Advertisement

Autoimmune Encephalitis

  • Agnes van Sonderen
  • Maarten J. TitulaerEmail author
Chapter

Abstract

This chapter gives an overview of the syndromes associated with antibodies directed to membrane-bound or synaptic proteins. In contrast to the classical syndromes, disease occurs in younger patients as well; patients are also seen by non-neurologists like psychiatrists and pediatricians, and patients tend to have a more favorable response to immunotherapy. The focus in this chapter is on the clinical characteristics which distinguishes these disorders and on the relevance of cerebrospinal fluid (CSF) analysis. Comparison of sensitivity and specificity for serum and CSF is extensively discussed. N-methyl-D-aspartate receptor (NMDAR) encephalitis is relatively common and discussed first. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) encephalitis and encephalitis associated with antibodies to the metabotropic glutamate receptors mGluR1 and mGluR5 are rare and will be reviewed briefly. Subsequently, syndromes associated with antibodies to the glycine receptor, VGKC complex, and dipeptidyl-peptidase-like protein-6 (DPP6) are described. Encephalitis with antibodies directed to the γ-aminobutyric acid (GABA) receptor type B and type A are reviewed last.

Keywords

Encephalitis Antibodies NMDA receptor VGKC GABA receptor AMPA receptor Glycine receptor 

References

  1. Alexopoulos H, Akrivou S, Dalakas MC (2013) Glycine receptor antibodies in stiff-person syndrome and other GAD-positive CNS disorders. Neurology 81(22):1962–1964PubMedCrossRefGoogle Scholar
  2. Anderson NE, Rosenblum MK, Posner JB (1988) Paraneoplastic cerebellar degeneration: clinical-immunological correlations. Ann Neurol 24(4):559–567PubMedCrossRefGoogle Scholar
  3. Andrade DM, Tai P, Dalmau J, Wennberg R (2011) Tonic seizures: a diagnostic clue of anti-LGI1 encephalitis? Neurology 76(15):1355–1357PubMedCentralPubMedCrossRefGoogle Scholar
  4. Armangue T, Titulaer MJ, Malaga I, Bataller L, Gabilondo I, Graus F et al (2012) Pediatric anti-N-methyl-D-aspartate receptor encephalitis-clinical analysis and novel findings in a series of 20 patients. J Pediatr 162:850–856.e2PubMedCentralPubMedCrossRefGoogle Scholar
  5. Armangue T, Leypoldt F, Malaga I, Raspall-Chaure M, Marti I, Nichter C et al (2013) Herpes simplex virus encephalitis is a trigger of brain autoimmunity. Ann Neurol 75(2):317–323CrossRefGoogle Scholar
  6. Babbitt CJ, Levine GK, Lake J (2014) Use of dexmedetomidine as adjunctive therapy for anti-NMDA receptor encephalitis. J Pediatr Intensive Care (in press)Google Scholar
  7. Balint B, Jarius S, Nagel S, Haberkorn U, Probst C, Blocker IM et al (2014) Progressive encephalomyelitis with rigidity and myoclonus: a new variant with DPPX antibodies. Neurology 82(17):1521–1528PubMedCrossRefGoogle Scholar
  8. Barber PA, Anderson NE, Vincent A (2000) Morvan’s syndrome associated with voltage-gated K + channel antibodies. Neurology 54(3):771–772PubMedCrossRefGoogle Scholar
  9. Boronat A, Sabater L, Saiz A, Dalmau J, Graus F (2011) GABA(B) receptor antibodies in limbic encephalitis and anti-GAD-associated neurologic disorders. Neurology 76(9):795–800PubMedCentralPubMedCrossRefGoogle Scholar
  10. Boronat A, Gelfand JM, Gresa-Arribas N, Jeong HY, Walsh M, Roberts K et al (2013) Encephalitis and antibodies to dipeptidyl-peptidase-like protein-6, a subunit of Kv4.2 potassium channels. Ann Neurol 73(1):120–128PubMedCentralPubMedCrossRefGoogle Scholar
  11. Bourke D, Roxburgh R, Vincent A, Cleland J, Jeffery O, Dugan N et al (2013) Hypoventilation in glycine-receptor antibody related progressive encephalomyelitis, rigidity and myoclonus. J Clin Neurosci 21(5):876–878PubMedCrossRefGoogle Scholar
  12. Brenner T, Sills GJ, Hart Y, Howell S, Waters P, Brodie MJ et al (2013) Prevalence of neurologic autoantibodies in cohorts of patients with new and established epilepsy. Epilepsia 54(6):1028–1035PubMedCrossRefGoogle Scholar
  13. Buckley C, Oger J, Clover L, Tuzun E, Carpenter K, Jackson M et al (2001) Potassium channel antibodies in two patients with reversible limbic encephalitis. Ann Neurol 50(1):73–78PubMedCrossRefGoogle Scholar
  14. Butler CR, Miller TD, Kaur MS, Baker IW, Boothroyd GD, Illman NA et al (2014) Persistent anterograde amnesia following limbic encephalitis associated with antibodies to the voltage-gated potassium channel complex. J Neurol Neurosurg Psychiatry 85(4):387–391PubMedCrossRefGoogle Scholar
  15. Carr I (1982) The Ophelia syndrome: memory loss in Hodgkin’s disease. Lancet 1(8276):844–845PubMedCrossRefGoogle Scholar
  16. Clardy SL, Lennon VA, Dalmau J, Pittock SJ, Jones HR Jr, Renaud DL et al (2013) Childhood onset of stiff-man syndrome. JAMA Neurol 70(12):1531–1536PubMedGoogle Scholar
  17. Corsellis JA, Goldberg GJ, Norton AR (1968) “Limbic encephalitis” and its association with carcinoma. Brain 91(3):481–496PubMedCrossRefGoogle Scholar
  18. Dalmau J, Tuzun E, Wu HY, Masjuan J, Rossi JE, Voloschin A et al (2007) Paraneoplastic anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol 61(1):25–36PubMedCentralPubMedCrossRefGoogle Scholar
  19. Dalmau J, Gleichman AJ, Hughes EG, Rossi JE, Peng X, Lai M et al (2008) Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol 7(12):1091–1098PubMedCentralPubMedCrossRefGoogle Scholar
  20. Dalmau J, Lancaster E, Martinez-Hernandez E, Rosenfeld MR, Balice-Gordon R (2011) Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurol 10(1):63–74PubMedCentralPubMedCrossRefGoogle Scholar
  21. Damasio J, Leite MI, Coutinho E, Waters P, Woodhall M, Santos MA et al (2013) Progressive encephalomyelitis with rigidity and myoclonus: the first pediatric case with glycine receptor antibodies. JAMA Neurol 70(4):498–501PubMedCrossRefGoogle Scholar
  22. De Blauwe SN, Santens P, Vanopdenbosch LJ (2013) Anti-glycine receptor antibody mediated progressive encephalomyelitis with rigidity and myoclonus associated with breast cancer. Case Rep Neurol Med 2013, 589154PubMedCentralPubMedGoogle Scholar
  23. Derksen A, Stettner M, Stocker W, Seitz RJ (2013) Antiglycine receptor-related stiff limb syndrome in a patient with chronic lymphocytic leukaemia. BMJ Case Rep 2013 [Epub ahead of print] doi:  10.1136/bcr-2013-008667
  24. Dhamija R, Renaud DL, Pittock SJ, McKeon A, Lachance DH, Nickels KC et al (2011) Neuronal voltage-gated potassium channel complex autoimmunity in children. Pediatr Neurol 44(4):275–281PubMedCrossRefGoogle Scholar
  25. Ekizoglu E, Tuzun E, Woodhall M, Lang B, Jacobson L, Icoz S et al (2014) Investigation of neuronal autoantibodies in two different focal epilepsy syndromes. Epilepsia 55(3):414–422PubMedCrossRefGoogle Scholar
  26. Finke C, Kopp UA, Pruss H, Dalmau J, Wandinger KP, Ploner CJ (2012) Cognitive deficits following anti-NMDA receptor encephalitis. J Neurol Neurosurg Psychiatry 83(2):195–198PubMedCentralPubMedCrossRefGoogle Scholar
  27. Florance NR, Davis RL, Lam C, Szperka C, Zhou L, Ahmad S et al (2009) Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents. Ann Neurol 66(1):11–18PubMedCentralPubMedCrossRefGoogle Scholar
  28. Frisch C, Malter MP, Elger CE, Helmstaedter C (2013) Neuropsychological course of voltage-gated potassium channel and glutamic acid decarboxylase antibody related limbic encephalitis. Eur J Neurol 20(9):1297–1304PubMedCrossRefGoogle Scholar
  29. Fukata Y, Lovero KL, Iwanaga T, Watanabe A, Yokoi N, Tabuchi K et al (2010) Disruption of LGI1-linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc Natl Acad Sci U S A 107(8):3799–3804PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gabilondo I, Saiz A, Galan L, Gonzalez V, Jadraque R, Sabater L et al (2011) Analysis of relapses in anti-NMDAR encephalitis. Neurology 77(10):996–999PubMedCrossRefGoogle Scholar
  31. Geis C, Weishaupt A, Hallermann S, Grunewald B, Wessig C, Wultsch T et al (2010) Stiff person syndrome-associated autoantibodies to amphiphysin mediate reduced GABAergic inhibition. Brain 133(11):3166–3180PubMedCrossRefGoogle Scholar
  32. Gleichman AJ, Spruce LA, Dalmau J, Seeholzer SH, Lynch DR (2012) Anti-NMDA receptor encephalitis antibody binding is dependent on amino acid identity of a small region within the GluN1 amino terminal domain. J Neurosci 32(32):11082–11094PubMedCentralPubMedCrossRefGoogle Scholar
  33. Granerod J, Ambrose HE, Davies NW, Clewley JP, Walsh AL, Morgan D et al (2010) Causes of encephalitis and differences in their clinical presentations in England: a multicentre, population-based prospective study. Lancet Infect Dis 10(12):835–844PubMedCrossRefGoogle Scholar
  34. Granger AJ, Gray JA, Lu W, Nicoll RA (2011) Genetic analysis of neuronal ionotropic glutamate receptor subunits. J Physiol 589(Pt 17):4095–4101PubMedCentralPubMedCrossRefGoogle Scholar
  35. Graus F, Boronat A, Xifro X, Boix M, Svigelj V, Garcia A et al (2010) The expanding clinical profile of anti-AMPA receptor encephalitis. Neurology 74(10):857–859PubMedCrossRefGoogle Scholar
  36. Gresa-Arribas N, Titulaer MJ, Torrents A, Aguilar E, McCracken L, Leypoldt F et al (2013) Antibody titres at diagnosis and during follow-up of anti-NMDA receptor encephalitis: a retrospective study. Lancet Neurol 13:167–177PubMedCentralPubMedCrossRefGoogle Scholar
  37. Hacohen Y, Deiva K, Pettingill P, Waters P, Siddiqui A, Chretien P et al (2014) N-methyl-D-aspartate receptor antibodies in post-herpes simplex virus encephalitis neurological relapse. Mov Disord 29(1):90–96PubMedCrossRefGoogle Scholar
  38. Hoftberger R, Titulaer MJ, Sabater L, Dome B, Rozsas A, Hegedus B et al (2013) Encephalitis and GABAB receptor antibodies: novel findings in a new case series of 20 patients. Neurology 81(17):1500–1506PubMedCentralPubMedCrossRefGoogle Scholar
  39. Hughes EG, Peng X, Gleichman AJ, Lai M, Zhou L, Tsou R et al (2010) Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 30(17):5866–5875PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hutchinson M, Waters P, McHugh J, Gorman G, O’Riordan S, Connolly S et al (2008) Progressive encephalomyelitis, rigidity, and myoclonus: a novel glycine receptor antibody. Neurology 71(16):1291–1292PubMedCrossRefGoogle Scholar
  41. Iizuka T, Leite MI, Lang B, Waters P, Urano Y, Miyakawa S et al (2012) Glycine receptor antibodies are detected in progressive encephalomyelitis with rigidity and myoclonus (PERM) but not in saccadic oscillations. J Neurol 259(8):1566–1573PubMedCrossRefGoogle Scholar
  42. Iorio R, Damato V, Mirabella M, Vita MG, Hulsenboom E, Plantone D et al (2013) Cerebellar degeneration associated with mGluR1 autoantibodies as a paraneoplastic manifestation of prostate adenocarcinoma. J Neuroimmunol 263(1–2):155–158PubMedCrossRefGoogle Scholar
  43. Irani SR, Bera K, Waters P, Zuliani L, Maxwell S, Zandi MS et al (2010a) N-methyl-D-aspartate antibody encephalitis: temporal progression of clinical and paraclinical observations in a predominantly non-paraneoplastic disorder of both sexes. Brain 133(Pt 6):1655–1667PubMedCentralPubMedCrossRefGoogle Scholar
  44. Irani SR, Alexander S, Waters P, Kleopa KA, Pettingill P, Zuliani L et al (2010b) 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 133(9):2734–2748PubMedCentralPubMedCrossRefGoogle Scholar
  45. Irani SR, Michell AW, Lang B, Pettingill P, Waters P, Johnson MR et al (2011) Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann Neurol 69(5):892–900PubMedCrossRefGoogle Scholar
  46. Jarius S, Steinmeyer F, Knobel A, Streitberger K, Hotter B, Horn S et al (2013) GABAB receptor antibodies in paraneoplastic cerebellar ataxia. J Neuroimmunol 256(1–2):94–96PubMedCrossRefGoogle Scholar
  47. Jeffery OJ, Lennon VA, Pittock SJ, Gregory JK, Britton JW, McKeon A (2013) GABAB receptor autoantibody frequency in service serologic evaluation. Neurology 81(10):882–887PubMedCentralPubMedCrossRefGoogle Scholar
  48. Kayser MS, Titulaer MJ, Gresa-Arribas N, Dalmau J (2013) Frequency and characteristics of isolated psychiatric episodes in anti-NMDA receptor encephalitis. JAMA Neurol 70(9):1133–1139, Ref Type: Journal (Full)PubMedCrossRefGoogle Scholar
  49. Kleopa KA, Elman LB, Lang B, Vincent A, Scherer SS (2006) Neuromyotonia and limbic encephalitis sera target mature Shaker-type K + channels: subunit specificity correlates with clinical manifestations. Brain 129(Pt 6):1570–1584PubMedCrossRefGoogle Scholar
  50. Kyskan R, Chapman K, Mattman A, Sin D (2013) Antiglycine receptor antibody and encephalomyelitis with rigidity and myoclonus (PERM) related to small cell lung cancer. BMJ Case Rep 2013 [Epub ahead of print] doi:  10.1136/bcr-2013-010027
  51. Lai M, Hughes EG, Peng X, Zhou L, Gleichman AJ, Shu H et al (2009) AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann Neurol 65(4):424–434PubMedCentralPubMedCrossRefGoogle Scholar
  52. Lai M, Huijbers MG, Lancaster E, Graus F, Bataller L, Balice-Gordon R et al (2010) Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol 9(8):776–785PubMedCentralPubMedCrossRefGoogle Scholar
  53. Lancaster E, Lai M, Peng X, Hughes E, Constantinescu R, Raizer J et al (2010) Antibodies to the GABA(B) receptor in limbic encephalitis with seizures: case series and characterisation of the antigen. Lancet Neurol 9(1):67–76PubMedCentralPubMedCrossRefGoogle Scholar
  54. Lancaster E, Martinez-Hernandez E, Titulaer MJ, Boulos M, Weaver S, Antoine JC et al (2011a) Antibodies to metabotropic glutamate receptor 5 in the Ophelia syndrome. Neurology 77(18):1698–1701PubMedCentralPubMedCrossRefGoogle Scholar
  55. Lancaster E, Huijbers MG, Bar V, Boronat A, Wong A, Martinez-Hernandez E et al (2011b) Investigations of caspr2, an autoantigen of encephalitis and neuromyotonia. Ann Neurol 69(2):303–311PubMedCentralPubMedCrossRefGoogle Scholar
  56. Leypoldt F, Buchert R, Kleiter I, Marienhagen J, Gelderblom M, Magnus T et al (2012) Fluorodeoxyglucose positron emission tomography in anti-N-methyl-D-aspartate receptor encephalitis: distinct pattern of disease. J Neurol Neurosurg Psychiatry 83(7):681–686PubMedCentralPubMedCrossRefGoogle Scholar
  57. Leypoldt F, Titulaer MJ, Aguilar E, Walther J, Bonstrup M, Havemeister S et al (2013) Herpes simplex virus-1 encephalitis can trigger anti-NMDA receptor encephalitis: case report. Neurology 81(18):1637–1639PubMedCentralPubMedCrossRefGoogle Scholar
  58. Lilleker JB, Jones MS, Mohanraj R (2013) VGKC complex antibodies in epilepsy: diagnostic yield and therapeutic implications. Seizure 22(9):776–779PubMedCrossRefGoogle Scholar
  59. Mackay G, Ahmad K, Stone J, Sudlow C, Summers D, Knight R et al (2012) NMDA receptor autoantibodies in sporadic Creutzfeldt-Jakob disease. J Neurol 259(9):1979–1981PubMedCrossRefGoogle Scholar
  60. Majoie HJ, de Baets M, Renier W, Lang B, Vincent A (2006) Antibodies to voltage-gated potassium and calcium channels in epilepsy. Epilepsy Res 71(2–3):135–141PubMedCrossRefGoogle Scholar
  61. Marignier R, Chenevier F, Rogemond V, Sillevis SP, Renoux C, Cavillon G et al (2010) Metabotropic glutamate receptor type 1 autoantibody-associated cerebellitis: a primary autoimmune disease? Arch Neurol 67(5):627–630PubMedCrossRefGoogle Scholar
  62. Martinez-Hernandez E, Horvath J, Shiloh-Malawsky Y, Sangha N, Martinez-Lage M, Dalmau J (2011) Analysis of complement and plasma cells in the brain of patients with anti-NMDAR encephalitis. Neurology 77(6):589–593PubMedCentralPubMedCrossRefGoogle Scholar
  63. Mas N, Saiz A, Leite MI, Waters P, Baron M, Castano D et al (2011) Antiglycine-receptor encephalomyelitis with rigidity. J Neurol Neurosurg Psychiatry 82(12):1399–1401PubMedCrossRefGoogle Scholar
  64. Mat A, Adler H, Merwick A, Chadwick G, Gullo G, Dalmau JO et al (2013) Ophelia syndrome with metabotropic glutamate receptor 5 antibodies in CSF. Neurology 80(14):1349–1350PubMedCentralPubMedCrossRefGoogle Scholar
  65. McKeon A, Martinez-Hernandez E, Lancaster E, Matsumoto JY, Harvey RJ, McEvoy KM et al (2013) Glycine receptor autoimmune spectrum with stiff-man syndrome phenotype. JAMA Neurol 70(1):44–50PubMedCentralPubMedCrossRefGoogle Scholar
  66. Mikasova L, De RP, Bouchet D, Georges F, Rogemond V, Didelot A et al (2012) Disrupted surface cross-talk between NMDA and Ephrin-B2 receptors in anti-NMDA encephalitis. Brain 135(Pt 5):1606–1621PubMedCrossRefGoogle Scholar
  67. Mohammad SS, Sinclair K, Pillai S, Merheb V, Aumann TD, Gill D et al (2014) Herpes simplex encephalitis relapse with chorea is associated with autoantibodies to N-methyl-D-aspartate receptor or dopamine-2 receptor. Mov Disord 29(1):117–122PubMedCrossRefGoogle Scholar
  68. Moscato E, Peng XY, Parsons T, Dalmau J, Balice-Gordon R (2012) Acute mechanisms underlying antibody effects in anti-NMDA receptor encephalitis. J Neuroimmunol 253(1–2):145Google Scholar
  69. Mundiyanapurath S, Jarius S, Probst C, Stocker W, Wildemann B, Bosel J (2013) GABA-B-receptor antibodies in paraneoplastic brainstem encephalitis. J Neuroimmunol 259(1–2):88–91PubMedCrossRefGoogle Scholar
  70. Ohkawa T, Fukata Y, Yamasaki M, Miyazaki T, Yokoi N, Takashima H et al (2013) Autoantibodies to epilepsy-related LGI1 in limbic encephalitis neutralize LGI1-ADAM22 interaction and reduce synaptic AMPA receptors. J Neurosci 33(46):18161–18174PubMedCentralPubMedCrossRefGoogle Scholar
  71. Petit-Pedrol M, Armangue T, Peng X, Bataller L, Cellucci T, Davis R et al (2014) Encephalitis with refractory seizures, status epilepticus, and antibodies to the GABAA receptor: a case series, characterisation of the antigen, and analysis of the effects of antibodies. Lancet Neurol 13(3):276–286PubMedCrossRefGoogle Scholar
  72. Planaguma J, Leypoldt F, Mannara F, Gutierrez-Cuesta J, Martin-Garcia E, Aguilar E et al (2014) Human N-methyl-D-aspartate receptor antibodies alter memory and behaviour in mice. Brain (in press)Google Scholar
  73. Pruss H, Dalmau J, Harms L, Holtje M, Ahnert-Hilger G, Borowski K et al (2010) Retrospective analysis of NMDA receptor antibodies in encephalitis of unknown origin. Neurology 75(19):1735–1739PubMedCrossRefGoogle Scholar
  74. Quek AM, Britton JW, McKeon A, So E, Lennon VA, Shin C et al (2012) Autoimmune epilepsy: clinical characteristics and response to immunotherapy. Arch Neurol 69(5):582–593PubMedCentralPubMedCrossRefGoogle Scholar
  75. Radja GK, Cavanna AE (2013) Treatment of VGKC complex antibody-associated limbic encephalitis: a systematic review. J Neuropsychiatry Clin Neurosci 25(4):264–271PubMedCrossRefGoogle Scholar
  76. Schmitt SE, Pargeon K, Frechette ES, Hirsch LJ, Dalmau J, Friedman D (2012) Extreme delta brush: a unique EEG pattern in adults with anti-NMDA receptor encephalitis. Neurology 79(11):1094–1100PubMedCentralPubMedCrossRefGoogle Scholar
  77. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613–643PubMedCrossRefGoogle Scholar
  78. Shillito P, Molenaar PC, Vincent A, Leys K, Zheng W, van den Berg RJ et al (1995) Acquired neuromyotonia: evidence for autoantibodies directed against K + channels of peripheral nerves. Ann Neurol 38(5):714–722PubMedCrossRefGoogle Scholar
  79. Shin YW, Lee ST, Shin JW, Moon J, Lim JA, Byun JI et al (2013) VGKC-complex/LGI1-antibody encephalitis: clinical manifestations and response to immunotherapy. J Neuroimmunol 265(1–2):75–81PubMedCrossRefGoogle Scholar
  80. Sillevis SP, Kinoshita A, de Leeuw B, Moll W, Coesmans M, Jaarsma D et al (2000) Paraneoplastic cerebellar ataxia due to autoantibodies against a glutamate receptor. N Engl J Med 342(1):21–27CrossRefGoogle Scholar
  81. Sommer C, Weishaupt A, Brinkhoff J, Biko L, Wessig C, Gold R et al (2005) Paraneoplastic stiff-person syndrome: passive transfer to rats by means of IgG antibodies to amphiphysin. Lancet 365(9468):1406–1411PubMedCrossRefGoogle Scholar
  82. Szabo A, Dalmau J, Manley G, Rosenfeld M, Wong E, Henson J et al (1991) HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal. Cell 67(2):325–333PubMedCrossRefGoogle Scholar
  83. Titulaer MJ, Dalmau J (2014) Antibodies to NMDA and other synaptic receptors in choreoathetosis and relapsing symptoms post-Herpes Virus Encephalitis. Mov Dis 29(1):3–6CrossRefGoogle Scholar
  84. Titulaer MJ, McCracken L, Gabilondo I, Armangue T, Glaser C, Iizuka T et al (2013a) Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol 12:157–165PubMedCentralPubMedCrossRefGoogle Scholar
  85. Titulaer MJ, McCracken L, Gabilondo I, Iizuka T, Kawachi I, Bataller L et al (2013b) Late-onset anti-NMDA receptor encephalitis. Neurology 81(12):1058–1063PubMedCentralPubMedCrossRefGoogle Scholar
  86. Tuzun E, Zhou L, Baehring JM, Bannykh S, Rosenfeld MR, Dalmau J (2009) Evidence for antibody-mediated pathogenesis in anti-NMDAR encephalitis associated with ovarian teratoma. Acta Neuropathol 118(6):737–743PubMedCentralPubMedCrossRefGoogle Scholar
  87. van Coevorden-Hameete MH, de Graaff GE, Titulaer MJ, Hoogenraad CC, Sillevis Smitt PA (2014) Molecular and cellular mechanisms underlying anti-neuronal antibody mediated disorders of the central nervous system. Autoimmun Rev 13(3):299–312PubMedCrossRefGoogle Scholar
  88. Viaccoz A, Desestret V, Ducray F, Picard G, Cavillon G, Rogemond V et al (2014) Clinical specificities of adult male patients with NMDA receptor antibodies encephalitis. Neurology 82(7):556–563PubMedCrossRefGoogle Scholar
  89. Vincent A, Bien CG, Irani SR, Waters P (2011) Autoantibodies associated with diseases of the CNS: new developments and future challenges. Lancet Neurol 10(8):759–772PubMedCrossRefGoogle Scholar
  90. Vitaliani R, Mason W, Ances B, Zwerdling T, Jiang Z, Dalmau J (2005) Paraneoplastic encephalitis, psychiatric symptoms, and hypoventilation in ovarian teratoma. Ann Neurol 58(4):594–604PubMedCentralPubMedCrossRefGoogle Scholar
  91. Wei YC, Liu CH, Lin JJ, Lin KJ, Huang KL, Lee TH et al (2013) Rapid progression and brain atrophy in anti-AMPA receptor encephalitis. J Neuroimmunol 261(1–2):129–133PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of NeurologyErasmus Medical CenterRotterdamThe Netherlands
  2. 2.Department of NeurologyHaga HospitalThe HagueThe Netherlands

Personalised recommendations