Benign epileptiform discharges of childhood and associated conditions
https://doi.org/10.17650/2073-8803-2018-13-3-7-24
Abstract
This article provides a detailed description of benign epileptiform discharges of childhood (BEDC) as one of electroencephalography patterns in children. We emphasize that BEDC are not specific for both idiopathic (genetic) focal epilepsy and epilepsy in general. BEDC can be observed in a number of various disorders and also in neurologically healthy children. We developed a detailed classification of BEDC-associated states that are divided into 3 groups: neurologically healthy children, children with various forms of epilepsy, and patients with various neurological disorders without epilepsy. We found that there are 2 main factors responsible for BEDC in electroencephalogram: genetic predisposition and white matter lesions, usually occurring during the antenatal or perinatal period. BEDC should be considered rather a manifestation of congenital abnormalities in brain maturation than a marker of epilepsy. We also discuss the need for therapy in patients with BEDC-associated states.
About the Author
K. Yu. Mukhin
Svt. Luka’s Institute of Child Neurology and Epilepsy; Svt. Luka’s Institute of Child and Adult Neurology
Russian Federation
Russian Federation
5 Nagornaya St., Troitsk, Moscow 108841;
9 Akad. Anokhina St., 119579 Moscow
References
1. Alikhanov A.A., Mukhin K.Yu., Petrukhin A.S. et al. Rolandic epilepsy and cortical dysplasia: a pseudoform or a sporadic association? Zhurnal nevropatologii i psikhiatrii = Journal of Neuropathology and Psychiatry 2002;102(6):61–3. (In Russ.).
2. Belousova E.D. Risk factors, treatment strategy, and prognosis of convulsive syndrome and epilepsy in children with cerebral palsy. Summary of thesis … of doctor of medical sciences. Moscow, 2004. 43 p. (In Russ.).
3. Bobylova M.Yu., Mukhin K.Yu. Hereditary disorders and chromosomal abnormalities accompanied by epilepsy: general characteristics and brief semiology. In: Epileptic syndromes. Diagnosis and therapy. Moscow: “Binom”, 2018. (In Russ.).
4. Borovikov K.S. Focal childhood epilepsy with structural brain changes and benign epileptiform discharges on EEG (FECSBCBEDC). Summary of thesis … of candidate of medical sciences. Moscow, 2018. (In Russ.).
5. Gastaut A. Dictionary of epilepsy. Part I. Definitions. Geneva: WHO, 1975. P. 63. (In Russ.).
6. Glukhova L.Yu., Mukhin K.Yu. Autistic epileptiform regression and its treatment. In: Autism spectrum disorders: medical and psychological assistance. Lviv: Ms Publishing, 2014. Pp. 106–12. (In Russ.).
7. Zenkov L.R. Nonconvulsive epileptic encephalopathies with mental, communicative, and behavioral disorders. Vestnik epileptologii = Bulletin of Epileptology 2004;1(2): 7–11. (In Russ.).
8. Zenkov L.R. Non-paroxysmal epileptic disorders. Moscow: Medpress-Inform, 2007. 278 p. (In Russ.).
9. Karlov V.A. Epileptic encephalopathy. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2006;106(2):4–12. (In Russ.).
10. Karlov V.A. Pathophysiology of epilepsy. In: Epilepsy in children and adult men and women. Moscow: Meditsina, 2010. Pp. 37–71. (In Russ.).
11. Kryzhanovskiy G.N. Plasticity in disorders of the nervous system. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2001;101(2):4–7. (In Russ.).
12. Kuzmich G.V. Clinical and prognostic value of epileptiform activity on EEG in children with cerebral palsy in the absence of epilepsy. Summary of thesis … of candidate of medical sciences. Moscow, 2014. 25 p. (In Russ.).
13. Mironov M.B., Mukhin K.Yu., Petrukhin A.S. Transformation of Rolandic epilepsy into Jeavons syndrome (two case reports). Russkiy zhurnal detskoy nevrologii = Russian Journal of Child Neurology 2009;4(4):14–21. (In Russ.).
14. Mukhin K.Yu., Glukhova L.Yu., Petrukhin A.S. et al. Diagnostic criteria for atypical benign partial epilepsy of childhood. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2001;101(1):13–21. (In Russ.).
15. Mukhin K. Yu. Benign epileptiform discharges of childhood and their specificity. In: Epilepsy: atlas of electroclinical diagnosis. Мoscow: Alvares Pаblishing, 2004. Pp. 277–88. (In Russ.).
16. Mukhin K.Yu., Petrukhin A.S., Mironov M.B. et al. Epilepsy with electrical status epilepticus during slow-wave sleep: diagnostic criteria, differential diagnosis and approaches to therapy. Moscow, 2005. 32 p. (In Russ.).
17. Mukhin K.Yu., Golovteev A.L. Acquired epileptic frontal syndrome. Russkiy zhurnal detskoy nevrologii = Russian Journal of Child Neurology 2008;3(1):21–9. (In Russ.).
18. Mukhin K.Yu. Idiopathic focal epilepsy with pseudogeneralized seizures: a special form of epilepsy in children. Russkiy zhurnal detskoy nevrologii = Russian Journal of Child Neurology 2009;4(2):3–19. (In Russ.).
19. Mukhin K.Yu., Mironov M.B., Borovikov K.S., Petrukhin A.S. Focal childhood epilepsy with structural brain changes and benign epileptiform discharges on EEG (FECSBC-BEDC) (preliminary results). Russkiy zhurnal detskoy nevrologii = Russian Journal of Child Neurology 2010;5(1):3–17. (In Russ.).
20. Mukhin K.Yu. Cognitive epileptiform disintegration and similar syndromes. In: Epileptic encephalopathies and similar syndromes in children. Moscow: ArtServis Ltd, 2011. Pp. 390–424. (In Russ.).
21. Mukhin K.Yu., Kuzmich G.V., Balkanskaya S.V. et al. Characteristics of epileptiform activity on EEG in children with periventricular leukomalacia and cerebral palsy in the absence of epilepsy. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2012:7(2):71–6. (In Russ.).
22. [Nogovitsyn V.Yu., Nesterovskiy Yu.E., Osipova G.N. et al. Polymorphic electroencephalography patterns of benign epileptiform discharges of childhood. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2004;104(10):48–56, (In Russ.).
23. Petrukhin A.S. Development of the nervous system. In: Pediatric neurology. Moscow: Meditsina, 2004. Pp. 32–70. (In Russ.).
24. Tysyachina M.D., Mukhin K.Yu., Kakaulina V.S. et al. Epileptic seizures in patients with triple X syndrome. Russkiy zhurnal detskoy nevrologii = Russian Journal of Child Neurology 2009;4(4):38–47. (In Russ.).
25. Aarts J.H.P., Binnie C.D., Smit A.M., Wilkins A.J. Seleсtive cognitive impairment during foсal and generalized epileptiform EEG activity. Brain 1984;107: 293–308.
26. Ambrosetto G. Unilateral opercular macrogyria and benign childhood epilepsy with centrotemporal (rolandic) spikes: report of a case. Epilepsia 1992;33(3):499–503.
27. Anyanwu C., Ghavami F., Schuelein M., Motamedi G.K. Ethosuximide-induced conversion of typical childhood absence to Rolandic spikes. J Child Neurol 2013;28(1):111–4.
28. Arhan E., Serdaroglu A., Aydin K. et al. Epileptic encephalopathy with electrical status epilepticus: an electroclinical study of 59 patients. Seizure 2015;26:86–93.
29. Ben-Zeev B., Kivity S., Pshitizki Y. et al. Congenital hydrocephalus and continuous spike wave in slow sleep – a common association? J Child Neurol 2004;19(2): 129–34.
30. Berroya A.M., Bleasel A.F., Stevermuer T.L. et al. Spike morphology, location and frequency in benign epilepsy with centrotemporal spikes. J Child Neurol 2005;20(3):188–94.
31. Вrау F.P., Wiser W.C. Evidence for a genetic aetiology of temporal central abnormalities in focal epilepsy. N Engl J Med 1964;271:926–33.
32. Camfield C.S., Berg A., Stephani U., Wirrell E.C. Transition issues for benign epilepsy with centrotemporal spikes, nonlesional focal epilepsy in otherwise normal children, childhood absence epilepsy, and juvenile myoclonic epilepsy. Epilepsia 2014;55(Suppl 3):16–20.
33. Caraballo R.H., Cersosimo R., Fejerman N. Symptomatic focal epilepsies imitating atypical evolutions of idiopathic focal epilepsies in childhood. In: Benign focal epilepsies in infancy, childhood and adolescence. UK: J.L., 2007. Pp. 221–242.
34. Cavazzuti G.B., Cappella L., Nalin A. Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 1980;21:43–55.
35. Cerminara C., Coniglio A., El-Malhany N. et al. Two epileptic syndromes, one brain: childhood absence epilepsy and benign childhood epilepsy with centrotemporal spikes. Seizure 2012;21(1):70–4.
36. 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;28:24–7.
37. Degen R., Holthausen H., Pieper T. et al. Benign epileptic discharges in patients with lesional partial epilepsies. Pediatr Neurol 1999;20(5):354–9.
38. De Negri M. The maturational development of the child: developmental disorders and epilepsy. In: Continuous spikes and waves during slow sleep. Electrical status epilepticus during slow sleep. Acquired epileptic aphasia and related conditions. London: John Libbey, 1995. Pp. 3–8.
39. Deonna T., Roulet-Perez E. Cognitive and behavioural disorders of epileptic origin in children. London: Mac Keith Press, 2005. Pp. 81–114.
40. Doose H. Symptomatology in children with focal sharp waves of genetic origin. Eur J Pediatr 1989;149:210–5.
41. Doose H., Baier W.K. Benign partial epilepsy and related conditions: multifactorial pathogenesis with hereditary impairment of brain maturation. Eur J Pediatr 1989;149:152–8.
42. Doose H., Neubauer B.A., Carlsson G. Children with benign focal sharp waves in the EEG – developmental disorders and epilepsy. Neuropediatrics 1996;27(5): 227–41.
43. Doose H., Neubauer B.A., Petersen B. The concept of hereditary impairment of brain maturation. Epileptic Disord 2000;2(Suppl 1):45–9.
44. Doose H. EEG in childhood epilepsy. Hamburg: John Libbey, 2003. Pp. 191–243.
45. Duarte S., Duarte A., Monteiro J.P. et al. Epilepsy and epileptiform abnormalities in a population of children with autism spectrum disorders. Fifty years of Landau– Kleffner Syndrome, Alden Biesen, Belgium. November, 2–4, 2007.
46. Dulac O., Milh M., Holmes G.L. Brain maturation and epilepsy. Handb Clin Neurol 2013;111:441–6.
47. Eeg-Olofsson O., Lundberg S., Raininko R. MRI in rolandic epilepsy. Epileptic Disord 2000;2(Suppl 1):51–3.
48. Engel J. Seizures and Epilepsy. 2nd edn. Oxford: Oxford University Press, 2013. Pp. 3–32.
49. Fejerman N., Caraballo R.H. Benign focal epilepsies in infancy, childhood and adolescence. UK: J.L., 2007. 266 p.
50. Fejerman N. Benign childhood epilepsy with centrotemporal spikes. In: Atlas of Epilepsies. London: Springer, 2010. Pp. 957–964.
51. Fonseca L.C., Tedrus G.M., Bastos A. et al. Reactivity of rolandic spikes. Clin Electroencephalogr 1996;27(3):116–20.
52. Gastaut Y. Un element deroutant de la semiology electroencephalographique: les points prerolandique sans signification focale. Rev Neurol (Paris) 1952;87:488–90.
53. Gelisse P., Genton P., Bureau M. et al. Are there generalized spike waves and typical absences in benign rolandic epilepsy? Brain Dev 1999;21:390–6.
54. Gobbi G., Boni A., Filippini M. Rolandic epilepsy and related syndromes: a spectrum? Epilepsia 2002;43(Suppl 8):32.
55. Gregory D.L., Wong P.K. Topographical analysis of the centrotemporal discharges in benign rolandic epilepsy of childhood. Epilepsia 1984;25(6):705–11.
56. Guerrini R., Genton P., Bureau M. et al. Multilobar polymicrogiria, intractable drop attack seizures, and sleep-related electrical status epilepticus. Neurology 1998;51:504–12.
57. Guzzetta F., Battaglia D., Veredice Ch. et al. Early thalamic injury associated with epilepsy and continuous spike–wave during slow sleep. Epilepsia 2005;46(6):889–900.
58. Johnston M.V. Clinical disorders of brain plasticity. Brain Dev 2004;26(2):73–80.
59. Hadjipanayis A., Hadjichristoulou C., Youroukos S. Epilepsy in patients with cerebral palsy. Dev Med Child Neurol 1997;39:659–63.
60. Heida J.G., Chudomel O., Galanopoulou A.S. et al. Sex influence on the maturation of endogenous systems involved in seizure control. In: Biology of seizure susceptibility in developing brain. UK: John Libbey Eurotext, 2008. Pp. 129–44.
61. Heijbel J., Blom S., Rasmuson M. Benign epilepsy of childhood with centro-temporal EEG foci: a genetic study. Epilepsia 1975;16:285–93.
62. Holthausen H., Pieper T., Winkler P. et al. Electro-clinical-pathological correlations in focal cortical dysplasia (FCD) at young ages. Childs Nerv Syst 2014;30:2015–26.
63. Kagan-Kushnir T., Roberts S.W., Snead O.C. Screening electroencephalograms in autism spectrum disorders: evidence-based guideline. J Child Neurol 2005;20(3):240.
64. Kellaway P. The electroencephalographic features of benign centrotemporal (rolandic) epilepsy of childhood. Epilepsia 2000;41(8):1053–6.
65. Kim H.L., Donnelly J.H., Tournay A.E. et al. Absence of seizures despite high prevalence of epileptiform EEG abnormalities in children with autism monitored in a tertiary care center. Epilepsia 2006;47(2):394–8.
66. Kim H.J., Kim S.H., Kim H.D. et al. Genetic and epileptic features in Rett syndrome. Yonsei Med J 2012;53(3):495–500.
67. Kim S.E., Lee J.H., Chung H.K. et al. Alterations in white matter microstructures and cognitive dysfunctions in benign childhood epilepsy with centrotemporal spikes. Eur J Neurol 2014;21(5):708–17.
68. Kuzniecky R., Andermann F., Guerrini R. The congenital bilateral perisylvian syndrome. In: Dysplasias of cerebral cortex and epilepsy. 1996. Pp. 271–277.
69. Luders H.-O., Noachtar S. Atlas and classification of electroencephalography. 2000. 208 p.
70. Maher J., Ronen G.M., Ogunyemi A.O., Goulden K.J. Occipital paroxysmal discharges suppressed by eye opening: variability in clinical and seizure manifestations in childhood. Epilepsia 1995;36:52–7.
71. Mantovani J.F. Autistic regression and Landau-Kleffner syndrome: progress or confusion? Devel Med Child Neurol 2000;42:349–53.
72. Matsuoka H., Nakamura M., Ohno T. et al. The role of cognitive – motor function in precipitation and inhibition of epileptic seizures. Epilepsia 2005; 46(Suppl 1):17–20.
73. Mukhin K.Yu., Mironov M.B., Borovikov K.S. et al. Unexpected favorable prognosis in children with focal epilepsy due to perinatal brain damage. Epilepsia 2015;56(Suppl 1):173.
74. Nayrac P., Beaussart M. Pre-rolandic spike-waves: a very peculiar EEG reading; electroclinical study of 21 cases. Rev Neurol 1958;99:201–6.
75. Nass R., Gross A., Devinsky O. Autism and autistic epileptiform regression with occipital spikes. Devel Med Child Neurol 1998;40:453–8.
76. Neubauer B.A. The genetics of rolandic epilepsy. Epileptic Disord 2000;2(Suppl 1):67–8.
77. Panayiotopoulos C., Bureau M., Caraballo R. et al. In. Epileptic syndromes in infancy, childhood and adolescence. 5th edn. Paris: John Libbey Eurotext, 2012. Pp. 217–54.
78. Pavlidis E., Rubboli G., Nikanorova M. et al. Encephalopathy with status epilepticus during sleep (ESES) induced by oxcarbazepine in idiopathic focal epilepsy in childhood. Funct Neurol 2015;8:1–3.
79. Pressler R.M. Entwicklung Eines Computerisierten EEG Getriggerten Testsystems zur Erkennung Kognitiver Leistungsstörungen Während Subklinischen Epileptiformen Entladungen im Kindesalter. HumboltUniversität zu Berlin, 1997.
80. Sarnat H.B., Born D.E. Synaptophysin immunocytochemistry with thermal intensification: a marker of terminal axonal maturation in the human fetal nervous system. Brain Dev 1999;21:41–50.
81. Sarnat H.B., Flores-Sarnat L. Fetal synaptogenesis and epilepsy of early infancy. In: Biology of seizure susceptibility in developing brain. UK: John Libbey Eurotext, 2008. Pp. 185–204.
82. Stephani U., Doose H. Benign idiopathic partial epilepsy and brain lesion. Epilepsia 1999;40(3):373–6.
83. Strug L.J., Clarke T., Chiang Th. et al. Centrotemporal sharp wave EEG trait in rolandic epilepsy maps to Elongator Protein Complex 4 (ELP4). Eur J Hum Genet 2009;17:1171–81.
84. Talwar D., Rask C.A., Torres F. Clinical manifestations in children with occipital spike-wave paroxysms. Epilepsia 1992;33(4):667–74.
85. Tassinari C.A., Cantaluppo G., Dalla Bernardina B. еt al. Encephalopathy related to status epilepticus during slow sleep (ESES) including Landau–Kleffner syndrome. In: Epileptic syndromes in infancy, childhood and adolescence. 5th edn. Paris: John Libbey Eurotext, 2012. Pp. 255–75.
86. Tarta-Arsene O., Pieper T., Hartlieb T., et al. Overrepresentation of age related epileptiform discharges in children with hemispheric epilepsy syndromes. Epilepsia 2015;56(Suppl 1):249.
87. Tuchman R.F., Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics 1997;99:560–66.
88. Tuchman R. Autistic regression and epilepsy. Fifty years of Landau–Kleffner syndrome. Alden Biesen, Belgium. November, 2–4, 2007.
89. Veggiotti P., Bova S., Granocchio E. et al. Acquired epileptic frontal syndrome as long-term outcome in two children with CSWS. Neurophysiol Clin 2001;31:387–97.
90. Wanigasinghe J., Reid S.M., Mackay M. et al. Epilepsy in hemiplegic cerebral palsy due to perinatal arterial ischaemic stroke. Dev Med Child Neurol 2010;52(11):1021–7.
91. Wolff M., Reckert T., Niemann G. Congenital hemiplegia: correlations between lesion patterns and childhood epilepsies. Epilepsia 1998;39(Suppl 2):92.
Review
For citations:
Mukhin K.Yu. Benign epileptiform discharges of childhood and associated conditions. Russian Journal of Child Neurology. 2018;13(3):7-24. (In Russ.) https://doi.org/10.17650/2073-8803-2018-13-3-7-24
Views:
17236
Email this article 