Treating Immune-Related Epilepsy

Epilepsy (CW Bazil, Section Editor)
  • 60 Downloads
Part of the following topical collections:
  1. Topical Collection on Epilepsy

Abstract

Purpose of Review

This review explores different treatment modalities for immune-mediated epilepsy, including epilepsy caused by autoantibodies as well as epilepsy in the context of systemic autoimmune disease.

Recent Findings

Autoimmune epilepsy is an increasingly recognized entity. Conventional treatments for epilepsy, such as antiseizure medications and epilepsy surgery, are less successful in treating epilepsy caused by autoimmune disease. Immunomodulatory therapies such as corticosteroids, intravenous immunoglobulin, and plasma exchange are generally more successful in treating immune-mediated epilepsy than conventional epilepsy therapies.

Summary

Autoimmune epilepsy should be considered as a possible etiology for patients with frequent seizures of unknown etiology. The response to immunotherapies is often promising, particularly in patients with antibodies to neuronal cell surface antigens.

Keywords

Autoimmune epilepsy Encephalitis Treatment Immunotherapy 

Notes

Compliance with Ethical Standards

Conflict of Interest

Sonal Bhatia declares no conflict of interest.

Sarah E. Schmitt has received personal fees from SAGE Therapeutics.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Falco-Walter JJ, Scheffer IE, Fisher RS. The new definition and classification of seizures and epilepsy. Epilepsy Res. 2017;139:73–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Brenner T, Sills GJ, Hart Y, Howell S, Waters P, Brodie MJ, et al. Prevalence of neurologic autoantibodies in cohorts of patients with new and established epilepsy. Epilepsia. 2013;54(6):1028–35.  https://doi.org/10.1111/epi.12127.CrossRefPubMedGoogle Scholar
  3. 3.
    •• Dubey D, Algallaf A, Hayes R, Freeman M, Chen K, Ding K, et al. Neurologic autoantibody prevalence in epilepsy of unknown etiology. JAMA Neurol. 2017;74(4):397–402. This study indicates that autoantibodies may be detected in up to 35% of patients with epilepsy of unknown etiology; furthermore, it identifies clinical characteristics that predict the presence of autoantibodies.  https://doi.org/10.1001/jamaneurol.2016.5429.CrossRefPubMedGoogle Scholar
  4. 4.
    •• Quek AM, Britton JW, McKeon A, So E, Lennon VA, Shin C, et al. Autoimmune epilepsy: clinical characteristics and response to immunotherapy. Arch Neurol. 2012;69(5):582–93. This study demonstrated that the majority of patients with known or suspected autoimmune epilepsy will demonstrated a response to immunotherapy within a median time of four months.  https://doi.org/10.1001/archneurol.2011.2985.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Vincent A, Buckley C, Schott JM, Baker I, Dewar BK, Detert N, et al. Potassium channel antibody-associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain. 2004;127(3):701–12.  https://doi.org/10.1093/brain/awh077.CrossRefPubMedGoogle Scholar
  6. 6.
    Lai M, Huijbers MG, Lancaster E, Graus F, Bataller L, Balice-Gordon R, et al. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol. 2010;9(8):776–85.  https://doi.org/10.1016/S1474-4422(10)70137-X.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Schmitt SE, Pargeon K, Frechette ES, Hirsch LJ, Dalmau J, Friedman D, et al. Extreme delta brush: a unique EEG pattern in adults with anti-NMDA receptor encephalitis. Neurology. 2012;79(11):1094–100.  https://doi.org/10.1212/WNL.0b013e3182698cd8.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Zuliani L, Graus F, Giometto B, Bien C, Vincent A. Central nervous system neuronal surface antibody associated syndromes: review and guidelines for recognition. J Neurol Neurosurg Psychiatry. 2012;83(6):638–45.  https://doi.org/10.1136/jnnp-2011-301237.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Graus F, Titulaer MJ, Balu R, Benseler S, Bien CG, Cellucci T, et al. A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol. 2016;4:391–404.CrossRefGoogle Scholar
  10. 10.
    Dahm L, Ott C, Steiner J, Stepniak B, Teegen B, Saschenbrecker S, et al. Seroprevalence of autoantibodies against brain antigens in health and disease. Ann Neurol. 2014;76(1):82–94.  https://doi.org/10.1002/ana.24189.CrossRefPubMedGoogle Scholar
  11. 11.
    Leypoldt F, Armangue T, Dalmau J. Autoimmune encephalopathies. Ann N Y Acad Sci. 2015;1338(1):94–114.  https://doi.org/10.1111/nyas.12553.CrossRefPubMedGoogle Scholar
  12. 12.
    Gresa-Arribas N, Titulaer MJ, Torrents A, Aguilar E, McCracken L, Leypoldt F, et al. Antibody titres at diagnosis and during follow-up of anti-NMDA receptor encephalitis: a retrospective study. Lancet Neurol. 2014;2:167–77.CrossRefGoogle Scholar
  13. 13.
    McCracken L, Zhang J, Greene M, Crivaro A, Gonzalez J, Kamoun M, et al. Improving the antibody-based evaluation of autoimmune encephalitis. Neurol Neuroimmunol Neuroinflamm. 2017;4(6):e404.  https://doi.org/10.1212/NXI.0000000000000404.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Gultekin SH, Rosenfeld MR, Voltz R, Eichen J, Posner JB, Dalmau J. Paraneoplastic limbic encephalitis: neurological symptoms, immunological findings and tumour association in 50 patients. Brain. 2000;123(7):1481–94.  https://doi.org/10.1093/brain/123.7.1481.CrossRefPubMedGoogle Scholar
  15. 15.
    Irani SR, Michell AW, Lang B, Pettingill P, Waters P, Johnson MR, et al. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann Neurol. 2011;69(5):892–900.  https://doi.org/10.1002/ana.22307.CrossRefPubMedGoogle Scholar
  16. 16.
    Lai M, Hughes EG, Peng X, Zhou L, Gleichman AJ, Shu H, et al. AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann Neurol. 2009;65(4):424–34.  https://doi.org/10.1002/ana.21589.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Höftberger R, Titulaer MJ, Sabater L, Dome B, Rózsás A, Hegedus B, et al. Encephalitis and GABAB receptor antibodies: novel findings in a new case series of 20 patients. Neurology. 2013;81(17):1500–6.  https://doi.org/10.1212/WNL.0b013e3182a9585f.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Titulaer MJ, Soffietti R, Dalmau J, Gilhus NE, Giometto B, Graus F, et al. Screening for tumors in paraneoplastic syndromes: report of an EFNS task force. Eur J Neurol. 2011;18(1):19–e3.  https://doi.org/10.1111/j.1468-1331.2010.03220.x.CrossRefPubMedGoogle Scholar
  19. 19.
    Suleiman J, Brilot F, Lang B, Vincent A, Dale RC. Autoimmune epilepsy in children: case series and proposed guidelines for identification. Epilepsia. 2013;6:1036–45.CrossRefGoogle Scholar
  20. 20.
    •• Feyissa AM, Lόpez Chiriboga AS, Britton JW. Antiepileptic drug therapy in patients with autoimmune epilepsy. Neurol Neuroimmunol Neuroinflamm. 2017;4(4):e353. This study demonstrates the poor response most patients with autoimmune epilepsy have to traditional antiseizure medications, particularly in comparison with immunotherapy.  https://doi.org/10.1212/NXI.0000000000000353.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Malter MP, Frisch C, Zeitler H, Surges R, Urbach H, Helmstaedter C, et al. Treatment of immune-mediated temporal lobe epilepsy with GAD antibodies. Seizure. 2015;30:57–63.  https://doi.org/10.1016/j.seizure.2015.05.017.CrossRefPubMedGoogle Scholar
  22. 22.
    Irani SR, Stagg CJ, Schott JM, Rosenthal CR, Schneider SA, Pettingill P, 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):3151–62.  https://doi.org/10.1093/brain/awt212.CrossRefPubMedGoogle Scholar
  23. 23.
    Beghi E, Shorvon S. Antiepileptic drugs and the immune system. Epilepsia. 2011;52:40–4.  https://doi.org/10.1111/j.1528-1167.2011.03035.x.CrossRefPubMedGoogle Scholar
  24. 24.
    Bianchi M, Rossoni G, Sacerdote P, Panerai AE, Berti F. Carbamazepine exerts anti-inflammatory effects in the rat. Eur J Pharmacol. 1995;294(1):71–4.  https://doi.org/10.1016/0014-2999(95)00516-1.CrossRefPubMedGoogle Scholar
  25. 25.
    Himmerich H, Bartsch S, Hamer H, Mergl R, Schönherr J, Petersein C, et al. Modulation of cytokine production by drugs with antiepileptic or mood stabilizer properties in anti-CD3- and anti-Cd40-stimulated blood in vitro. Oxidative Med Cell Longev. 2014;2014:8061–2.CrossRefGoogle Scholar
  26. 26.
    Almeida V, Pimentel J, Campos A, Bentes C, Maruta C, Morgado C, et al. Surgical control of limbic encephalitis associated with LGI1 antibodies. Epileptic Disord. 2012;14:345–8.PubMedGoogle Scholar
  27. 27.
    •• Carreño M, Bien CG, Asadi-Pooya AA, Sperling M, Marusic P, Elisak M, et al. Epilepsy surgery in drug resistant temporal lobe epilepsy associated with neuronal antibodies. Epilepsy Res. 2017;129:101–5. This study demonstrates that patients with neuronal antibody have a low likelihood of an Engel class I outcome following epilepsy surgery.  https://doi.org/10.1016/j.eplepsyres.2016.12.010.CrossRefPubMedGoogle Scholar
  28. 28.
    Muehlebner A, Groeppel G, Pahs G, Hainfellner JA, Prayer D, Czech T, et al. Beneficial effect of epilepsy surgery in a case of childhood non-paraneoplastic limbic encephalitis. Epilepsy Res. 2010;90(3):295–9.  https://doi.org/10.1016/j.eplepsyres.2010.05.009.CrossRefPubMedGoogle Scholar
  29. 29.
    Mathon B, Bédos Ulvin L, Adam C, Adam C, Baulac M, Dupont S, et al. Surgical treatment for mesial temporal lobe epilepsy associated with hippocampal sclerosis. Rev Neurol (Paris). 2015;171(3):315–25.  https://doi.org/10.1016/j.neurol.2015.01.561.CrossRefGoogle Scholar
  30. 30.
    Sakuma H, Awaya Y, Shiomi M, Yamanouchi H, Takahashi Y, Saito Y, et al. Acute encephalitis with refractory, repetitive partial seizures (AERRPS): a peculiar form of childhood encephalitis. Acta Neurol Scand. 2010;121(4):251–6.  https://doi.org/10.1111/j.1600-0404.2009.01198.x.CrossRefPubMedGoogle Scholar
  31. 31.
    Gaspard N, Foreman BP, Alvarez V, Cabrera Kang C, Probasco JC, Jongeling AC, et al. New-onset refractory status epilepticus: etiology, clinical features, and outcome. Neurology. 2015;85(18):1604–13.  https://doi.org/10.1212/WNL.0000000000001940.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kramer U, Chi CS, Lin KL, Specchio N, Sahin M, Olson H, et al. Febrile infection-related epilepsy syndrome (FIRES): pathogenesis, treatment, and outcome: a multicenter study on 77 children. Epilepsia. 2011;52(11):1956–65.  https://doi.org/10.1111/j.1528-1167.2011.03250.x.CrossRefPubMedGoogle Scholar
  33. 33.
    Thakur KT, Probasco JC, Hocker SE, Roehl K, Henry B, Kossoff EH, et al. Ketogenic diet for adults in super-refractory status epilepticus. Neurology. 2014;8:665–70.CrossRefGoogle Scholar
  34. 34.
    Petit-Pedrol M, Armangue T, Peng X, Bataller L, Cellucci T, Davis R, et al. Encephalitis with refractory seizures, status epilepticus, and antibodies to the GABAA receptor: a case series, characterization of the antigen, and analysis of the effects of antibodies. Lancet Neurol. 2014;13(3):276–86.  https://doi.org/10.1016/S1474-4422(13)70299-0.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Appavu B, Vanatta L, Condie J, Kerrigan JF, Jarrar R, et al. Ketogenic diet treatment for pediatric super-refractory status epilepticus. Seizure. 2016;41:62–5.  https://doi.org/10.1016/j.seizure.2016.07.006.CrossRefPubMedGoogle Scholar
  36. 36.
    Dalmau J, Lancaster E, Martinez-Hernandez E, Rosenfeld MR, Balice-Gordon R. Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. 2011;10:Lancet Neurol, 63–74.Google Scholar
  37. 37.
    •• Toledano M, Britton JW, McKeon A, Shin C, Lennon VA, Quek AM, et al. Utility of an immunotherapy trial in evaluating patients with presumed autoimmune epilepsy. Neurology. 2014;82(18):1578–86. This study demonstrated that immunotherapy with methylprednisolone or IVIG produces a high rate of seizure reduction/seizure freedom in patients with suspected autoimmunity, even in the absence of an identified autoantibody.  https://doi.org/10.1212/WNL.0000000000000383.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    American College of Rheumatology Ad Hoc Committee on glucocorticoid-induced osteoporosis. Arthritis Rheum. 2001; 44(7):1496–503.Google Scholar
  39. 39.
    Gabriel SE, Jaakkimainen L, Bombardier C. Risk for serious gastrointestinal complications related to use of nonsteroidal anti-inflammatory drugs. A meta-analysis Ann Intern Med. 1991;115(10):787–96.  https://doi.org/10.7326/0003-4819-115-10-787.CrossRefPubMedGoogle Scholar
  40. 40.
    Stern A, Green H, Paul M, Vidal L, Leibovici L. Prophylaxis for Pneumocystis pneumonia (PCP) in non-HIV immunocompromised patients. Cochrane Database Syst Rev. 2014:(10):CD005590.Google Scholar
  41. 41.
    Suleiman J, Dale RC. The recognition and treatment of autoimmune epilepsy in children. Dev Med Child Neurol. 2015;57(5):431–40.  https://doi.org/10.1111/dmcn.12647.CrossRefPubMedGoogle Scholar
  42. 42.
    Irani SR, Gelfand JM, Bettcher BM, Singhal NS, Geshwind MD. Effect of rituximab in patients with leucine-rich, glioma-inactivated 1 antibody-associated encephalopathy. JAMA Neurol. 2014;71(7):896–900.  https://doi.org/10.1001/jamaneurol.2014.463.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Wong SH, Saunders MD, Larner AJ, Das K, Hart IK. An effective immunotherapy regimen for VGKC antibody-positive limbic encephalitis. J Neurol Neurosurg Psychiatry. 2010;81(10):1167–9.  https://doi.org/10.1136/jnnp.2009.178293.CrossRefPubMedGoogle Scholar
  44. 44.
    Toledano M, Pittock SJ. Autoimmune epilepsy. Semin Neurol. 2015;35(03):245–58.  https://doi.org/10.1055/s-0035-1552625.CrossRefPubMedGoogle Scholar
  45. 45.
    Dogan Onugoren M, Deuretzbacher D, Haensch CA, Hagedorn HJ, Halve S, Isenmann S, et al. Limbic encephalitis due to GABAB and AMPA receptor antibodies: a case series. J Neurol Neurosurg Psychiatry. 2015;86(9):965–72.  https://doi.org/10.1136/jnnp-2014-308814.CrossRefPubMedGoogle Scholar
  46. 46.
    Carvajal-González A, Leite MI, Waters P, Woodhall M, Coutinho E, Balint B, et al. Glycine receptor antibodies in PERM and related syndromes: characteristics, clinical features and outcomes. Brain. 2014;137(Pt 8):2178–92.  https://doi.org/10.1093/brain/awu142.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Guan HZ, Ren HT, Yang XZ, Lu Q, Peng B, Zhu YC, et al. Limbic encephalitis associated with anti-γ-aminobutyric acid B receptor antibodies: a case series from China. Chin Med J. 2015;128(22):3023–8.  https://doi.org/10.4103/0366-6999.168989.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Cui J, Bu H, He J, Zhao Z, Han W, Gao R, et al. The gamma-aminobutyric acid-B receptor (GABAB) encephalitis: clinical manifestations and response to immunotherapy. Int J Neurosci. 2017;6:1–7.CrossRefGoogle Scholar
  49. 49.
    Dalmau J, Gleichman AJ, Hughes EG, Rossi JE, Peng X, Lai M, et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol. 2008;7(12):1091–8.  https://doi.org/10.1016/S1474-4422(08)70224-2.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Dalmau J, Graus F, Rosenblum MK, Posner JB. Anti-Hu-associated paraneoplastic encephalomyelitis/sensory neuronopathy. A clinical study of 71 patients. Medicine (Baltimore). 1992;71(2):59–72.  https://doi.org/10.1097/00005792-199203000-00001.CrossRefGoogle Scholar
  51. 51.
    Murinson CC, Guarnaccia JB. Stiff-person syndrome with amphiphysin antibodies: distinctive features of a rare disease. Neurology. 2008: Dec 9;71(24):1955–8.  https://doi.org/10.1212/01.wnl.0000327342.58936.e0.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sillevis Smitt P, Grefkens J, de Leeuw B, van den Bent M, van Putten W, Hooijkaas H, et al. Survival and outcome in 73 anti-Hu positive patients with paraneoplastic encephalomyelitis/sensory neuronopathy. J Neurol. 2002;249(6):745–53.  https://doi.org/10.1007/s00415-002-0706-4.CrossRefPubMedGoogle Scholar
  53. 53.
    Meinck HM, Faber L, Morgenthaler N, Seissler J, Maile S, Butler M, et al. Antibodies against glutamic acid decarboxylase: prevalence in neurological diseases. J Neurol Neurosurg Psychiatry. 2001;71(1):100–3.  https://doi.org/10.1136/jnnp.71.1.100.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Gagnon MM, Savard M. Limbic encephalitis associated with GAD65 antibodies: brief review of the relevant literature. Can J Neurol Sci. 2016;43(4):486–93.  https://doi.org/10.1017/cjn.2016.13.CrossRefPubMedGoogle Scholar
  55. 55.
    Douglas CA, Ellershaw J. Anti-Hu antibodies may indicate a positive response to chemotherapy in paraneoplastic syndrome secondary to small cell lung cancer. Palliat Med. 2013;17:638–9.CrossRefGoogle Scholar
  56. 56.
    Orange D, Frank M, Tian S, Dousmanis A, Marmur R, Buckley N, et al. Cellular immune suppression in paraneoplastic neurologic syndromes targeting intracellular antigens. Arch Neurol. 2012;69(9):1132–40.  https://doi.org/10.1001/archneurol.2012.595.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Bertsias GK, Ionnidis JP, Aringer M, Bollen E, Bombardieri S, Bruce IN, et al. EULAR recommendations for the management of systemic lupus erythematosus with neuropsychiatric manifestations: report of a task force of the EULAR standing committee for clinical affairs. Ann Rheum Dis. 2010;69(12):2074–82.  https://doi.org/10.1136/ard.2010.130476.CrossRefPubMedGoogle Scholar
  58. 58.
    Atwater BD, Ai Z, Wolff MR. Fulminant myopericarditis from phenytoin-induced systemic lupus erythematosus. WMJ. 2008;107(6):298–300.PubMedGoogle Scholar
  59. 59.
    Barile-Fabris L, Ariza-Andraca R, Olguín-Ortega L, Jara LJ, Fraga-Mouret A, Miranda-Limón JM, et al. Controlled trial of IV cyclophosphamide versus IV methylprednidolone in severe neurological manifestations in systemic lupus erythematosus. Ann Rheum Dis. 2005;64(4):620–5.  https://doi.org/10.1136/ard.2004.025528.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Vasconcellos E, Pina-Garza JE, Fakhoury T, Fenichel GM. Pediatric manifestations of Hashimoto’s encephalopathy. Pediatr Neurol. 1999;20(5):394–8.  https://doi.org/10.1016/S0887-8994(99)00006-5.CrossRefPubMedGoogle Scholar
  61. 61.
    Olmez I, Moses H, Sriram S, Kirshner H, Lagrange AH, Pawate S. Diagnostic and therapeutic aspects of Hashimoto’s encephalopathy. J Neurol Sci. 2013;331(1-2):67–71.  https://doi.org/10.1016/j.jns.2013.05.009.CrossRefPubMedGoogle Scholar
  62. 62.
    Chong JY, Rowland LP, Utiger RD. Hashimoto encephalopathy: syndrome or myth? Arch Neurol. 2003;60(2):164–71.  https://doi.org/10.1001/archneur.60.2.164.CrossRefPubMedGoogle Scholar
  63. 63.
    Stern BJ, Krumholz A, Johns C, Scott P, Nissim J. Sarcoidosis and its neurological manifestations. Arch Neurol. 1985;42(9):909–17.  https://doi.org/10.1001/archneur.1985.04060080095022.CrossRefPubMedGoogle Scholar
  64. 64.
    Baumann RJ, Robertson WC Jr. Neurosarcoid presents differently in children than in adults. Pediatrics. 2003;112(6):e480–6.  https://doi.org/10.1542/peds.112.6.e480.CrossRefPubMedGoogle Scholar
  65. 65.
    Malmgren K, Lycke J, Engman E, Hedström A, Jönsson L, Rydenhag B, et al. Successful epilepsy surgery in a patient with neurosarcoidosis. Epilepsia. 2010;51(6):1101–3.  https://doi.org/10.1111/j.1528-1167.2010.02580.x.CrossRefPubMedGoogle Scholar
  66. 66.
    Lorentzen AO, Sveberg L, Midtvedt O, Kerty E, Heuser K. Overnight response to infliximab in neurosarcoidosis: a case report and review of infliximab treatment practice. Clin Neuropharmacol. 2014;37(5):142–8.  https://doi.org/10.1097/WNF.0000000000000047.CrossRefPubMedGoogle Scholar
  67. 67.
    Marnane M, Lynch T, Scott J, Stack J, Kelly PJ. Steroid-unresponsive neurosarcoidosis successfully treated with adalimumab. J Neurol. 2009;256(1):139–40.CrossRefPubMedGoogle Scholar
  68. 68.
    Alaedini A, Okamoto H, Briani C, Wollenberg K, Shill HA, Bushara KO, et al. Immune cross-reactivity in celiac disease: anti-gliadin antibodies bind to neuronal synapsin I. J Immunol. 2007;178(10):6590–5.  https://doi.org/10.4049/jimmunol.178.10.6590.CrossRefPubMedGoogle Scholar
  69. 69.
    Chapman RW, Laidlow JM, Colin-Jone D, Eade OE, Smith CL. Increased prevalence of epilepsy in celiac disease. BMJ. 1978;22:250–1.CrossRefGoogle Scholar
  70. 70.
    Hadijvassiliou M, Grünewald RA, Davies-Jones GA. Gluten sensitivity as a neurological illness. J Neurol Neurosurg Psychiatry. 2002;72(5):560–3.  https://doi.org/10.1136/jnnp.72.5.560.CrossRefGoogle Scholar
  71. 71.
    Ventura A, Bouquet F, Sartorelli C, Barbi E, Torre G, Tommasini G, et al. Coeliac disease, folic acid deficiency and epilepsy with cerebral calcifications. Acta Pediatr Scand. 1991;80(5):559–62.  https://doi.org/10.1111/j.1651-2227.1991.tb11906.x.CrossRefGoogle Scholar
  72. 72.
    Bye AM, Andermann F, Robitaille Y, Oliver M, Bohane T, Andermann E. Cortical vascular abnormalities in the syndrome of celiac disease, epilepsy, bilateral occipital calcifications and folate deficiency. Ann Neurol. 1993;34(3):399–403.  https://doi.org/10.1002/ana.410340316.CrossRefPubMedGoogle Scholar
  73. 73.
    Bashiri H, Afshari D, Babaei N, Ghadami MR. Celiac disease and epilepsy: the effect of gluten-free diet on seizure control. Adv Clin Exp Med. 2016;25(4):751–4.  https://doi.org/10.17219/acem/43585.CrossRefPubMedGoogle Scholar
  74. 74.
    Krumholz A, Stern BJ, Stern EG. Clinical implications of seizures in neurosarcoidosis. Arch Neurol. 1991;48(8):842–4.  https://doi.org/10.1001/archneur.1991.00530200084023.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of NeurologyMedical University of South CarolinaCharlestonUSA
  2. 2.Medical University of South CarolinaCharlestonUSA

Personalised recommendations