Herpes simplex virus-induced anti-N-methyl-d-aspartate receptor encephalitis: a systematic literature review with analysis of 43 cases

Developmental Medicine and Child Neurology

Volumn 59, Issue 8, 2017, Pages 796-805

  Nosadini, Margherita ^a   Mohammad, Shekeeb S ^b   Corazza, Francesco ^a   Ruga, Ezia Maria ^c   Kothur, Kavitha ^b   Perilongo, Giorgio ^c   Frigo, Anna Chiara ^c   Toldo, Irene ^a   Dale, Russell C ^b   Sartori, Stefano ^a  

^a UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACICLOVIR; CARBAMAZEPINE; GLUCOSE; METHYLPREDNISOLONE; OLANZAPINE; PREDNISOLONE; PREDNISONE;

ANTI N METHYL D ASPARTATE RECEPTOR ENCEPHALITIS; ANTIVIRAL THERAPY; CASE REPORT; CEREBROSPINAL FLUID; CHILD; COGNITIVE DEFECT; CONFUSION; DAILY LIFE ACTIVITY; DISEASE DURATION; DISORIENTATION; DRUG DOSE REDUCTION; DRUG MEGADOSE; DYSKINESIA; DYSLEXIA; ECHOLALIA; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; FEMALE; FEVER; FOCAL EPILEPSY; FOLLOW UP; HEADACHE; HERPES SIMPLEX; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS; HUMAN; HYPERSALIVATION; IMMUNOTHERAPY; IRRITABILITY; LATENT PERIOD; LETHARGY; LEUKOCYTE; LUMBAR PUNCTURE; MOOD DISORDER; MOTOR DYSFUNCTION; NUCLEAR MAGNETIC RESONANCE IMAGING; OBSESSION; OBSESSIVE COMPULSIVE DISORDER; PLASMA EXCHANGE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSOPAGNOSIA; RANKIN SCALE; RECURRENT DISEASE; RELAPSE; REVIEW; SCHOOL CHILD; SLEEP DISORDER; SPEECH DISORDER; STEREOTYPY; SYSTEMATIC REVIEW; TONIC CLONIC SEIZURE; VOMITING; ADULT; ANTI-N-METHYL-D-ASPARTATE RECEPTOR ENCEPHALITIS; COMPLICATION; MENTAL DISORDERS; MICROBIOLOGY; MOVEMENT DISORDERS; PATHOGENICITY; PATHOPHYSIOLOGY; SIMPLEXVIRUS;

ADULT; ANTI-N-METHYL-D-ASPARTATE RECEPTOR ENCEPHALITIS; CHILD; ENCEPHALITIS, HERPES SIMPLEX; FEMALE; HUMANS; MENTAL DISORDERS; MOVEMENT DISORDERS; SIMPLEXVIRUS;

EID: 85018850607     PISSN: 00121622     EISSN: 14698749     Source Type: Journal    
DOI: 10.1111/dmcn.13448     Document Type: Review

References (69)

1. Whitley RJ, Lakeman F. Herpes simplex virus infections of the central nervous system: therapeutic and diagnostic considerations. Clin Infect Dis 1995; 20: 414–20.
2. Kimura H, Aso K, Kuzushima K, Hanada N, Shibata M, Morishima T. Relapse of herpes simplex encephalitis in children. Pediatrics 1992; 89: 891–4.
3. Sköldenberg B, Aurelius E, Hjalmarsson A, et al. Incidence and pathogenesis of clinical relapse after herpes simplex encephalitis in adults. J Neurol 2006; 253: 163–70.
4. Schleede L, Bueter W, Baumgartner-Sigl S, et al. Pediatric herpes simplex virus encephalitis: a retrospective multicenter experience. J Child Neurol 2013; 28: 321–31.
5. Raschilas F, Wolff M, Delatour F, et al. Outcome of and prognostic factors for herpes simplex encephalitis in adult patients: results of a multicenter study. Clin Infect Dis 2002; 35: 254–60.
6. Ito Y, Kimura H, Yabuta Y, et al. Exacerbation of herpes simplex encephalitis after successful treatment with acyclovir. Clin Infect Dis 2000; 30: 185–7.
7. De Tiège X, Rozenberg F, Des Portes V, et al. Herpes simplex encephalitis relapses in children: differentiation of two neurologic entities. Neurology 2003; 61: 241–3.
8. De Tiège X, De Laet C, Mazoin N, et al. Postinfectious immune-mediated encephalitis after pediatric herpes simplex encephalitis. Brain Dev 2005; 27: 304–7.
9. Prüss H, Finke C, Höltje M, et al. N-methyl-D-aspartate receptor antibodies in herpes simplex encephalitis. Ann Neurol 2012; 72: 902–11.
10. Irani SR, Bera K, Waters P, et al. N-methyl-D-aspartate antibody encephalitis: temporal progression of clinical and paraclinical observations in a predominantly non-paraneoplastic disorder of both sexes. Brain 2010; 133: 1655–67.
11. 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: 157–65.
12. Granerod J, Cunningham R, Zuckerman M, et al. Causality in acute encephalitis: defining aetiologies. Epidemiol Infect 2010; 138: 783–800.
13. van Swieten JC, Koudstaal PJ, Visser MC, et al. Interobserver agreement for the assessment of handicap in stroke patients. Stroke 1988; 19: 604–7.
14. Armangue T, Titulaer MJ, Málaga I, et al. Pediatric anti-N-methyl-D-aspartate receptor encephalitis-clinical analysis and novel findings in a series of 20 patients. J Pediatr 2013; 162: 850–6.e2.
15. Leypoldt F, Titulaer MJ, Aguilar E, et al. Herpes simplex virus-1 encephalitis can trigger anti-NMDA receptor encephalitis: case report. Neurology 2013; 81: 1637–9.
16. Armangue T, Leypoldt F, Málaga I, et al. Herpes simplex virus encephalitis is a trigger of brain autoimmunity. Ann Neurol 2014; 75: 317–23.
17. Desena A, Graves D, Warnack W, Greenberg BM. Herpes simplex encephalitis as a potential cause of anti-N-methyl-D-aspartate receptor antibody encephalitis: report of 2 cases. JAMA Neurol 2014; 71: 344–6.
18. Hacohen Y, Deiva K, Pettingill P, et al. N-methyl-D-aspartate receptor antibodies in post-herpes simplex virus encephalitis neurological relapse. Mov Disord 2014; 29: 90–6.
19. Hacohen Y, Absoud M, Hemingway C, et al. NMDA receptor antibodies associated with distinct white matter syndromes. Neurol Neuroimmunol Neuroinflamm 2014; 1: e2.
20. Mohammad SS, Sinclair K, Pillai S, et al. Herpes simplex encephalitis relapse with chorea is associated with autoantibodies to N-Methyl-D-aspartate receptor or dopamine-2 receptor. Mov Disord 2014; 29: 117–22.
21. Wickström R, Fowler A, Cooray G, Karlsson-Parra A, Grillner P. Viral triggering of anti-NMDA receptor encephalitis in a child - an important cause for disease relapse. Eur J Paediatr Neurol 2014; 18: 543–6.
22. Bektaş Ö, Tanyel T, Kocabaş BA, Fitöz S, Ince E, Deda G. Anti-N-methyl-D-aspartate receptor encephalitis that developed after herpes encephalitis: a case report and literature review. Neuropediatrics 2014; 45: 396–401.
23. Yushvayev-Cavalier Y, Nichter C, Ramirez-Zamora A. Possible autoimmune association between herpes simplex virus infection and subsequent anti-N-methyl-D-aspartate receptor encephalitis: a pediatric patient with abnormal movements. Pediatr Neurol 2015; 52: 454–6.
24. Bamford A, Crowe BH, Hacohen Y, et al. Pediatric herpes simplex virus encephalitis complicated by N-methyl-D-aspartate receptor antibody encephalitis. J Pediatric Infect Dis Soc 2015; 4: e17–21.
25. Ellul MA, Griffiths MJ, Iyer A, et al. Anti-N-methyl-D-aspartate receptor encephalitis in a young child with histological evidence on brain biopsy of co-existent herpes simplex virus type 1 infection. Pediatr Infect Dis J 2016; 35: 347–9.
26. Sutcu M, Akturk H, Somer A, et al. Role of autoantibodies to N-methyl-D-aspartate (NMDA) receptor in relapsing herpes simplex encephalitis: a retrospective, one-center experience. J Child Neurol 2016; 31: 345–50.
27. Armangue T, Moris G, Cantarín-Extremera V, et al. Autoimmune post-herpes simplex encephalitis of adults and teenagers. Neurology 2015; 85: 1736–43.
28. Pistacchi M, Marsala SZ, Gioulis M, Sanson F, Giometto B. Uncommon relapse after post-herpes simplex encephalitis: an atypical case report. Acta Neurol Belg 2015; 115: 691–5.
29. Morris NA, Kaplan TB, Linnoila J, Cho T. HSV encephalitis-induced anti-NMDAR encephalitis in a 67-year-old woman: report of a case and review of the literature. J Neurovirol 2016; 22: 33–7.
30. García-Moreno J, Igartua Laraudogoitia J, Montes Ros M. Pneumocystis jirovecii pneumonia in a patient with anti-N-methyl D-aspartate receptor postherpetic encephalitis. Pediatr Infect Dis J 2016; 35: 816–7.
31. Geoghegan S, Walsh A, King MD, et al. Anti-N-methyl-D-aspartate receptor antibody mediated neurologic relapse post herpes simplex encephalitis: a case series. Pediatr Infect Dis J 2016; 35: e258–61.
32. Casares-Vivas M, Portilla-Cuenca JC, Gallego-Texeira I, Calderón-Pecellín A, Gallego-Curto E, Casado-Naranjo I. Anti-NMDA antibody encephalitis secondary to herpes simplex virus infection. Med Intensiva 2016; 40: 193–5.
33. Schein F, Gagneux-Brunon A, Antoine JC, et al. Anti-N-methyl-D-aspartate receptor encephalitis after herpes simplex virus-associated encephalitis: an emerging disease with diagnosis and therapeutic challenges. Infection 2016 Nov 8. doi: 10.1007/s15010-016-0959-y. [E-pub ahead of print].
34. Westman G, Studahl M, Ahlm C, et al. N-methyl-D-aspartate receptor autoimmunity affects cognitive performance in herpes simplex encephalitis. Clin Microbiol Infect 2016; 22: 934–40.
35. Davies G, Irani SR, Coltart C, et al. Anti-N-methyl-D-aspartate receptor antibodies: a potentially treatable cause of encephalitis in the intensive care unit. Crit Care Med 2010; 38: 679–82.
36. Hacohen Y, Wright S, Waters P, et al. Paediatric autoimmune encephalopathies: clinical features, laboratory investigations and outcomes in patients with or without antibodies to known central nervous system autoantigens. J Neurol Neurosurg Psychiatry 2013; 84: 748–55.
37. Safadieh L, Dabbagh O. Anti-N-methyl-D-aspartate (NMDA) receptor encephalitis in a young Lebanese girl. J Child Neurol 2013; 28: 1222–5.
38. Veciana M, Becerra JL, Fossas P, et al. EEG extreme delta brush: an ictal pattern in patients with anti-NMDA receptor encephalitis. Epilepsy Behav 2015; 49: 280–5.
39. Huang X, Fan C, Wu J, et al. Clinical analysis on anti-N-methyl-D-aspartate receptor encephalitis cases: Chinese experience. Int J Clin Exp Med 2015; 8: 18927–35.
40. Pike MG, Kennedy CR, Neville BG, Levin M. Herpes simplex encephalitis with relapse. Arch Dis Child 1991; 66: 1242–4.
41. Gascon GG, al-Jarallah AA, Okamoto E, al Ahdal M, Kessie G, Frayha H. Chorea as a presentation of herpes simplex encephalitis relapse. Brain Dev 1993; 15: 178–81.
42. Wang HS, Kuo MF, Huang SC, Chou ML. Choreoathetosis as an initial sign of relapsing of herpes simplex encephalitis. Pediatr Neurol 1994; 11: 341–5.
43. Barthez-Carpentier MA, Rozenberg F, Dussaix E, et al. Relapse of herpes simplex encephalitis. J Child Neurol 1995; 10: 363–8.
44. Hargrave DR, Webb DW. Movement disorders in association with herpes simplex virus encephalitis in children: a review. Dev Med Child Neurol 1998; 40: 640–2.
45. Huang Q, Wu Y, Qin R, Wei X, Ma M. Clinical characteristics and outcomes between children and adults with anti-N-Methyl-D-Aspartate receptor encephalitis. J Neurol 2016; 263: 2446–55.
46. Duan BC, Weng WC, Lin KL, et al. Variations of movement disorders in anti-N-methyl-D-aspartate receptor encephalitis: a nationwide study in Taiwan. Medicine (Baltimore) 2016; 95: e4365.
47. Kreye J, Wenke NK, Chayka M, et al. Human cerebrospinal fluid monoclonal N-methyl-D-aspartate receptor autoantibodies are sufficient for encephalitis pathogenesis. Brain 2016; 139: 2641–52.
48. Dale RC, Brilot F, Duffy LV, et al. Utility and safety of rituximab in pediatric autoimmune and inflammatory CNS disease. Neurology 2014; 83: 142–50.
49. Byrne S, Walsh C, Hacohen Y, et al. Earlier treatment of NMDAR antibody encephalitis in children results in a better outcome. Neurol Neuroimmunol Neuroinflamm 2015; 2: e130.
50. Nosadini M, Mohammad SS, Ramanathan S, Brilot F, Dale RC. Immune therapy in autoimmune encephalitis: a systematic review. Expert Rev Neurother 2015; 15: 1391–419.
51. Sartori S, Nosadini M, Cesaroni E, et al. Paediatric anti-N-methyl-D-aspartate receptor encephalitis: the first Italian multicenter case series. Eur J Paediatr Neurol 2015; 19: 453–63.
52. Reiber H, Ungefehr S, Jacobi C. The intrathecal, polyspecific and oligoclonal immune response in multiple sclerosis. Mult Scler 1998; 4: 111–7.
53. Smyk DS, Alexander AK, Walker M, Walker M. Acute disseminated encephalomyelitis progressing to multiple sclerosis: are infectious triggers involved? Immunol Res 2014; 60: 16–22.
54. Loshaj-Shala A, Regazzoni L, Daci A, et al. Guillain Barré syndrome (GBS): new insights in the molecular mimicry between C. jejuni and human peripheral nerve (HPN) proteins. J Neuroimmunol 2015; 289: 168–76.
55. Cunningham MW. Rheumatic fever, autoimmunity, and molecular mimicry: the streptococcal connection. Int Rev Immunol 2014; 33: 314–29.
56. Linnoila JJ, Binnicker MJ, Majed M, Klein CJ, McKeon A. CSF herpes virus and autoantibody profiles in the evaluation of encephalitis. Neurol Neuroimmunol Neuroinflamm 2016; 3: e245.
57. Casanova-Gracia N, Banzo-Arguis C, Sanz-Asin P, Zapata-Usabel M, Jordana-Vilanova N, Cortina-Lacambra MT. Encephalitis associated to anti-NMDA receptor antibodies: a description of two cases in the child/youth population (In Spanish). Rev Neurol 2012; 54: 475–8.
58. Schäbitz WR, Rogalewski A, Hagemeister C, Bien CG. VZV brainstem encephalitis triggers NMDA receptor immunoreaction. Neurology 2014; 83: 2309–11.
59. Venâncio P, Brito MJ, Pereira G, Vieira JP. Anti-N-methyl-D-aspartate receptor encephalitis with positive serum antithyroid antibodies, IgM antithyroid antibodies, IgM antibodies against mycoplasma pneumoniae and human herpesvirus 7 PCR in the CSF. Pediatr Infect Dis J 2014; 33: 882–3.
60. Solís N, Salazar L, Hasbun R. Anti-NMDA Receptor antibody encephalitis with concomitant detection of Varicella zoster virus. J Clin Virol 2016; 83: 26–8.
61. Thompson KA, Blessing WW, Wesselingh SL. Herpes simplex replication and dissemination is not increased by corticosteroid treatment in a rat model of focal Herpes encephalitis. J Neurovirol 2000; 6: 25–32.
62. Meyding-Lamadé U, Oberlinner C, Rau PR, et al. Experimental herpes simplex virus encephalitis: a combination therapy of acyclovir and glucocorticoids reduces long-term magnetic resonance imaging abnormalities. J Neurovirol 2003; 9: 118–25.
63. Yamamoto K, Chiba HO, Ishitobi M, Nakagawa H, Ogawa T, Ishii K. Acute encephalopathy with bilateral striatal necrosis: favourable response to corticosteroid therapy. Eur J Paediatr Neurol 1997; 1: 41–5.
64. Kamei S, Sekizawa T, Shiota H, et al. Evaluation of combination therapy using aciclovir and corticosteroid in adult patients with herpes simplex virus encephalitis. J Neurol Neurosurg Psychiatry 2005; 76: 1544–9.
65. Musallam B, Matoth I, Wolf DG, Engelhard D, Averbuch D. Steroids for deteriorating herpes simplex virus encephalitis. Pediatr Neurol 2007; 37: 229–32.
66. Maraş Genç H, Uyur Yalçın E, Sayan M, et al. Clinical outcomes in children with herpes simplex encephalitis receiving steroid therapy. J Clin Virol 2016; 80: 87–92.
67. Sergerie Y, Boivin G, Gosselin D, Rivest S. Delayed but not early glucocorticoid treatment protects the host during experimental herpes simplex virus encephalitis in mice. J Infect Dis 2007; 195: 817–25.
68. Martinez-Torres F, Menon S, Pritsch M, et al. Protocol for German trial of Acyclovir and corticosteroids in Herpes-simplex-virus-encephalitis (GACHE): a multicenter, multinational, randomized, double-blind, placebo-controlled German, Austrian and Dutch trial [ISRCTN45122933]. BMC Neurol 2008; 8: 40.
69. Kothur K, Wienholt L, Mohammad SS, et al. Utility of CSF cytokine/chemokines as markers of active intrathecal inflammation: comparison of demyelinating, anti-NMDAR and enteroviral encephalitis. PLoS ONE 2016; 11: e0161656.