Journal of Neural Transmission

, Volume 120, Issue 11, pp 1579–1589 | Cite as

Movement disorders in systemic lupus erythematosus and the antiphospholipid syndrome

  • José Fidel Baizabal-Carvallo
  • Cecilia Bonnet
  • Joseph Jankovic
Neurology and Preclinical Neurological Studies - Review Article

Abstract

Movement disorders (MDs), particularly chorea, may be the presenting neurological complication of systemic lupus erythematosus (SLE) and the antiphospholipid syndrome (APS), but the association is not often initially recognized. Current evidence suggests an autoimmune mechanism related to antiphospholipid antibodies in these two conditions, although the antigenic target within the central nervous system has not yet been identified. Based on a comprehensive review of the literature, this article summarizes the current knowledge on MDs in SLE and APS. A high index of suspicion is required to make an early diagnosis and initiate appropriate treatment to provide symptomatic relief and to prevent other systemic complications related to the autoimmune process.

Keywords

Systemic lupus erythematosus Primary antiphospholipid syndrome Movement disorders Chorea Ataxia Parkinsonism 

References

  1. (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599–608Google Scholar
  2. al Jishi F, al Kawi MZ, el Ramahi K, Omer S (1995) Hemichorea in systemic lupus erythematosus: significance of MRI findings. Lupus 4(4):321–323PubMedGoogle Scholar
  3. al-Arfaj HF, Naddaf HO (1995) Cerebellar atrophy in systemic lupus erythematosus. Lupus 4(5):412–414PubMedGoogle Scholar
  4. Alcock R, Elsik M, Yiannikas C, Yiannikas J (2011) Antiphospholipid syndrome and rheumatic fever: a case spanning three decades of changing concepts and common immunological mechanisms. Lupus 20(12):1316–1320PubMedGoogle Scholar
  5. Angelini L, Zibordi F, Zorzi G, Nardocci N, Caporali R, Ravelli A, Martini A (1996) Neurological disorders, other than stroke, associated with antiphospholipid antibodies in childhood. Neuropediatrics 27(3):149–153PubMedGoogle Scholar
  6. Antonini A, Leenders KL, Vontobel P, Maguire RP, Missimer J, Psylla M, Gunther I (1997) Complementary PET studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson’s disease. Brain 120(Pt 12):2187–2195PubMedGoogle Scholar
  7. Appenzeller S, Cendes F, Costallat LT (2008) Cerebellar ataxia in systemic lupus erythematosus. Lupus 17(12):1122–1126PubMedGoogle Scholar
  8. Appenzeller S, Yeh S, Maruyama M, Barros SM, de Carvalho JF (2012) Chorea in primary antiphospholipid syndrome is associated with rheumatic fever. Rheumatol Int 32:2857–2861PubMedGoogle Scholar
  9. Asherson RA, Harris NE, Gharavi AE, Hughes GR (1986) Systemic lupus erythematosus, antiphospholipid antibodies, chorea, and oral contraceptives. Arthritis Rheum 29(12):1535–1536PubMedGoogle Scholar
  10. Asherson RA, Derksen RH, Harris EN, Bouma BN, Gharavi AE, Kater L, Hughes GR (1987) Chorea in systemic lupus erythematosus and “lupus-like” disease: association with antiphospholipid antibodies. Semin Arthritis Rheum 16(4):253–259PubMedGoogle Scholar
  11. Asherson RA, Gibson DG, Evans DW, Baguley E, Hughes GR (1988) Diagnostic and therapeutic problems in two patients with antiphospholipid antibodies, heart valve lesions, and transient ischaemic attacks. Ann Rheum Dis 47(11):947–953PubMedGoogle Scholar
  12. Avcin T, Benseler SM, Tyrrell PN, Cucnik S, Silverman ED (2008) A followup study of antiphospholipid antibodies and associated neuropsychiatric manifestations in 137 children with systemic lupus erythematosus. Arthritis Rheum 59(2):206–213PubMedGoogle Scholar
  13. Baizabal-Carvallo JF, Jankovic J (2012) Movement disorders in autoimmune diseases. Mov Disord 27(8):935–946PubMedGoogle Scholar
  14. Baizabal-Carvallo JF, Alonso-Juarez M, Koslowski M (2011) Chorea in systemic lupus erythematosus. J Clin Rheumatol 17(2):69–72PubMedGoogle Scholar
  15. Baizabal-Carvallo JF, Stocco A, Muscal E, Jankovic J (2013) The spectrum of movement disorders in children with anti-NMDR encephalitis. Mov Disord. doi:10.1002/mds.25354 PubMedGoogle Scholar
  16. Bardella D, Rossi ML, Temporin G (2002) Infantile cerebellar thrombosis: a case of lupus anticoagulants? Pediatr Med Chir 24(5):392–393PubMedGoogle Scholar
  17. Bertsias GK, Ioannidis JP, Aringer M, Bollen E, Bombardieri S, Bruce IN, Cervera R, Dalakas M, Doria A, Hanly JG, Huizinga TW, Isenberg D, Kallenberg C, Piette JC, Schneider M, Scolding N, Smolen J, Stara A, Tassiulas I, Tektonidou M, Tincani A, van Buchem MA, van Vollenhoven R, Ward M, Gordon C, Boumpas DT (2010) 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 Diseases 69(12):2074–2082Google Scholar
  18. Bingisser R, Speich R, Fontana A, Gmur J, Vogel B, Landis T (1994) Lupus erythematosus and Miller-Fisher syndrome. Arch Neurol 51(8):828–830PubMedGoogle Scholar
  19. Blank M, Krause I, Fridkin M, Keller N, Kopolovic J, Goldberg I, Tobar A, Shoenfeld Y (2002) Bacterial induction of autoantibodies to beta2-glycoprotein-I accounts for the infectious etiology of antiphospholipid syndrome. J Clin Invest 109(6):797–804PubMedGoogle Scholar
  20. Blank M, Krause I, Magrini L, Spina G, Kalil J, Jacobsen S, Thiesen HJ, Cunningham MW, Guilherme L, Shoenfeld Y (2006) Overlapping humoral autoimmunity links rheumatic fever and the antiphospholipid syndrome. Rheumatology (Oxford) 45(7):833–841Google Scholar
  21. Bruyn GW, Padberg G (1984) Chorea and systemic lupus erythematosus. A critical review. Eur Neurol 23(4):278–290PubMedGoogle Scholar
  22. Caronti B, Calderaro C, Alessandri C, Conti F, Tinghino R, Pini C, Palladini G, Valesini G (1998) Serum anti-beta2-glycoprotein I antibodies from patients with antiphospholipid antibody syndrome bind central nervous system cells. J Autoimmun 11(5):425–429PubMedGoogle Scholar
  23. Cervera R, Asherson RA, Font J, Tikly M, Pallares L, Chamorro A, Ingelmo M (1997) Chorea in the antiphospholipid syndrome. Clinical, radiologic, and immunologic characteristics of 50 patients from our clinics and the recent literature. Medicine (Baltimore) 76(3):203–212Google Scholar
  24. Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, Jacobsen S, Lakos G, Tincani A, Kontopoulou-Griva I, Galeazzi M, Meroni PL, Derksen RH, de Groot PG, Gromnica-Ihle E, Baleva M, Mosca M, Bombardieri S, Houssiau F, Gris JC, Quere I, Hachulla E, Vasconcelos C, Roch B, Fernandez-Nebro A, Boffa MC, Hughes GR, Ingelmo M (2002) Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 46(4):1019–1027PubMedGoogle Scholar
  25. Chacon J, Garcia-Moreno JM, Valencia J, Redondo L, Alegre S, Castro A, Perez G (1999) Parkinson disease of juvenile onset with systemic lupus erythematosus in a pre-symptomatic stage. Rev Neurol 29(8):725–727PubMedGoogle Scholar
  26. Chan AY, Li EK, Wong GL, Liu DT (2006) Cerebellum vasculopathy and normal tension glaucoma in systemic lupus erythematosus: report of a case and review of the literature. Rheumatol Int 27(1):101–102PubMedGoogle Scholar
  27. Chapman J, Cohen-Armon M, Shoenfeld Y, Korczyn AD (1999) Antiphospholipid antibodies permeabilize and depolarize brain synaptoneurosomes. Lupus 8(2):127–133PubMedGoogle Scholar
  28. Collins KO, Comer JB (2003) Maternal haloperidol therapy associated with dyskinesia in a newborn. Am J Health Syst Pharm 60(21):2253–2255PubMedGoogle Scholar
  29. Dale RC, Yin K, Ding A, Merheb V, Varadkhar S, McKay D, Singh-Grewal D, Brilot F (2011) Antibody binding to neuronal surface in movement disorders associated with lupus and antiphospholipid antibodies. Dev Med Child Neurol 53(6):522–528PubMedGoogle Scholar
  30. Dalmau J, Gleichman AJ, Hughes EG, Rossi JE, Peng X, Lai M, Dessain SK, Rosenfeld MR, Balice-Gordon R, Lynch DR (2008) Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol 7(12):1091–1098PubMedGoogle Scholar
  31. de la Fuente-Fernandez R (1997) Lupus anticoagulant and chorea. Neurology 49(2):639–640PubMedGoogle Scholar
  32. DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B (2001) A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 7(11):1189–1193PubMedGoogle Scholar
  33. Diniz RE, Goldenberg J, Andrade LE, Leser PG, Silva NP, Roizenblatt S, Hilario MO (1994) Antiphospholipid antibodies in rheumatic fever chorea. J Rheumatol 21(7):1367–1368PubMedGoogle Scholar
  34. Donaldson IM, Espiner EA (1971) Disseminated lupus erythematosus presenting as chorea gravidarum. Arch Neurol 25(3):240–244PubMedGoogle Scholar
  35. Dubois EL, Tuffanelli DL (1964) Clinical manifestations of systemic lupus erythematosus. Computer analysis of 520 cases. JAMA 190:104–111PubMedGoogle Scholar
  36. Engelen M, Tijssen MA (2005) Paroxysmal non-kinesigenic dyskinesia in antiphospholipid syndrome. Mov Disord 20(1):111–113PubMedGoogle Scholar
  37. Fabiani G, Teive HA, Germiniani FM, Sa DS, Werneck LC (2002) Reversible parkinsonian syndrome in systemic and brain vasculitis. Mov Disord 17(3):601–604PubMedGoogle Scholar
  38. Faust TW, Chang EH, Kowal C, Berlin R, Gazaryan IG, Bertini E, Zhang J, Sanchez-Guerrero J, Fragoso-Loyo HE, Volpe BT, Diamond B, Huerta PT (2010) Neurotoxic lupus autoantibodies alter brain function through two distinct mechanisms. Proc Natl Acad Sci USA 107(43):18569–18574PubMedGoogle Scholar
  39. Feigin A, Antonini A, Fukuda M, De Notaris R, Benti R, Pezzoli G, Mentis MJ, Moeller JR, Eidelberg D (2002) Tc-99m ethylene cysteinate dimer SPECT in the differential diagnosis of parkinsonism. Mov Disord 17(6):1265–1270PubMedGoogle Scholar
  40. Figueroa F, Berrios X, Gutierrez M, Carrion F, Goycolea JP, Riedel I, Jacobelli S (1992) Anticardiolipin antibodies in acute rheumatic fever. J Rheumatol 19(8):1175–1180PubMedGoogle Scholar
  41. Franco Sorolla JM, Povar MJ, Montori Lasilla M, Vidal Fernández AI, López Lancis A, Velilla Marco J, Portolés Suso A (1992) Cerebellar syndrome as first manifestation of late onset systemic lupus erythematosus. An Med Interna 9(9):442–444PubMedGoogle Scholar
  42. Furie R, Ishikawa T, Dhawan V, Eidelberg D (1994) Alternating hemichorea in primary antiphospholipid syndrome: evidence for contralateral striatal hypermetabolism. Neurology 44(11):2197–2199PubMedGoogle Scholar
  43. Galanaud D, Dormont D, Marsault C, Wechsler B, Piette JC (2000) Brain MRI in patients with past lupus-associated chorea. Stroke 31(12):3079–3083PubMedGoogle Scholar
  44. Garcia-Moreno JM, Chacon J (2002) Juvenile parkinsonism as a manifestation of systemic lupus erythematosus: case report and review of the literature. Mov Disord 17(6):1329–1335PubMedGoogle Scholar
  45. Gelosa G, Tremolizzo L, Galbussera A, Perego R, Capra M, Frigo M, Apale P, Ferrarese C, Appollonio I (2009) Narrowing the window for ‘senile chorea’: a case with primary antiphospholipid syndrome. J Neurol Sci 284(1–2):211–213PubMedGoogle Scholar
  46. Gharavi AE, Pierangeli SS, Espinola RG, Liu X, Colden-Stanfield M, Harris EN (2002) Antiphospholipid antibodies induced in mice by immunization with a cytomegalovirus-derived peptide cause thrombosis and activation of endothelial cells in vivo. Arthritis Rheum 46(2):545–552PubMedGoogle Scholar
  47. Girardi G, Redecha P, Salmon JE (2004) Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med 10(11):1222–1226PubMedGoogle Scholar
  48. Goeb V, Dubreuil F, Cabre P, Jean-Baptiste G, Arfi S (2004) Lupus revealing itself after a stiff-person syndrome. Lupus 13(3):215PubMedGoogle Scholar
  49. Gono T, Kawaguchi Y, Kaneko H, Nishimura K, Hanaoka M, Kataoka S, Okamoto Y, Katsumata Y, Yamanaka H (2011) Anti-NR2A antibody as a predictor for neuropsychiatric systemic lupus erythematosus. Rheumatology (Oxford) 50(9):1578–1585Google Scholar
  50. Guttman M, Lang AE, Garnett ES, Nahmias C, Firnau G, Tyndel FJ, Gordon AS (1987) Regional cerebral glucose metabolism in SLE chorea: further evidence that striatal hypometabolism is not a correlate of chorea. Mov Disord 2(3):201–210PubMedGoogle Scholar
  51. Hanajima R, Ugawa Y, Terao Y, Furubayashi T, Machii K, Shiio Y, Enomoto H, Uesugi H, Mochizuki H, Kanazawa I (1999) Intracortical inhibition of the motor cortex is normal in chorea. J Neurol Neurosurg Psychiatry 66(6):783–786PubMedGoogle Scholar
  52. Hanyuda M, Yoda Y, Shiozawa T, Hanaoka R, Miwa Y, Kaga S, Kasama T, Negishi M, Ide H (2002) A case with systemic lupus erythematosus presenting with reversible edematous lesion in cerebellum. Ryumachi 42(5):801–806PubMedGoogle Scholar
  53. Harel L, Zecharia A, Straussberg R, Volovitz B, Amir J (2000) Successful treatment of rheumatic chorea with carbamazepine. Pediatric Neurol 23(2):147–151Google Scholar
  54. Hodges JR (1987) Chorea and the lupus anticoagulant. J Neurol Neurosurg Psychiatry 50(3):368–369PubMedGoogle Scholar
  55. Hosokawa S, Ichiya Y, Kuwabara Y, Ayabe Z, Mitsuo K, Goto I, Kato M (1987) Positron emission tomography in cases of chorea with different underlying diseases. J Neurol Neurosurg Psychiatry 50(10):1284–1287PubMedGoogle Scholar
  56. Ishikawa N, Kobayashi M (2010) Recurrent acute cerebellar ataxia associated with anti-cardiolipin antibodies. Brain Dev 32(7):588–591PubMedGoogle Scholar
  57. Iskander MK, Khan M (1989) Chorea as the initial presentation of oral contraceptive related systemic lupus erythematosus. J Rheumatol 16(6):850–851PubMedGoogle Scholar
  58. Jacob A, Hack B, Chen P, Quigg RJ, Alexander JJ (2011) C5a/CD88 signaling alters blood–brain barrier integrity in lupus through nuclear factor-kappaB. J Neurochem 119(5):1041–1051PubMedGoogle Scholar
  59. Jankovic J (2009) Treatment of hyperkinetic movement disorders. Lancet Neurol 8(9):844–856PubMedGoogle Scholar
  60. Jankovic J, Clarence-Smith K (2011) Tetrabenazine for the treatment of chorea and other hyperkinetic movement disorders. Expert Rev Neurother 11(11):1509–1523PubMedGoogle Scholar
  61. Johnson RT, Richardson EP (1968) The neurological manifestations of systemic lupus erythematosus. Medicine (Baltimore) 47(4):337–369Google Scholar
  62. Joseph FG, Lammie GA, Scolding NJ (2007) CNS lupus: a study of 41 patients. Neurology 69(7):644–654PubMedGoogle Scholar
  63. Kashihara K, Nakashima S, Kohira I, Shohmori T, Fujiwara Y, Kuroda S (1998) Hyperintense basal ganglia on T1-weighted MR images in a patient with central nervous system lupus and chorea. AJNR Am J Neuroradiol 19(2):284–286PubMedGoogle Scholar
  64. Katzav A, Pick CG, Korczyn AD, Oest E, Blank M, Shoenfeld Y, Chapman J (2001) Hyperactivity in a mouse model of the antiphospholipid syndrome. Lupus 10(7):496–499PubMedGoogle Scholar
  65. Katzav A, Faust-Socher A, Kvapil F, Michaelson DM, Blank M, Pick CG, Shoenfeld Y, Korczyn AD, Chapman J (2011) Antiphospholipid syndrome induction exacerbates a transgenic Alzheimer disease model on a female background. Neurobiol Aging 32(2):272–279PubMedGoogle Scholar
  66. Khubchandani RP, Viswanathan V, Desai J (2007) Unusual neurologic manifestations (I): Parkinsonism in juvenile SLE. Lupus 16(8):572–575PubMedGoogle Scholar
  67. Kiechl-Kohlendorfer U, Ellemunter H, Kiechl S (1999) Chorea as the presenting clinical feature of primary antiphospholipid syndrome in childhood. Neuropediatrics 30(2):96–98PubMedGoogle Scholar
  68. Kim JS, Lee KS, Lee KH, Kim YI, Kim BS, Chung YA, Chung SK (2002) Evidence of thalamic disinhibition in patients with hemichorea: semiquantitative analysis using SPECT. J Neurol Neurosurg Psychiatry 72(3):329–333PubMedGoogle Scholar
  69. Kirk A, Harding SR (1993) Cardioembolic caudate infarction as a cause of hemichorea in lupus anticoagulant syndrome. Can J Neurol Sci 20(2):162–164PubMedGoogle Scholar
  70. Kovacs JA, Urowitz MB, Gladman DD, Zeman R (1995) The use of single photon emission computerized tomography in neuropsychiatric SLE: a pilot study. J Rheumatol 22(7):1247–1253PubMedGoogle Scholar
  71. Krakauer M, Law I (2009) FDG PET brain imaging in neuropsychiatric systemic lupus erythematosis with choreic symptoms. Clin Nucl Med 34(2):122–123PubMedGoogle Scholar
  72. Kranick SM, Mowry EM, Colcher A, Horn S, Golbe LI (2010) Movement disorders and pregnancy: a review of the literature. Mov Disord 25(6):665–671PubMedGoogle Scholar
  73. Kunas RC, McRae A, Kesselring J, Villiger PM (1995) Antidopaminergic antibodies in a patient with a complex autoimmune disorder and rapidly progressing Parkinson’s disease. J Allergy Clin Immunol 96(5 Pt 1):688–690PubMedGoogle Scholar
  74. Kuroe K, Kurahashi K, Nakano I, Morimatsu Y, Takemori H (1994) A neuropathological study of a case of lupus erythematosus with chorea. J Neurol Sci 123(1–2):59–63PubMedGoogle Scholar
  75. Kwon SU, Koh JY, Kim JS (1999) Vertebrobasilar artery territory infarction as an initial manifestation of systemic lupus erythematosus. Clin Neurol Neurosurg 101(1):62–67PubMedGoogle Scholar
  76. Kwong KL, Chu R, Wong SN (2000) Parkinsonism as unusual neurological complication in childhood systemic lupus erythematosus. Lupus 9(6):474–477PubMedGoogle Scholar
  77. Lai M, Huijbers MG, Lancaster E, Graus F, Bataller L, Balice-Gordon R, Cowell JK, Dalmau J (2010) Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol 9(8):776–785PubMedGoogle Scholar
  78. Lancaster E, Martinez-Hernandez E, Dalmau J (2011) Encephalitis and antibodies to synaptic and neuronal cell surface proteins. Neurology 77(2):179–189PubMedGoogle Scholar
  79. Lancman ME, Pomeraniec C, Norscini J (1992) Magnetic resonance imaging findings in lupus ataxia. Acta Neurol Scand 86(4):425–426PubMedGoogle Scholar
  80. Lauvsnes MB, Omdal R (2012) Systemic lupus erythematosus, the brain, and anti-NR2 antibodies. J Neurol 259(4):622–629PubMedGoogle Scholar
  81. Lazurova I, Macejova Z, Benhatchi K, Oetterova M, Antolova E, Asherson RA, Rovensky J (2007) Efficacy of intravenous immunoglobulin treatment in lupus erythematosus chorea. Clin Rheumatol 26(12):2145–2147PubMedGoogle Scholar
  82. Lee PH, Joo US, Bang OY, Seo CH (2004) Basal ganglia hyperperfusion in a patient with systemic lupus erythematosus-related parkinsonism. Neurology 63(2):395–396PubMedGoogle Scholar
  83. Levine JS, Branch DW, Rauch J (2002) The antiphospholipid syndrome. N Engl J Med 346(10):752–763PubMedGoogle Scholar
  84. Lim SM, Oldfield M, Abbott RJ (1998) Systemic lupus erythematosus presenting with steroid-responsive parkinsonism and post-hemiplegic dystonia. Eur J Neurol 5(3):309–312PubMedGoogle Scholar
  85. Liu B, Dluzen DE (2007) Oestrogen and nigrostriatal dopaminergic neurodegeneration: animal models and clinical reports of Parkinson’s disease. Clin Exp Pharmacol Physiol 34(7):555–565PubMedGoogle Scholar
  86. Maia DP, Fonseca PG, Camargos ST, Pfannes C, Cunningham MC, Cardoso F (2012) Pregnancy in patients with Sydenham’s Chorea. Parkinsonism Relat Disord 18(5):458–461PubMedGoogle Scholar
  87. Manto MU, Rondeaux P, Jacquy J, Hildebrand JG (1996) Subacute pancerebellar syndrome associated with systemic lupus erythematosus. Clin Neurol Neurosurg 98(2):157–160PubMedGoogle Scholar
  88. Martino D, Chew NK, Mir P, Edwards MJ, Quinn NP, Bhatia KP (2006) Atypical movement disorders in antiphospholipid syndrome. Mov Disord 21(7):944–949PubMedGoogle Scholar
  89. Medaoud S, Lounici A, Zaibek A (2003) Parkinsonian syndrome during the systemic lupus erythematosus: a case report. Rev Med Interne 24(12):839–841PubMedGoogle Scholar
  90. Meroni PL, Borghi MO, Raschi E, Tedesco F (2011) Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat Rev Rheumatol 7(6):330–339PubMedGoogle Scholar
  91. Milanov I, Bogdanova D (2001) Antiphospholipid syndrome and dystonia-parkinsonism. A case report. Parkinsonism Relat Disord 7(2):139–141PubMedGoogle Scholar
  92. Mimenza-Alvarado AJ, Tellez-Zenteno JF, Cantu-Brito C, Garcia-Ramos G (2002) Systemic lupus erythematosus with affection to brainstem: report of three cases. Rev Neurol 35(2):128–131PubMedGoogle Scholar
  93. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, De Groot PG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA (2006) International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 4(2):295–306PubMedGoogle Scholar
  94. Miyoshi Y, Atsumi T, Kitagawa H, Ogura N, Amasaki Y, Tsutsumi A, Ohnishi K, Fujisaku A, Sagawa A, Koike T (1993) Parkinson-like symptoms as a manifestation of systemic lupus erythematosus. Lupus 2(3):199–201PubMedGoogle Scholar
  95. Morales-Buenrostro LE, Tellez-Zenteno JF, Estanol B (2002) Symptomatic hemiparkinsonism with abnormal SPECT in a patient with systemic lupus erythematosus (SLE). Neurologia 17(7):391–393PubMedGoogle Scholar
  96. Morris HR, Lees AJ (1999) Primary antiphospholipid syndrome presenting as a corticobasal degeneration syndrome. Mov Disord 14(3):530–532PubMedGoogle Scholar
  97. Munhoz RP, Fameli H, Teive HA (2010) Stiff person syndrome as the initial manifestation of systemic lupus erythematosus. Mov Disord 25(4):516–517PubMedGoogle Scholar
  98. Nagaoka S, Kato K, Ishigatsubo Y, Chiba J, Sakamoto H, Nose K, Tani K, Okubo T (1984) A case of systemic lupus erythematosus with akinesia, muscle rigidity and neurogenic bladder. Ryumachi 24(5):382–388PubMedGoogle Scholar
  99. Nectoux F, Euller-Ziegler L, Grisot C, Quaranta JF, Duplay H, Ziegler G (1992) Lupus chorea revealing. Study in magnetic resonance imaging. Success of plasma exchanges after resistance to pulsed cortisone. Rev Rhum Mal Osteoartic 59(6):436–438PubMedGoogle Scholar
  100. Nordal EB, Nielsen J, Marhaug G (1999) Chorea in juvenile primary antiphospholipid syndrome. Reversible decreased circulation in the basal ganglia visualised by single photon emission computed tomography. Scand J Rheumatol 28(5):324–327PubMedGoogle Scholar
  101. Omdal R, Brokstad K, Waterloo K, Koldingsnes W, Jonsson R, Mellgren SI (2005) Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur J Neurol 12(5):392–398PubMedGoogle Scholar
  102. Orta Daniel SJ, Ulises RO (2008) Stroke of the substance nigra and parkinsonism as first manifestation of systemic lupus erythematosus. Parkinsonism Relat Disord 14(4):367–369PubMedGoogle Scholar
  103. Orzechowski NM, Wolanskyj AP, Ahlskog JE, Kumar N, Moder KG (2008) Antiphospholipid antibody-associated chorea. J Rheumatol 35(11):2165–2170PubMedGoogle Scholar
  104. Osawa H, Yamabe H, Kaizuka M, Tamura N, Tsunoda S, Shirato KI, Okumura K (1997) Systemic lupus erythematosus associated with transverse myelitis and parkinsonian symptoms. Lupus 6(7):613–615PubMedGoogle Scholar
  105. Poch G (1960) Enfermedades del colágeno. Manifestaciones neurológicas, musculares y psiquiátricas. López Libreros Editores SRL, Buenos AiresGoogle Scholar
  106. Rafai MA, El Moutawakil B, Gam I, Hakim K, Fadel H, Kissani N, Slassi I (2005) Systemic lupus erythematosus presenting with a choreo-athetosic syndrome associated with antiphospholipid antibodies. Revue Neurol (Paris) 161(10):967–970Google Scholar
  107. Ramesh S, Morrell CN, Tarango C, Thomas GD, Yuhanna IS, Girardi G, Herz J, Urbanus RT, de Groot PG, Thorpe PE, Salmon JE, Shaul PW, Mineo C (2011) Antiphospholipid antibodies promote leukocyte–endothelial cell adhesion and thrombosis in mice by antagonizing eNOS via beta2GPI and apoER2. J Clin Invest 121(1):120–131PubMedGoogle Scholar
  108. Reiner P, Galanaud D, Leroux G, Vidailhet M, Haroche J, du Huong LT, Frances C, Papo T, de Gennes C, Musset L, Wechsler B, Amoura Z, Piette JC, Costedoat-Chalumeau N (2011) Long-term outcome of 32 patients with chorea and systemic lupus erythematosus or antiphospholipid antibodies. Mov Disord 26(13):2422–2427PubMedGoogle Scholar
  109. Rey C, Koric L, Guedj E, Felician O, Kaphan E, Boucraut J, Ceccaldi M (2012) Striatal hypermetabolism in limbic encephalitis. J Neurol 259(6):1106–1110PubMedGoogle Scholar
  110. Riccio A, Andreassi C, Eboli ML (1998) Antiphospholipid antibodies bind to rat cerebellar granule cells: the role of N-methyl-d-aspartate receptors. Neurosci Lett 257(2):116–118PubMedGoogle Scholar
  111. Robert M, Sunitha R, Thulaseedharan NK (2006) Neuropsychiatric manifestations systemic lupus erythematosus: a study from South India. Neurol India 54(1):75–77PubMedGoogle Scholar
  112. Sadeh M, Sarova-Pinhas I, Ohry A (1980) Sensory ataxia as an initial symptom of systemic lupus erythematosus. J Rheumatol 7(3):420–421PubMedGoogle Scholar
  113. Santos MJ, Reis P, da Silva JA, de Queiroz MV (1994) Ischemic lesion of the CNS in patients with systemic lupus erythematosus. Acta Med Port 7(4):201–206PubMedGoogle Scholar
  114. Schultz KN, von Esenwein SA, Hu M, Bennett AL, Kennedy RT, Musatov S, Toran-Allerand CD, Kaplitt MG, Young LJ, Becker JB (2009) Viral vector-mediated overexpression of estrogen receptor-alpha in striatum enhances the estradiol-induced motor activity in female rats and estradiol-modulated GABA release. J Neurosci 29(6):1897–1903PubMedGoogle Scholar
  115. Seminario C, Pasano J (1930) Cuatro casos clínicos de lupus eritematoso agudo. Sem Med (B Air) 2:721–730Google Scholar
  116. Shahar E, Goshen E, Tauber Z, Lahat E (1998) Parkinsonian syndrome complicating systemic lupus erythematosus. Pediatr Neurol 18(5):456–458PubMedGoogle Scholar
  117. Shimomura T, Kuno N, Takenaka T, Maeda M, Takahashi K (1993) Purkinje cell antibody in lupus ataxia. Lancet 342(8867):375–376PubMedGoogle Scholar
  118. Shoenfeld Y, Nahum A, Korczyn AD, Dano M, Rabinowitz R, Beilin O, Pick CG, Leider-Trejo L, Kalashnikova L, Blank M, Chapman J (2003) Neuronal-binding antibodies from patients with antiphospholipid syndrome induce cognitive deficits following intrathecal passive transfer. Lupus 12(6):436–442PubMedGoogle Scholar
  119. Shrot S, Katzav A, Korczyn AD, Litvinju Y, Hershenson R, Pick CG, Blank M, Zaech J, Shoenfeld Y, Sirota P, Chapman J (2002) Behavioral and cognitive deficits occur only after prolonged exposure of mice to antiphospholipid antibodies. Lupus 11(11):736–743PubMedGoogle Scholar
  120. Singer HS, Krumholz A, Giuliano J, Kiessling LS (1997) Antiphospholipid antibodies: an epiphenomenon in Tourette syndrome. Mov Disord 12(5):738–742PubMedGoogle Scholar
  121. Singh RR, Prasad K, Kumar A, Misra A, Padmakumar K, Malaviya AN (1988) Cerebellar ataxia in systemic lupus erythematosus: three case reports. Ann Rheum Dis 47(11):954–956PubMedGoogle Scholar
  122. Song CH, Oftadeh LC, Oh C, Louie J, Yu KT (1997) Successful treatment of steroid-resistant chorea associated with lupus by use of valproic acid and clonidine-HCL patch. Clin Pediatr (Phila) 36(11):659–662Google Scholar
  123. Sunden-Cullberg J, Tedroff J, Aquilonius SM (1998) Reversible chorea in primary antiphospholipid syndrome. Mov Disord 13(1):147–149PubMedGoogle Scholar
  124. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25(11):1271–1277PubMedGoogle Scholar
  125. Tan EK, Chan LL, Auchus AP (2001) Reversible parkinsonism in systemic lupus erythematosus. J Neurol Sci 193(1):53–57PubMedGoogle Scholar
  126. Tan KM, Lennon VA, Klein CJ, Boeve BF, Pittock SJ (2008) Clinical spectrum of voltage-gated potassium channel autoimmunity. Neurology 70(20):1883–1890PubMedGoogle Scholar
  127. Tanne D, Katzav A, Beilin O, Grigoriadis NC, Blank M, Pick CG, Landenberg P, Shoenfeld Y, Chapman J (2008) Interaction of inflammation, thrombosis, aspirin and enoxaparin in CNS experimental antiphospholipid syndrome. Neurobiol Dis 30(1):56–64PubMedGoogle Scholar
  128. Toren P, Toren A, Weizman A, Mozes T, Eldar S, Magor A, Mandel M, Rechavi G, Many A, Mester R (1994) Tourette’s disorder: is there an association with the antiphospholipid syndrome? Biol Psychiatry 35(7):495–498PubMedGoogle Scholar
  129. Tsai MH, Lu CS, Chen CJ, Tsai WP, Liou LB (2002) Extrapontine myelinolysis in a patient with systemic lupus erythematosus: a case report. J Formos Med Assoc 101(7):505–508PubMedGoogle Scholar
  130. Tsokos GC (2011) Systemic lupus erythematosus. N Engl J Med 365(22):2110–2121PubMedGoogle Scholar
  131. Tuchman AJ, Daras M, David S (1983) Cerebellar ataxia in systemic lupus erythematosus. N Y State J Med 83(7):983–984PubMedGoogle Scholar
  132. Unterman A, Nolte JE, Boaz M, Abady M, Shoenfeld Y, Zandman-Goddard G (2011) Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum 41(1):1–11PubMedGoogle Scholar
  133. Venegoni E, Biasioli R, Lamperti E, Rinaldi E, Salmaggi A, Novi C (1994) Tremor as an early manifestation of systemic lupus erythematosus. Clin Exp Rheumatol 12(2):199–201PubMedGoogle Scholar
  134. Vernino S, Tuite P, Adler CH, Meschia JF, Boeve BF, Boasberg P, Parisi JE, Lennon VA (2002) Paraneoplastic chorea associated with CRMP-5 neuronal antibody and lung carcinoma. Ann Neurol 51(5):625–630PubMedGoogle Scholar
  135. Willoughby EO, Cardon L, Rubnitz ME (1964) Clinicopathologic conference: psychotic episodes, meningitis and chest pain. Postgrad Med 35:318–326PubMedGoogle Scholar
  136. Wu SW, Graham B, Gelfand MJ, Gruppo RE, Dinopolous A, Gilbert DL (2007) Clinical and positron emission tomography findings of chorea associated with primary antiphospholipid antibody syndrome. Mov Disord 22(12):1813–1815PubMedGoogle Scholar
  137. Yaginuma M, Suenaga M, Shiono Y, Sakamoto M (2000) Acute cerebellar ataxia of a patient with SLE. Clin Neurol Neurosurg 102(1):37–39PubMedGoogle Scholar
  138. Yancey CL, Doughty RA, Athreya BH (1981) Central nervous system involvement in childhood systemic lupus erythematosus. Arthritis Rheum 24(11):1389–1395PubMedGoogle Scholar
  139. Ziporen L, Shoenfeld Y, Levy Y, Korczyn AD (1997) Neurological dysfunction and hyperactive behavior associated with antiphospholipid antibodies. A mouse model. J Clin Invest 100(3):613–619PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • José Fidel Baizabal-Carvallo
    • 1
  • Cecilia Bonnet
    • 2
  • Joseph Jankovic
    • 1
  1. 1.Parkinson’s Disease Center and Movement Disorders Clinic, Department of NeurologyBaylor College of MedicineHoustonUSA
  2. 2.Department of Neurology, 1st Faculty of Medicine, General University HospitalCharles University in PraguePragueCzech Republic

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