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Journal of Pediatric Epilepsy 2018; 07(02): 052-062
DOI: 10.1055/s-0038-1668592
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Electroencephalography Findings in Autoimmune and Neuroinflammation-Related Epilepsies

Jeong-A Kim
1   Carman and Ann Adams Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center Wayne State University School of Medicine, Detroit, Michigan, United States
2   Carman and Ann Adams Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center Wayne State University School of Medicine, Detroit, Michigan, United States
,
Dara V.F. Albert
3   Department of Pediatrics, Nationwide Children's Hospital, The Ohio State University, Columbus, Ohio, United States
4   Division of Neurology, Nationwide Children's Hospital, The Ohio State University, Columbus, Ohio, United States
,
Amanda R.B. Weber
1   Carman and Ann Adams Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center Wayne State University School of Medicine, Detroit, Michigan, United States
2   Carman and Ann Adams Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center Wayne State University School of Medicine, Detroit, Michigan, United States
› Author Affiliations
Further Information

Publication History

02 June 2018

20 June 2018

Publication Date:
03 September 2018 (online)

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Abstract

Autoimmune epilepsy occurs in association with localized central nervous system or systemic immune-mediated inflammation. Traditional anticonvulsant medications are frequently ineffective, and alternative approaches including immunomodulatory agents may be required. Identification of patients with autoimmune epilepsy may be challenging due to the variability of presentation and normal or nonspecific diagnostic results. Electroencephalography (EEG) features tend to include patterns of encephalopathy, generalized or focal interictal epileptiform abnormalities, or status epilepticus. Occasionally, specific EEG features may lend insight into the diagnosis. In this review article, we discuss EEG features of several suspected or proven immune-mediated pediatric epilepsies, including Rasmussen's encephalitis, idiopathic hemiconvulsion-hemiplegia syndrome, febrile infection-related epilepsy syndrome, epilepsies associated with autoantibodies to neuronal surface or intracellular antigens, and other systemic autoimmune diseases.

Keywords

electroencephalography - autoimmune epilepsy - pediatrics
 

  • References

  • 1 Fisher RS, Cross JH, French JA. , et al. Operational classification of seizure types by the International League Against Epilepsy: Position Paper of the ILAE Commission for Classification and Terminology. Epilepsia 2017; 58 (04) 522-530
    CrossrefPubMedGoogle Scholar
  • 2 Ong MS, Kohane IS, Cai T, Gorman MP, Mandl KD. Population-level evidence for an autoimmune etiology of epilepsy. JAMA Neurol 2014; 71 (05) 569-574
    CrossrefPubMedGoogle Scholar
  • 3 Korff CM, Dale RC. The immune system in pediatric seizures and epilepsies. Pediatrics 2017; 140 (03) e20163534
    CrossrefPubMedGoogle Scholar
  • 4 Suleiman J, Brilot F, Lang B, Vincent A, Dale RC. Autoimmune epilepsy in children: case series and proposed guidelines for identification. Epilepsia 2013; 54 (06) 1036-1045
    CrossrefPubMedGoogle Scholar
  • 5 van Baalen A, Häusler M, Boor R. , et al. Febrile infection-related epilepsy syndrome (FIRES): a nonencephalitic encephalopathy in childhood. Epilepsia 2010; 51 (07) 1323-1328
    CrossrefPubMedGoogle Scholar
  • 6 Sakuma H, Awaya Y, Shiomi M. , et al. Acute encephalitis with refractory, repetitive partial seizures (AERRPS): a peculiar form of childhood encephalitis. Acta Neurol Scand 2010; 121 (04) 251-256
    CrossrefPubMedGoogle Scholar
  • 7 Mikaeloff Y, Jambaqué I, Hertz-Pannier L. , et al. Devastating epileptic encephalopathy in school-aged children (DESC): a pseudo encephalitis. Epilepsy Res 2006; 69 (01) 67-79
    CrossrefPubMedGoogle Scholar
  • 8 Wilder-Smith EP, Lim EC, Teoh HL. , et al. The NORSE (new-onset refractory status epilepticus) syndrome: defining a disease entity. Ann Acad Med Singapore 2005; 34 (07) 417-420
    PubMedGoogle Scholar
  • 9 Kramer U, Chi CS, Lin KL. , et al. Febrile infection-related epilepsy syndrome (FIRES): pathogenesis, treatment, and outcome: a multicenter study on 77 children. Epilepsia 2011; 52 (11) 1956-1965
    CrossrefPubMedGoogle Scholar
  • 10 Appenzeller S, Helbig I, Stephani U. , et al. Febrile infection-related epilepsy syndrome (FIRES) is not caused by SCN1A, POLG, PCDH19 mutations or rare copy number variations. Dev Med Child Neurol 2012; 54 (12) 1144-1148
    CrossrefPubMedGoogle Scholar
  • 11 Specchio N, Fusco L, Vigevano F. Acute-onset epilepsy triggered by fever mimicking FIRES (febrile infection-related epilepsy syndrome): the role of protocadherin 19 (PCDH19) gene mutation. Epilepsia 2011; 52 (11) e172-e175
    CrossrefPubMedGoogle Scholar
  • 12 Kramer U, Shorer Z, Ben-Zeev B, Lerman-Sagie T, Goldberg-Stern H, Lahat E. Severe refractory status epilepticus owing to presumed encephalitis. J Child Neurol 2005; 20 (03) 184-187
    CrossrefPubMedGoogle Scholar
  • 13 Okanishi T, Mori Y, Kibe T. , et al. Refractory epilepsy accompanying acute encephalitis with multifocal cortical lesions: possible autoimmune etiology. Brain Dev 2007; 29 (09) 590-594
    CrossrefPubMedGoogle Scholar
  • 14 Illingworth MA, Hanrahan D, Anderson CE. , et al. Elevated VGKC-complex antibodies in a boy with fever-induced refractory epileptic encephalopathy in school-age children (FIRES). Dev Med Child Neurol 2011; 53 (11) 1053-1057
    CrossrefPubMedGoogle Scholar
  • 15 Baxter P, Clarke A, Cross H. , et al. Idiopathic catastrophic epileptic encephalopathy presenting with acute onset intractable status. Seizure 2003; 12 (06) 379-387
    CrossrefPubMedGoogle Scholar
  • 16 Nabbout R, Mazzuca M, Hubert P. , et al. Efficacy of ketogenic diet in severe refractory status epilepticus initiating fever induced refractory epileptic encephalopathy in school age children (FIRES). Epilepsia 2010; 51 (10) 2033-2037
    CrossrefPubMedGoogle Scholar
  • 17 Specchio N, Fusco L, Claps D, Vigevano F. Epileptic encephalopathy in children possibly related to immune-mediated pathogenesis. Brain Dev 2010; 32 (01) 51-56
    CrossrefPubMedGoogle Scholar
  • 18 Bien CG, Widman G, Urbach H. , et al. The natural history of Rasmussen's encephalitis. Brain 2002; 125 (Pt 8): 1751-1759
    CrossrefPubMedGoogle Scholar
  • 19 Aguilar MJ, Rasmussen T. Role of encephalitis in pathogenesis of epilepsy. Arch Neurol 1960; 2: 663-676
    CrossrefPubMedGoogle Scholar
  • 20 Longaretti F, Dunkley C, Varadkar S, Vargha-Khadem F, Boyd SG, Cross JH. Evolution of the EEG in children with Rasmussen's syndrome. Epilepsia 2012; 53 (09) 1539-1545
    CrossrefPubMedGoogle Scholar
  • 21 Varadkar S, Bien CG, Kruse CA. , et al. Rasmussen's encephalitis: clinical features, pathobiology, and treatment advances. Lancet Neurol 2014; 13 (02) 195-205
    CrossrefPubMedGoogle Scholar
  • 22 Bien CG, Granata T, Antozzi C. , et al. Pathogenesis, diagnosis and treatment of Rasmussen encephalitis: a European consensus statement. Brain 2005; 128 (Pt 3): 454-471
    CrossrefPubMedGoogle Scholar
  • 23 Bauer J, Elger CE, Hans VH. , et al. Astrocytes are a specific immunological target in Rasmussen's encephalitis. Ann Neurol 2007; 62 (01) 67-80
    CrossrefPubMedGoogle Scholar
  • 24 Schafer DP, Lehrman EK, Kautzman AG. , et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012; 74 (04) 691-705
    CrossrefPubMedGoogle Scholar
  • 25 Rogers SW, Andrews PI, Gahring LC. , et al. Autoantibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science 1994; 265 (5172): 648-651
    CrossrefPubMedGoogle Scholar
  • 26 Hart YM, Cortez M, Andermann F. , et al. Medical treatment of Rasmussen's syndrome (chronic encephalitis and epilepsy): effect of high-dose steroids or immunoglobulins in 19 patients. Neurology 1994; 44 (06) 1030-1036
    CrossrefPubMedGoogle Scholar
  • 27 Granata T, Gobbi G, Spreafico R. , et al. Rasmussen's encephalitis: early characteristics allow diagnosis. Neurology 2003; 60 (03) 422-425
    CrossrefPubMedGoogle Scholar
  • 28 Bien CG, Gleissner U, Sassen R, Widman G, Urbach H, Elger CE. An open study of tacrolimus therapy in Rasmussen encephalitis. Neurology 2004; 62 (11) 2106-2109
    CrossrefPubMedGoogle Scholar
  • 29 Olson HE, Lechpammer M, Prabhu SP. , et al. Clinical application and evaluation of the Bien diagnostic criteria for Rasmussen encephalitis. Epilepsia 2013; 54 (10) 1753-1760
    CrossrefPubMedGoogle Scholar
  • 30 Auvin S, Bellavoine V, Merdariu D. , et al. Hemiconvulsion-hemiplegia-epilepsy syndrome: current understandings. Eur J Paediatr Neurol 2012; 16 (05) 413-421
    CrossrefPubMedGoogle Scholar
  • 31 Mirsattari SM, Wilde NJ, Pigott SE. Long-term cognitive outcome of hemiconvulsion-hemiplegia-epilepsy syndrome affecting the left cerebral hemisphere. Epilepsy Behav 2008; 13 (04) 678-680
    CrossrefPubMedGoogle Scholar
  • 32 Yamazaki S, Ikeno K, Abe T, Tohyama J, Adachi Y. Hemiconvulsion-hemiplegia-epilepsy syndrome associated with CACNA1A S218L mutation. Pediatr Neurol 2011; 45 (03) 193-196
    CrossrefPubMedGoogle Scholar
  • 33 Salih MA, Kabiraj M, Al-Jarallah AS, El Desouki M, Othman S, Palkar VA. Hemiconvulsion-hemiplegia-epilepsy syndrome. A clinical, electroencephalographic and neuroradiological study. Childs Nerv Syst 1997; 13 (05) 257-263
    CrossrefPubMedGoogle Scholar
  • 34 Nabbout R, Vezzani A, Dulac O, Chiron C. Acute encephalopathy with inflammation-mediated status epilepticus. Lancet Neurol 2011; 10 (01) 99-108
    CrossrefPubMedGoogle Scholar
  • 35 Franzoni E, Garone C, Marchiani V. , et al. A new case of idiopathic hemiplegia hemiconvulsion syndrome. Neurol Sci 2010; 31 (06) 799-805
    CrossrefPubMedGoogle Scholar
  • 36 Auvin S, Devisme L, Maurage CA. , et al. Neuropathological and MRI findings in an acute presentation of hemiconvulsion-hemiplegia: a report with pathophysiological implications. Seizure 2007; 16 (04) 371-376
    CrossrefPubMedGoogle Scholar
  • 37 Kimura M, Tasaka M, Sejima H, Takusa Y, Ichiyama T, Yamaguchi S. Hemiconvulsion-hemiplegia syndrome and elevated interleukin-6: case report. J Child Neurol 2002; 17 (09) 705-707
    CrossrefPubMedGoogle Scholar
  • 38 Dalmau J, Tüzün E, Wu HY. , et al. Paraneoplastic anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol 2007; 61 (01) 25-36
    CrossrefPubMedGoogle Scholar
  • 39 Granerod J, Cousens S, Davies NW, Crowcroft NS, Thomas SL. New estimates of incidence of encephalitis in England. Emerg Infect Dis 2013;19(9)
    PubMedGoogle Scholar
  • 40 Moscato EH, Peng X, Jain A, Parsons TD, Dalmau J, Balice-Gordon RJ. Acute mechanisms underlying antibody effects in anti-N-methyl-D-aspartate receptor encephalitis. Ann Neurol 2014; 76 (01) 108-119
    CrossrefPubMedGoogle Scholar
  • 41 Dalmau J, Gleichman AJ, Hughes EG. , et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol 2008; 7 (12) 1091-1098
    CrossrefPubMedGoogle Scholar
  • 42 Höftberger R, Armangue T, Leypoldt F, Graus F, Dalmau J. Clinical neuropathology practice guide 4-2013: post-herpes simplex encephalitis: N-methyl-D-aspartate receptor antibodies are part of the problem. Clin Neuropathol 2013; 32 (04) 251-254
    CrossrefPubMedGoogle Scholar
  • 43 Konuskan B, Yildirim M, Topaloglu H. , et al. Clinical presentation of anti-N-methyl-D-aspartate receptor and anti-voltage-gated potassium channel complex antibodies in children: a series of 24 cases. Eur J Paediatr Neurol 2018; 22 (01) 135-142
    CrossrefPubMedGoogle Scholar
  • 44 Zekeridou A, Karantoni E, Viaccoz A. , et al. Treatment and outcome of children and adolescents with N-methyl-D-aspartate receptor encephalitis. J Neurol 2015; 262 (08) 1859-1866
    CrossrefPubMedGoogle Scholar
  • 45 Creten C, van der Zwaan S, Blankespoor RJ. , et al. Late onset autism and anti-NMDA-receptor encephalitis. Lancet 2011; 378 (9785): 98
    CrossrefPubMedGoogle Scholar
  • 46 Matoq AA, Rappoport AS, Yang Y, O'Babatunde J, Bakerywala R, Sheth RD. Anti-NMDA-receptor antibody encephalitis in infants. Epilepsy Behav Case Rep 2015; 4: 99-101
    PubMedGoogle Scholar
  • 47 Florance NR, Davis RL, Lam C. , et al. Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents. Ann Neurol 2009; 66 (01) 11-18
    CrossrefPubMedGoogle Scholar
  • 48 Hacohen Y, Wright S, Gadian J. , et al. N-methyl-d-aspartate (NMDA) receptor antibodies encephalitis mimicking an autistic regression. Dev Med Child Neurol 2016; 58 (10) 1092-1094
    CrossrefPubMedGoogle Scholar
  • 49 Albert DV, Pluto CP, Weber A. , et al. Utility of neurodiagnostic studies in the diagnosis of autoimmune encephalitis in children. Pediatr Neurol 2016; 55: 37-45
    CrossrefPubMedGoogle Scholar
  • 50 Titulaer MJ, McCracken L, Gabilondo I. , et al. Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol 2013; 12 (02) 157-165
    CrossrefPubMedGoogle Scholar
  • 51 Nosadini M, Boniver C, Zuliani L. , et al. Longitudinal electroencephalographic (EEG) findings in pediatric anti-N-methyl-D-aspartate (anti-NMDA) receptor encephalitis: the Padua experience. J Child Neurol 2015; 30 (02) 238-245
    CrossrefPubMedGoogle Scholar
  • 52 Schmitt SE, Pargeon K, Frechette ES, Hirsch LJ, Dalmau J, Friedman D. Extreme delta brush: a unique EEG pattern in adults with anti-NMDA receptor encephalitis. Neurology 2012; 79 (11) 1094-1100
    CrossrefPubMedGoogle Scholar
  • 53 Mohammad SS, Dale RC. EEG background activity and extreme delta brush in children with anti-NMDAR encephalitis. Eur J Paediatr Neurol 2018; 22 (01) 207-208
    CrossrefPubMedGoogle Scholar
  • 54 Gitiaux C, Simonnet H, Eisermann M. , et al. Early electro-clinical features may contribute to diagnosis of the anti-NMDA receptor encephalitis in children. Clin Neurophysiol 2013; 124 (12) 2354-2361
    CrossrefPubMedGoogle Scholar
  • 55 Lai M, Huijbers MG, Lancaster E. , et al. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol 2010; 9 (08) 776-785
    CrossrefPubMedGoogle Scholar
  • 56 Irani SR, Alexander S, Waters P. , et al. Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan's syndrome and acquired neuromyotonia. Brain 2010; 133 (09) 2734-2748
    CrossrefPubMedGoogle Scholar
  • 57 Suleiman J, Dale RC. The recognition and treatment of autoimmune epilepsy in children. Dev Med Child Neurol 2015; 57 (05) 431-440
    CrossrefPubMedGoogle Scholar
  • 58 Suleiman J, Brenner T, Gill D. , et al. VGKC antibodies in pediatric encephalitis presenting with status epilepticus. Neurology 2011; 76 (14) 1252-1255
    CrossrefPubMedGoogle Scholar
  • 59 Kröll-Seger J, Bien CG, Huppertz HJ. Non-paraneoplastic limbic encephalitis associated with antibodies to potassium channels leading to bilateral hippocampal sclerosis in a pre-pubertal girl. Epileptic Disord 2009; 11 (01) 54-59
    PubMedGoogle Scholar
  • 60 Irani SR, Michell AW, Lang B. , et al. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann Neurol 2011; 69 (05) 892-900
    CrossrefPubMedGoogle Scholar
  • 61 Gaspard N. Autoimmune epilepsy. Continuum (Minneapolis, Minn) 2016; 22 (1 Epilepsy): 227-245
    PubMedGoogle Scholar
  • 62 Irani SR, Stagg CJ, Schott JM. , et al. Faciobrachial dystonic seizures: the influence of immunotherapy on seizure control and prevention of cognitive impairment in a broadening phenotype. Brain 2013; 136 (Pt 10): 3151-3162
    CrossrefPubMedGoogle Scholar
  • 63 Carvajal-González A, Leite MI, Waters P. , et al. Glycine receptor antibodies in PERM and related syndromes: characteristics, clinical features and outcomes. Brain 2014; 137 (Pt 8): 2178-2192
    CrossrefPubMedGoogle Scholar
  • 64 Barbagallo M, Vitaliti G, Pavone P, Romano C, Lubrano R, Falsaperla R. Pediatric autoimmune encephalitis. J Pediatr Neurosci 2017; 12 (02) 130-134
    CrossrefPubMedGoogle Scholar
  • 65 Dale RC, Merheb V, Pillai S. , et al. Antibodies to surface dopamine-2 receptor in autoimmune movement and psychiatric disorders. Brain 2012; 135 (Pt 11): 3453-3468
    CrossrefPubMedGoogle Scholar
  • 66 Spatola M, Dalmau J. Seizures and risk of epilepsy in autoimmune and other inflammatory encephalitis. Curr Opin Neurol 2017; 30 (03) 345-353
    CrossrefPubMedGoogle Scholar
  • 67 Tsai MH, Cheng MY, Fu TY, Chuang YC. Faciobrachial dystonic seizures associated with Hashimoto encephalopathy. Eur J Neurol 2015; 22 (07) e72-e74
    CrossrefPubMedGoogle Scholar
  • 68 Schäuble B, Castillo PR, Boeve BF, Westmoreland BF. EEG findings in steroid-responsive encephalopathy associated with autoimmune thyroiditis. Clin Neurophysiol 2003; 114 (01) 32-37
    CrossrefPubMedGoogle Scholar
  • 69 Yu HJ, Lee J, Seo DW, Lee M. Clinical manifestations and treatment response of steroid in pediatric Hashimoto encephalopathy. J Child Neurol 2014; 29 (07) 938-942
    CrossrefPubMedGoogle Scholar
  • 70 Patnaik SK, Upreti V, Dhull P. Steroid responsive encephalopathy associated with autoimmune thyroiditis (SREAT) in childhood. J Pediatr Endocrinol Metab 2014; 27 (7-8): 737-744
    PubMedGoogle Scholar
  • 71 Berger I, Castiel Y, Dor T. Paediatric Hashimoto encephalopathy, refractory epilepsy and immunoglobulin treatment - unusual case report and review of the literature. Acta Paediatr 2010; 99 (12) 1903-1905
    CrossrefPubMedGoogle Scholar
  • 72 Işıkay S, Kocamaz H, Sezer S. , et al. The frequency of epileptiform discharges in celiac disease. Pediatr Neurol 2015; 53 (01) 78-82
    CrossrefPubMedGoogle Scholar
  • 73 Arroyo HA, De Rosa S, Ruggieri V, de Dávila MT, Fejerman N. ; Argentinean Epilepsy and Celiac Disease Group. Epilepsy, occipital calcifications, and oligosymptomatic celiac disease in childhood. J Child Neurol 2002; 17 (11) 800-806
    CrossrefPubMedGoogle Scholar
  • 74 Dai AI, Akcali A, Varan C, Demiryürek AT. Prevalence of resistant occipital lobe epilepsy associated with celiac disease in children. Childs Nerv Syst 2014; 30 (06) 1091-1098
    CrossrefPubMedGoogle Scholar
  • 75 Vieira-Karuta SC, Silva IC, Liberalesso PB, Bandeira M, Janz Jr L, Löhr Jr A. Epileptic seizures and EEG features in juvenile systemic lupus erythematosus. Arq Neuropsiquiatr 2008; 66 (3A, 3a): 468-470
    CrossrefPubMedGoogle Scholar
  • 76 Glanz BI, Schur PH, Khoshbin S. EEG abnormalities in systemic lupus erythematosus. Clin Electroencephalogr 1998; 29 (03) 128-131 (electroencephalography)
    PubMedGoogle Scholar