Neuropediatrics 2013; 44(06): 336-345
DOI: 10.1055/s-0033-1358603
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Autoantibody-Associated Movement Disorders

Shekeeb S. Mohammad
1   Neuroimmunology Group, Institute for Neuroscience and Muscle Research, The Kids Research Institute, The Children's Hospital at Westmead, University of Sydney, New South Wales, Australia
2   TY Nelson Department of Neurology and Neurosurgery, The Children's Hospital at Westmead, New South Wales, Australia
,
Sudarshini Ramanathan
1   Neuroimmunology Group, Institute for Neuroscience and Muscle Research, The Kids Research Institute, The Children's Hospital at Westmead, University of Sydney, New South Wales, Australia
,
Fabienne Brilot
1   Neuroimmunology Group, Institute for Neuroscience and Muscle Research, The Kids Research Institute, The Children's Hospital at Westmead, University of Sydney, New South Wales, Australia
,
Russell C. Dale
1   Neuroimmunology Group, Institute for Neuroscience and Muscle Research, The Kids Research Institute, The Children's Hospital at Westmead, University of Sydney, New South Wales, Australia
2   TY Nelson Department of Neurology and Neurosurgery, The Children's Hospital at Westmead, New South Wales, Australia
› Author Affiliations
Further Information

Publication History

17 July 2013

08 August 2013

Publication Date:
07 November 2013 (online)

Abstract

Autoantibodies to the extracellular domain of neuronal proteins cause different neurological conditions with movement disorders as a prominent feature. We reviewed the literature of autoantibody-mediated and autoantibody-associated diseases focusing on anti-N-methyl-d-aspartate receptor (NMDAR) encephalitis, autoimmune basal ganglia encephalitis, Sydenham chorea, and the rare syndrome of progressive encephalomyelitis with rigidity and myoclonus. NMDAR encephalitis is a diffuse encephalitis with psychiatric and cognitive features associated with autoantibodies against the NR1 subunit of the NMDAR. The movement disorder phenotype is diverse and often generalized in young children. Although orofacial dyskinesia was the initial movement phenotype, chorea, dystonia, catatonia, and stereotypical movements are now described. The stereotypical movements can be bizarre and include cycling movements and compulsive self-injurious behavior. Autoimmune basal ganglia encephalitis is an inflammatory encephalitis localizing to the basal ganglia that is sometimes associated with serum antibodies against dopamine-2 receptor. Although psychiatric features are common, the dominant problem is a movement disorder, with dystonia-parkinsonism being characteristic. Sydenham chorea is the prototypic poststreptococcal autoimmune neuropsychiatric disorder and several autoantibodies may be involved in disease generation. The syndrome is characterized by a pure chorea, although hypotonia, dysarthria, and emotional lability are common. Progressive encephalomyelitis with rigidity and myoclonus is a rare autoimmune disorder causing rigidity, stimulus sensitive spasms, and myoclonus of nonepileptic origin and is associated with autoantibodies of multiple types including those against the glycine receptor. These disorders are important to recognize and diagnose, as immune therapy can shorten disease duration and improve outcome.

 
  • References

  • 1 Blumkin L, Pranzatelli MR. Acquired ataxias, infectious and para-infectious. Handb Clin Neurol 2012; 103: 137-146
  • 2 Gorman MP. Update on diagnosis, treatment, and prognosis in opsoclonus-myoclonus-ataxia syndrome. Curr Opin Pediatr 2010; 22 (6) 745-750
  • 3 Lancaster E, Dalmau J. Neuronal autoantigens—pathogenesis, associated disorders and antibody testing. Nat Rev Neurol 2012; 8 (7) 380-390
  • 4 Panzer J, Dalmau J. Movement disorders in paraneoplastic and autoimmune disease. Curr Opin Neurol 2011; 24 (4) 346-353
  • 5 Hartley LM, Ng SY, Dale RC, Church AJ, Martinez A, de Sousa C. Immune mediated chorea encephalopathy syndrome in childhood. Dev Med Child Neurol 2002; 44 (4) 273-277
  • 6 Dale RC, Church AJ, Surtees RA , et al. Encephalitis lethargica syndrome: 20 new cases and evidence of basal ganglia autoimmunity. Brain 2004; 127 (Pt 1) 21-33
  • 7 Sébire G, Devictor D, Huault G, Aicardi J, Landrieu P, Tardieu M. Coma associated with intense bursts of abnormal movements and long-lasting cognitive disturbances: an acute encephalopathy of obscure origin. J Pediatr 1992; 121 (6) 845-851
  • 8 Dalmau J, Tüzün E, Wu HY , et al. Paraneoplastic anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol 2007; 61 (1) 25-36
  • 9 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 (2) 157-165
  • 10 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
  • 11 Hughes EG, Peng X, Gleichman AJ , et al. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 2010; 30 (17) 5866-5875
  • 12 Armangue T, Titulaer MJ, Málaga I , et al; Spanish Anti-N-methyl-D-Aspartate Receptor (NMDAR) Encephalitis Work Group. Pediatric anti-N-methyl-D-aspartate receptor encephalitis-clinical analysis and novel findings in a series of 20 patients. J Pediatr 2013; 162 (4) 850 , e2
  • 13 Florance NR, Davis RL, Lam C , et al. Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents. Ann Neurol 2009; 66 (1) 11-18
  • 14 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 (Pt 6) 1655-1667
  • 15 Dalmau J, Lancaster E, Martinez-Hernandez E, Rosenfeld MR, Balice-Gordon R. Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurol 2011; 10 (1) 63-74
  • 16 Rubio-Agustí I, Dalmau J, Sevilla T, Burgal M, Beltrán E, Bataller L. Isolated hemidystonia associated with NMDA receptor antibodies. Mov Disord 2011; 26 (2) 351-352
  • 17 Baizabal-Carvallo JF, Stocco A, Muscal E, Jankovic J. The spectrum of movement disorders in children with anti-NMDA receptor encephalitis. Mov Disord 2013; 28 (4) 543-547
  • 18 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 (7) 748-755
  • 19 Armangue T, Petit-Pedrol M, Dalmau J. Autoimmune encephalitis in children. J Child Neurol 2012; 27 (11) 1460-1469
  • 20 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 (2) 679-682
  • 21 Dale RC, Irani SR, Brilot F , et al. N-methyl-D-aspartate receptor antibodies in pediatric dyskinetic encephalitis lethargica. Ann Neurol 2009; 66 (5) 704-709
  • 22 Gable MS, Gavali S, Radner A , et al. Anti-NMDA receptor encephalitis: report of ten cases and comparison with viral encephalitis. Eur J Clin Microbiol Infect Dis 2009; 28 (12) 1421-1429
  • 23 Kleinig TJ, Thompson PD, Matar W , et al. The distinctive movement disorder of ovarian teratoma-associated encephalitis. Mov Disord 2008; 23 (9) 1256-1261
  • 24 Sansing LH, Tüzün E, Ko MW, Baccon J, Lynch DR, Dalmau J. A patient with encephalitis associated with NMDA receptor antibodies. Nat Clin Pract Neurol 2007; 3 (5) 291-296
  • 25 Vitaliani R, Mason W, Ances B, Zwerdling T, Jiang Z, Dalmau J. Paraneoplastic encephalitis, psychiatric symptoms, and hypoventilation in ovarian teratoma. Ann Neurol 2005; 58 (4) 594-604
  • 26 Lebas A, Husson B, Didelot A, Honnorat J, Tardieu M. Expanding spectrum of encephalitis with NMDA receptor antibodies in young children. J Child Neurol 2010; 25 (6) 742-745
  • 27 Poloni C, Korff CM, Ricotti V , et al. Severe childhood encephalopathy with dyskinesia and prolonged cognitive disturbances: evidence for anti-N-methyl-D-aspartate receptor encephalitis. Dev Med Child Neurol 2010; 52 (5) e78-e82
  • 28 Uchino A, Iizuka T, Urano Y , et al. Pseudo-piano playing motions and nocturnal hypoventilation in anti-NMDA receptor encephalitis: response to prompt tumor removal and immunotherapy. Intern Med 2011; 50 (6) 627-630
  • 29 Schimmel M, Bien CG, Vincent A, Schenk W, Penzien J. Successful treatment of anti-N-methyl-D-aspartate receptor encephalitis presenting with catatonia. Arch Dis Child 2009; 94 (4) 314-316
  • 30 Ramanathan S, Wong CH, Fung VS. Long duration between presentation of probable anti-N-methyl-D-aspartate receptor encephalitis and either clinical relapse or positive serum autoantibodies. J Clin Neurosci 2013; 20 (9) 1322-1323
  • 31 Consoli A, Ronen K, An-Gourfinkel I , et al. Malignant catatonia due to anti-NMDA-receptor encephalitis in a 17-year-old girl: case report. Child Adolesc Psychiatry Ment Health 2011; 5 (1) 15
  • 32 Baizabal-Carvallo JF, Jankovic J. Movement disorders in autoimmune diseases. Mov Disord 2012; 27 (8) 935-946
  • 33 Stamelou M, Plazzi G, Lugaresi E, Edwards MJ, Bhatia KP. The distinct movement disorder in anti-NMDA receptor encephalitis may be related to Status Dissociatus: a hypothesis. Mov Disord 2012; 27 (11) 1360-1363
  • 34 Chapman MR, Vause HE. Anti-NMDA receptor encephalitis: diagnosis, psychiatric presentation, and treatment. Am J Psychiatry 2011; 168 (3) 245-251
  • 35 Maat P, de Graaff E, van Beveren NM , et al. Psychiatric phenomena as initial manifestation of encephalitis by anti-NMDAR antibodies. Acta Neuropsychiatr 2013; 25 (3) 128-136
  • 36 Lopez-Alberola R, Georgiou M, Sfakianakis GN, Singer C, Papapetropoulos S. Contemporary Encephalitis Lethargica: phenotype, laboratory findings and treatment outcomes. J Neurol 2009; 256 (3) 396-404
  • 37 Vilensky JA, Foley P, Gilman S. Children and encephalitis lethargica: a historical review. Pediatr Neurol 2007; 37 (2) 79-84
  • 38 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
  • 39 Hall AJ. The lumleian lectures [abridged] on encephalitis lethargica (epidemic encephalitis). Lancet 1923; 201 (5198) 731-740
  • 40 Beattie GC, Glaser CA, Sheriff H , et al. Encephalitis with thalamic and basal ganglia abnormalities: etiologies, neuroimaging, and potential role of respiratory viruses. Clin Infect Dis 2013; 56 (6) 825-832
  • 41 Rail D, Scholtz C, Swash M. Post-encephalitic Parkinsonism: current experience. J Neurol Neurosurg Psychiatry 1981; 44 (8) 670-676
  • 42 Blunt SB, Lane RJ, Turjanski N, Perkin GD. Clinical features and management of two cases of encephalitis lethargica. Mov Disord 1997; 12 (3) 354-359
  • 43 The memorandum on encephalitis lethargica. Lancet 1924; 203 (5258) 1163
  • 44 Smith MT, Lester-Smith D, Zurynski Y, Noonan S, Carapetis JR, Elliott EJ. Persistence of acute rheumatic fever in a tertiary children's hospital. J Paediatr Child Health 2011; 47 (4) 198-203
  • 45 Cardoso F, Eduardo C, Silva AP, Mota CC. Chorea in fifty consecutive patients with rheumatic fever. Mov Disord 1997; 12 (5) 701-703
  • 46 Klawans HL, Brandabur MM. Chorea in childhood. Pediatr Ann 1993; 22 (1) 41-46 , 49–50
  • 47 Nausieda PA, Grossman BJ, Koller WC, Weiner WJ, Klawans HL. Sydenham chorea: an update. Neurology 1980; 30 (3) 331-334
  • 48 Teixeira Jr AL, Maia DP, Cardoso F. [The initial testing and the discrimination property of the UFMG Sydenham's Chorea Rating Scale (USCRS)]. Arq Neuropsiquiatr 2005; 63 (3B) 825-827
  • 49 Teixeira Jr AL, Maia DP, Cardoso F. UFMG Sydenham's chorea rating scale (USCRS): reliability and consistency. Mov Disord 2005; 20 (5) 585-591
  • 50 de Teixeira AL, Cardoso F, Maia DP , et al. Frequency and significance of vocalizations in Sydenham's chorea. Parkinsonism Relat Disord 2009; 15 (1) 62-63
  • 51 Mercadante MT, Campos MC, Marques-Dias MJ, Miguel EC, Leckman J. Vocal tics in Sydenham's chorea. J Am Acad Child Adolesc Psychiatry 1997; 36 (3) 305-306
  • 52 El Otmani H, Moutaouakil F, Fadel H, Slassi I. Chorea paralytica: a videotape case with rapid recovery and good long-term outcome. Acta Neurol Belg 2013;
  • 53 Cardoso F. Sydenham's Chorea. Curr Treat Options Neurol 2008; 10 (3) 230-235
  • 54 Giedd JN, Rapoport JL, Kruesi MJ , et al. Sydenham's chorea: magnetic resonance imaging of the basal ganglia. Neurology 1995; 45 (12) 2199-2202
  • 55 Barsottini OG, Ferraz HB, Seviliano MM, Barbieri A. Brain SPECT imaging in Sydenham's chorea. Braz J Med Biol Res 2002; 35 (4) 431-436
  • 56 Walker K, Brink A, Lawrenson J, Mathiassen W, Wilmshurst JM. Treatment of sydenham chorea with intravenous immunoglobulin. J Child Neurol 2012; 27 (2) 147-155
  • 57 Kirvan CA, Swedo SE, Heuser JS, Cunningham MW. Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea. Nat Med 2003; 9 (7) 914-920
  • 58 Dale RC, Candler PM, Church AJ, Wait R, Pocock JM, Giovannoni G. Neuronal surface glycolytic enzymes are autoantigen targets in post-streptococcal autoimmune CNS disease. J Neuroimmunol 2006; 172 (1-2) 187-197
  • 59 Brimberg L, Benhar I, Mascaro-Blanco A , et al. Behavioral, pharmacological, and immunological abnormalities after streptococcal exposure: a novel rat model of Sydenham chorea and related neuropsychiatric disorders. Neuropsychopharmacology 2012; 37 (9) 2076-2087
  • 60 Fusco C, Ucchino V, Frattini D, Pisani F, Della Giustina E. Acute and chronic corticosteroid treatment of ten patients with paralytic form of Sydenham's chorea. Eur J Paediatr Neurol 2012; 16 (4) 373-378
  • 61 Garvey MA, Snider LA, Leitman SF, Werden R, Swedo SE. Treatment of Sydenham's chorea with intravenous immunoglobulin, plasma exchange, or prednisone. J Child Neurol 2005; 20 (5) 424-429
  • 62 Carapetis JR, Currie BJ. Rheumatic chorea in northern Australia: a clinical and epidemiological study. Arch Dis Child 1999; 80 (4) 353-358
  • 63 Teixeira AL, Cardoso F, Maia DP, Cunningham MC. Sydenham's chorea may be a risk factor for drug induced parkinsonism. J Neurol Neurosurg Psychiatry 2003; 74 (9) 1350-1351
  • 64 Cardoso F. Sydenham's chorea. Handb Clin Neurol 2011; 100: 221-229
  • 65 Cardoso F, Vargas AP, Oliveira LD, Guerra AA, Amaral SV. Persistent Sydenham's chorea. Mov Disord 1999; 14 (5) 805-807
  • 66 Korn-Lubetzki I, Brand A, Steiner I. Recurrence of Sydenham chorea: implications for pathogenesis. Arch Neurol 2004; 61 (8) 1261-1264
  • 67 Aron AM, Freeman JM, Carter S. The Natural History of Sydenham's Chorea. Review of the Literature and Long-Term Evaluation with Emphasis on Cardiac Sequelae. Am J Med 1965; 38: 83-95
  • 68 Gimeno H, Barry S, Lin JP, Gordon A. Functional impact of Sydenham's Chorea: A Case Report. (e-pub ahead of print) Tremor Other Hyperkinet Mov (NY) 2013;
  • 69 Swedo SE, Leckman JF, Rose NR. From research subgroup to clinical syndrome: modifying the PANDAS criteria to describe PANS (pediatric acute-onset neuropsychiatric syndrome). Pediatr Therapeut 2012; 2: 113
  • 70 Singer HS, Gilbert DL, Wolf DS, Mink JW, Kurlan R. Moving from PANDAS to CANS. J Pediatr 2012; 160 (5) 725-731
  • 71 Singer HS, Hong JJ, Yoon DY, Williams PN. Serum autoantibodies do not differentiate PANDAS and Tourette syndrome from controls. Neurology 2005; 65 (11) 1701-1707
  • 72 Church AJ, Dale RC, Giovannoni G. Anti-basal ganglia antibodies: a possible diagnostic utility in idiopathic movement disorders?. Arch Dis Child 2004; 89 (7) 611-614
  • 73 Dale RC, Heyman I, Surtees RA , et al. Dyskinesias and associated psychiatric disorders following streptococcal infections. Arch Dis Child 2004; 89 (7) 604-610
  • 74 Martino D, Defazio G, Giovannoni G. The PANDAS subgroup of tic disorders and childhood-onset obsessive-compulsive disorder. J Psychosom Res 2009; 67 (6) 547-557
  • 75 Stern WM, Howard R, Chalmers RM , et al. Glycine receptor antibody mediated Progressive Encephalomyelitis with Rigidity and Myoclonus (PERM): a rare but treatable neurological syndrome. (e-pub ahead of print). Pract Neurol 2013;
  • 76 Hutchinson M, Waters P, McHugh J , et al. Progressive encephalomyelitis, rigidity, and myoclonus: a novel glycine receptor antibody. Neurology 2008; 71 (16) 1291-1292
  • 77 Damásio J, Leite MI, Coutinho E , et al. Progressive encephalomyelitis with rigidity and myoclonus: the first pediatric case with glycine receptor antibodies. JAMA Neurol 2013; 70 (4) 498-501
  • 78 Meinck HM, Thompson PD. Stiff man syndrome and related conditions. Mov Disord 2002; 17 (5) 853-866
  • 79 Turner MR, Irani SR, Leite MI, Nithi K, Vincent A, Ansorge O. Progressive encephalomyelitis with rigidity and myoclonus: glycine and NMDA receptor antibodies. Neurology 2011; 77 (5) 439-443
  • 80 Saidha S, Elamin M, Mullins G, Chaila E, Tormey VJ, Hennessy MJ. Treatment of progressive encephalomyelitis with rigidity and myoclonic jerks with rituximab: a case report. Eur J Neurol 2008; 15 (5) e33
  • 81 Clerinx K, Breban T, Schrooten M , et al. Progressive encephalomyelitis with rigidity and myoclonus: resolution after thymectomy. Neurology 2011; 76 (3) 303-304
  • 82 Suleiman J, Brilot F, Lang B, Vincent A, Dale RC. Autoimmune epilepsy in children: case series and proposed guidelines for identification. Epilepsia 2013; 54 (6) 1036-1045
  • 83 Dale RC, Brilot F, Fagan E, Earl J. Cerebrospinal fluid neopterin in paediatric neurology: a marker of active central nervous system inflammation. Dev Med Child Neurol 2009; 51 (4) 317-323
  • 84 Sinclair AJ, Wienholt L, Tantsis E, Brilot F, Dale RC. Clinical association of intrathecal and mirrored oligoclonal bands in paediatric neurology. Dev Med Child Neurol 2013; 55 (1) 71-75