotta N, Op de Beeck M , et al. Neurophysiological activity underlying altered brain metabolism in epileptic encephalopathies with CSWS. Epilepsy Res 2013; 105 (3) 316-325
    CrossrefPubMedGoogle Scholar
  • 51 Archambaud F, Bouilleret V, Hertz-Pannier L , et al. Optimizing statistical parametric mapping analysis of 18F-FDG PET in children. EJNMMI Res 2013; 3 (1) 2
    CrossrefPubMedGoogle Scholar
  • 52 Ligot N, Archambaud F, Trotta N , et al. Default mode network hypometabolism in epileptic encephalopathies with CSWS. Epilepsy Res 2014; 108 (5) 861-871
    CrossrefPubMedGoogle Scholar
  • 53 Iadecola C, Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 2007; 10 (11) 1369-1376
    CrossrefPubMedGoogle Scholar
  • 54 De Tiège X, Goldman S, Van Bogaert P. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain 2011; 134 (Pt 5): e177
    CrossrefPubMedGoogle Scholar
  • 55 Archer JS, Briellman RS, Abbott DF, Syngeniotis A, Wellard RM, Jackson GD. Benign epilepsy with centro-temporal spikes: spike triggered fMRI shows somato-sensory cortex activity. Epilepsia 2003; 44 (2) 200-204
    CrossrefPubMedGoogle Scholar
  • 56 Boor S, Vucurevic G, Pfleiderer C, Stoeter P, Kutschke G, Boor R. EEG-related functional MRI in benign childhood epilepsy with centrotemporal spikes. Epilepsia 2003; 44 (5) 688-692
    CrossrefPubMedGoogle Scholar
  • 57 Lengler U, Kafadar I, Neubauer BA, Krakow K. fMRI correlates of interictal epileptic activity in patients with idiopathic benign focal epilepsy of childhood. A simultaneous EEG-functional MRI study. Epilepsy Res 2007; 75 (1) 29-38
    CrossrefPubMedGoogle Scholar
  • 58 Masterton RA, Harvey AS, Archer JS , et al. Focal epileptiform spikes do not show a canonical BOLD response in patients with benign rolandic epilepsy (BECTS). Neuroimage 2010; 51 (1) 252-260
    CrossrefPubMedGoogle Scholar
  • 59 De Tiège X, Harrison S, Laufs H , et al. Impact of interictal epileptic activity on normal brain function in epileptic encephalopathy: an electroencephalography-functional magnetic resonance imaging study. Epilepsy Behav 2007; 11 (3) 460-465
    CrossrefPubMedGoogle Scholar
  • 60 Moeller F, Moehring J, Ick I , et al. EEG-fMRI in atypical benign partial epilepsy. Epilepsia 2013; 54 (8) e103-e108
    CrossrefPubMedGoogle Scholar
  • 61 Siniatchkin M, Groening K, Moehring J , et al. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain 2010; 133 (9) 2798-2813
    CrossrefPubMedGoogle Scholar
  • 62 Gusnard DA, Raichle ME, Raichle ME. Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2001; 2 (10) 685-694
    CrossrefPubMedGoogle Scholar
  • 63 Anticevic A, Cole MW, Murray JD, Corlett PR, Wang XJ, Krystal JH. The role of default network deactivation in cognition and disease. Trends Cogn Sci 2012; 16 (12) 584-592
    CrossrefPubMedGoogle Scholar
  • 64 Raichle ME. The brain's default mode network. Annu Rev Neurosci 2015; 38: 433-447
    CrossrefPubMedGoogle Scholar
  • 65 Oser N, Hubacher M, Specht K, Datta AN, Weber P, Penner IK. Default mode network alterations during language task performance in children with benign epilepsy with centrotemporal spikes (BECTS). Epilepsy Behav 2014; 33: 12-17
    CrossrefPubMedGoogle Scholar
  • 66 Adebimpe A, Aarabi A, Bourel-Ponchel E, Mahmoudzadeh M, Wallois F. EEG resting state analysis of cortical sources in patients with benign epilepsy with centrotemporal spikes. Neuroimage Clin 2015; 9: 275-282
    CrossrefPubMedGoogle Scholar
  • 67 Adebimpe A, Aarabi A, Bourel-Ponchel E, Mahmoudzadeh M, Wallois F. Functional brain dysfunction in patients with benign childhood epilepsy as revealed by graph theory. PLoS ONE 2015; 10 (10) e0139228
    CrossrefPubMedGoogle Scholar
  • 68 Verrotti A, Filippini M, Matricardi S, Agostinelli MF, Gobbi G. Memory impairment and benign epilepsy with centrotemporal spike (BECTS): a growing suspicion. Brain Cogn 2014; 84 (1) 123-131
    CrossrefPubMedGoogle Scholar
  • 69 Deonna T, Zesiger P, Davidoff V, Maeder M, Mayor C, Roulet E. Benign partial epilepsy of childhood: a longitudinal neuropsychological and EEG study of cognitive function. Dev Med Child Neurol 2000; 42 (9) 595-603
    CrossrefPubMedGoogle Scholar
  • 70 Baglietto MG, Battaglia FM, Nobili L , et al. Neuropsychological disorders related to interictal epileptic discharges during sleep in benign epilepsy of childhood with centrotemporal or rolandic spikes. Dev Med Child Neurol 2001; 43 (6) 407-412
    CrossrefPubMedGoogle Scholar
  • 71 Urbain C, Galer S, Van Bogaert P, Peigneux P. Pathophysiology of sleep-dependent memory consolidation processes in children. Int J Psychophysiol 2013; 89 (2) 273-283
    CrossrefPubMedGoogle Scholar
  • 72 Wilhelm I, Prehn-Kristensen A, Born J. Sleep-dependent memory consolidation—what can be learnt from children?. Neurosci Biobehav Rev 2012; 36 (7) 1718-1728
    CrossrefPubMedGoogle Scholar
  • 73 Bölsterli Heinzle BK, Fattinger S, Kurth S , et al. Spike wave location and density disturb sleep slow waves in patients with CSWS (continuous spike waves during sleep). Epilepsia 2014; 55 (4) 584-591
    CrossrefPubMedGoogle Scholar
  • 74 Urbain C, Di Vincenzo T, Peigneux P, Van Bogaert P. Is sleep-related consolidation impaired in focal idiopathic epilepsies of childhood? A pilot study. Epilepsy Behav 2011; 22 (2) 380-384
    CrossrefPubMedGoogle Scholar
  • 75 Galer S, Urbain C, De Tiège X , et al. Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood. Epilepsy Behav 2015; 43: 16-23
    CrossrefPubMedGoogle Scholar