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.
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(1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599–608
al Jishi F, al Kawi MZ, el Ramahi K, Omer S (1995) Hemichorea in systemic lupus erythematosus: significance of MRI findings. Lupus 4(4):321–323
al-Arfaj HF, Naddaf HO (1995) Cerebellar atrophy in systemic lupus erythematosus. Lupus 4(5):412–414
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):1316–1320
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):149–153
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):2187–2195
Appenzeller S, Cendes F, Costallat LT (2008) Cerebellar ataxia in systemic lupus erythematosus. Lupus 17(12):1122–1126
Appenzeller S, Yeh S, Maruyama M, Barros SM, de Carvalho JF (2012) Chorea in primary antiphospholipid syndrome is associated with rheumatic fever. Rheumatol Int 32:2857–2861
Asherson RA, Harris NE, Gharavi AE, Hughes GR (1986) Systemic lupus erythematosus, antiphospholipid antibodies, chorea, and oral contraceptives. Arthritis Rheum 29(12):1535–1536
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):253–259
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):947–953
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):206–213
Baizabal-Carvallo JF, Jankovic J (2012) Movement disorders in autoimmune diseases. Mov Disord 27(8):935–946
Baizabal-Carvallo JF, Alonso-Juarez M, Koslowski M (2011) Chorea in systemic lupus erythematosus. J Clin Rheumatol 17(2):69–72
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
Bardella D, Rossi ML, Temporin G (2002) Infantile cerebellar thrombosis: a case of lupus anticoagulants? Pediatr Med Chir 24(5):392–393
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):2074–2082
Bingisser R, Speich R, Fontana A, Gmur J, Vogel B, Landis T (1994) Lupus erythematosus and Miller-Fisher syndrome. Arch Neurol 51(8):828–830
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):797–804
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):833–841
Bruyn GW, Padberg G (1984) Chorea and systemic lupus erythematosus. A critical review. Eur Neurol 23(4):278–290
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):425–429
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):203–212
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):1019–1027
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):725–727
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):101–102
Chapman J, Cohen-Armon M, Shoenfeld Y, Korczyn AD (1999) Antiphospholipid antibodies permeabilize and depolarize brain synaptoneurosomes. Lupus 8(2):127–133
Collins KO, Comer JB (2003) Maternal haloperidol therapy associated with dyskinesia in a newborn. Am J Health Syst Pharm 60(21):2253–2255
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):522–528
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):1091–1098
de la Fuente-Fernandez R (1997) Lupus anticoagulant and chorea. Neurology 49(2):639–640
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):1189–1193
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):1367–1368
Donaldson IM, Espiner EA (1971) Disseminated lupus erythematosus presenting as chorea gravidarum. Arch Neurol 25(3):240–244
Dubois EL, Tuffanelli DL (1964) Clinical manifestations of systemic lupus erythematosus. Computer analysis of 520 cases. JAMA 190:104–111
Engelen M, Tijssen MA (2005) Paroxysmal non-kinesigenic dyskinesia in antiphospholipid syndrome. Mov Disord 20(1):111–113
Fabiani G, Teive HA, Germiniani FM, Sa DS, Werneck LC (2002) Reversible parkinsonian syndrome in systemic and brain vasculitis. Mov Disord 17(3):601–604
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):18569–18574
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):1265–1270
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):1175–1180
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):442–444
Furie R, Ishikawa T, Dhawan V, Eidelberg D (1994) Alternating hemichorea in primary antiphospholipid syndrome: evidence for contralateral striatal hypermetabolism. Neurology 44(11):2197–2199
Galanaud D, Dormont D, Marsault C, Wechsler B, Piette JC (2000) Brain MRI in patients with past lupus-associated chorea. Stroke 31(12):3079–3083
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):1329–1335
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):211–213
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):545–552
Girardi G, Redecha P, Salmon JE (2004) Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med 10(11):1222–1226
Goeb V, Dubreuil F, Cabre P, Jean-Baptiste G, Arfi S (2004) Lupus revealing itself after a stiff-person syndrome. Lupus 13(3):215
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):1578–1585
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):201–210
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):783–786
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):801–806
Harel L, Zecharia A, Straussberg R, Volovitz B, Amir J (2000) Successful treatment of rheumatic chorea with carbamazepine. Pediatric Neurol 23(2):147–151
Hodges JR (1987) Chorea and the lupus anticoagulant. J Neurol Neurosurg Psychiatry 50(3):368–369
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):1284–1287
Ishikawa N, Kobayashi M (2010) Recurrent acute cerebellar ataxia associated with anti-cardiolipin antibodies. Brain Dev 32(7):588–591
Iskander MK, Khan M (1989) Chorea as the initial presentation of oral contraceptive related systemic lupus erythematosus. J Rheumatol 16(6):850–851
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):1041–1051
Jankovic J (2009) Treatment of hyperkinetic movement disorders. Lancet Neurol 8(9):844–856
Jankovic J, Clarence-Smith K (2011) Tetrabenazine for the treatment of chorea and other hyperkinetic movement disorders. Expert Rev Neurother 11(11):1509–1523
Johnson RT, Richardson EP (1968) The neurological manifestations of systemic lupus erythematosus. Medicine (Baltimore) 47(4):337–369
Joseph FG, Lammie GA, Scolding NJ (2007) CNS lupus: a study of 41 patients. Neurology 69(7):644–654
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):284–286
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):496–499
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):272–279
Khubchandani RP, Viswanathan V, Desai J (2007) Unusual neurologic manifestations (I): Parkinsonism in juvenile SLE. Lupus 16(8):572–575
Kiechl-Kohlendorfer U, Ellemunter H, Kiechl S (1999) Chorea as the presenting clinical feature of primary antiphospholipid syndrome in childhood. Neuropediatrics 30(2):96–98
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):329–333
Kirk A, Harding SR (1993) Cardioembolic caudate infarction as a cause of hemichorea in lupus anticoagulant syndrome. Can J Neurol Sci 20(2):162–164
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):1247–1253
Krakauer M, Law I (2009) FDG PET brain imaging in neuropsychiatric systemic lupus erythematosis with choreic symptoms. Clin Nucl Med 34(2):122–123
Kranick SM, Mowry EM, Colcher A, Horn S, Golbe LI (2010) Movement disorders and pregnancy: a review of the literature. Mov Disord 25(6):665–671
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):688–690
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):59–63
Kwon SU, Koh JY, Kim JS (1999) Vertebrobasilar artery territory infarction as an initial manifestation of systemic lupus erythematosus. Clin Neurol Neurosurg 101(1):62–67
Kwong KL, Chu R, Wong SN (2000) Parkinsonism as unusual neurological complication in childhood systemic lupus erythematosus. Lupus 9(6):474–477
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):776–785
Lancaster E, Martinez-Hernandez E, Dalmau J (2011) Encephalitis and antibodies to synaptic and neuronal cell surface proteins. Neurology 77(2):179–189
Lancman ME, Pomeraniec C, Norscini J (1992) Magnetic resonance imaging findings in lupus ataxia. Acta Neurol Scand 86(4):425–426
Lauvsnes MB, Omdal R (2012) Systemic lupus erythematosus, the brain, and anti-NR2 antibodies. J Neurol 259(4):622–629
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):2145–2147
Lee PH, Joo US, Bang OY, Seo CH (2004) Basal ganglia hyperperfusion in a patient with systemic lupus erythematosus-related parkinsonism. Neurology 63(2):395–396
Levine JS, Branch DW, Rauch J (2002) The antiphospholipid syndrome. N Engl J Med 346(10):752–763
Lim SM, Oldfield M, Abbott RJ (1998) Systemic lupus erythematosus presenting with steroid-responsive parkinsonism and post-hemiplegic dystonia. Eur J Neurol 5(3):309–312
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):555–565
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):458–461
Manto MU, Rondeaux P, Jacquy J, Hildebrand JG (1996) Subacute pancerebellar syndrome associated with systemic lupus erythematosus. Clin Neurol Neurosurg 98(2):157–160
Martino D, Chew NK, Mir P, Edwards MJ, Quinn NP, Bhatia KP (2006) Atypical movement disorders in antiphospholipid syndrome. Mov Disord 21(7):944–949
Medaoud S, Lounici A, Zaibek A (2003) Parkinsonian syndrome during the systemic lupus erythematosus: a case report. Rev Med Interne 24(12):839–841
Meroni PL, Borghi MO, Raschi E, Tedesco F (2011) Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat Rev Rheumatol 7(6):330–339
Milanov I, Bogdanova D (2001) Antiphospholipid syndrome and dystonia-parkinsonism. A case report. Parkinsonism Relat Disord 7(2):139–141
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):128–131
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):295–306
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):199–201
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):391–393
Morris HR, Lees AJ (1999) Primary antiphospholipid syndrome presenting as a corticobasal degeneration syndrome. Mov Disord 14(3):530–532
Munhoz RP, Fameli H, Teive HA (2010) Stiff person syndrome as the initial manifestation of systemic lupus erythematosus. Mov Disord 25(4):516–517
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):382–388
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):436–438
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):324–327
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):392–398
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):367–369
Orzechowski NM, Wolanskyj AP, Ahlskog JE, Kumar N, Moder KG (2008) Antiphospholipid antibody-associated chorea. J Rheumatol 35(11):2165–2170
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):613–615
Poch G (1960) Enfermedades del colágeno. Manifestaciones neurológicas, musculares y psiquiátricas. López Libreros Editores SRL, Buenos Aires
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):967–970
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):120–131
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):2422–2427
Rey C, Koric L, Guedj E, Felician O, Kaphan E, Boucraut J, Ceccaldi M (2012) Striatal hypermetabolism in limbic encephalitis. J Neurol 259(6):1106–1110
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):116–118
Robert M, Sunitha R, Thulaseedharan NK (2006) Neuropsychiatric manifestations systemic lupus erythematosus: a study from South India. Neurol India 54(1):75–77
Sadeh M, Sarova-Pinhas I, Ohry A (1980) Sensory ataxia as an initial symptom of systemic lupus erythematosus. J Rheumatol 7(3):420–421
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):201–206
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):1897–1903
Seminario C, Pasano J (1930) Cuatro casos clínicos de lupus eritematoso agudo. Sem Med (B Air) 2:721–730
Shahar E, Goshen E, Tauber Z, Lahat E (1998) Parkinsonian syndrome complicating systemic lupus erythematosus. Pediatr Neurol 18(5):456–458
Shimomura T, Kuno N, Takenaka T, Maeda M, Takahashi K (1993) Purkinje cell antibody in lupus ataxia. Lancet 342(8867):375–376
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):436–442
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):736–743
Singer HS, Krumholz A, Giuliano J, Kiessling LS (1997) Antiphospholipid antibodies: an epiphenomenon in Tourette syndrome. Mov Disord 12(5):738–742
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):954–956
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):659–662
Sunden-Cullberg J, Tedroff J, Aquilonius SM (1998) Reversible chorea in primary antiphospholipid syndrome. Mov Disord 13(1):147–149
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):1271–1277
Tan EK, Chan LL, Auchus AP (2001) Reversible parkinsonism in systemic lupus erythematosus. J Neurol Sci 193(1):53–57
Tan KM, Lennon VA, Klein CJ, Boeve BF, Pittock SJ (2008) Clinical spectrum of voltage-gated potassium channel autoimmunity. Neurology 70(20):1883–1890
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):56–64
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):495–498
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):505–508
Tsokos GC (2011) Systemic lupus erythematosus. N Engl J Med 365(22):2110–2121
Tuchman AJ, Daras M, David S (1983) Cerebellar ataxia in systemic lupus erythematosus. N Y State J Med 83(7):983–984
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):1–11
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):199–201
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):625–630
Willoughby EO, Cardon L, Rubnitz ME (1964) Clinicopathologic conference: psychotic episodes, meningitis and chest pain. Postgrad Med 35:318–326
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):1813–1815
Yaginuma M, Suenaga M, Shiono Y, Sakamoto M (2000) Acute cerebellar ataxia of a patient with SLE. Clin Neurol Neurosurg 102(1):37–39
Yancey CL, Doughty RA, Athreya BH (1981) Central nervous system involvement in childhood systemic lupus erythematosus. Arthritis Rheum 24(11):1389–1395
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):613–619
Acknowledgments
CB is supported by the Czech Ministry of Education, research project MSM0021620849, Grantove agentury UK 441611 Charles University in Prague and IGA MZ ČR NT/12288-5/2011.
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Baizabal-Carvallo, J.F., Bonnet, C. & Jankovic, J. Movement disorders in systemic lupus erythematosus and the antiphospholipid syndrome. J Neural Transm 120, 1579–1589 (2013). https://doi.org/10.1007/s00702-013-1023-z
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DOI: https://doi.org/10.1007/s00702-013-1023-z