Antiphospholipid Antibodies: Neuropsychiatric Presentations

Abstract

Antiphospholipid antibodies (aPL) are associated with a wide range of neurological, psychological, and psychiatric manifestations. In addition to clearly delineated purely thrombotic manifestations, which define the neurological contribution to the antiphospholipid syndrome, the strength of the other described associations is highly variable, and the underlying pathophysiological mechanisms are not fully understood. Some indications seem to support a psychiatric impact of aPL. The magnitude of the association and cellular and molecular mechanisms involved need to be further elucidated.

Keywords

antiphospholipid antibodies - neurology - psychiatry

• References

• 1 Asherson RA, Khamashta MA, Ordi-Ros J , et al. The “primary” antiphospholipid syndrome: major clinical and serological features. Medicine (Baltimore) 1989; 68 (6) 366-374
• 2 Wilson WA, Gharavi AE, Koike T , et al. International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: report of an international workshop. Arthritis Rheum 1999; 42 (7) 1309-1311
• 3 McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: beta 2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci U S A 1990; 87 (11) 4120-4124
• 4 Galli M, Comfurius P, Maassen C , et al. Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet 1990; 335 (8705) 1544-1547
• 5 Miyakis S, Lockshin MD, Atsumi T , et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006; 4 (2) 295-306
• 6 Bevers EM, Galli M, Barbui T, Comfurius P, Zwaal RF. Lupus anticoagulant IgG's (LA) are not directed to phospholipids only, but to a complex of lipid-bound human prothrombin. Thromb Haemost 1991; 66 (6) 629-632
• 7 Lieby P, Poindron V, Roussi S , et al. Pathogenic antiphospholipid antibody: an antigen-selected needle in a haystack. Blood 2004; 104 (6) 1711-1715
• 8 Hughes GR. Thrombosis, abortion, cerebral disease, and the lupus anticoagulant. Br Med J (Clin Res Ed) 1983; 287 (6399) 1088-1089
• 9 Muscal E, Brey RL. Antiphospholipid syndrome and the brain in pediatric and adult patients. Lupus 2010; 19 (4) 406-411
• 10 Brey RL, Muscal E, Chapman J. Antiphospholipid antibodies and the brain: a consensus report. Lupus 2011; 20 (2) 153-157
• 11 Molad Y, Sidi Y, Gornish M, Lerner M, Pinkhas J, Weinberger A. Lupus anticoagulant: correlation with magnetic resonance imaging of brain lesions. J Rheumatol 1992; 19 (4) 556-561
• 12 Provenzale JM, Barboriak DP, Allen NB, Ortel TL. Patients with antiphospholipid antibodies: CT and MR findings of the brain. AJR Am J Roentgenol 1996; 167 (6) 1573-1578
• 13 Sanna G, Bertolaccini ML, Cuadrado MJ , et al. Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies. J Rheumatol 2003; 30 (5) 985-992
• 14 Tektonidou MG, Varsou N, Kotoulas G, Antoniou A, Moutsopoulos HM. Cognitive deficits in patients with antiphospholipid syndrome: association with clinical, laboratory, and brain magnetic resonance imaging findings. Arch Intern Med 2006; 166 (20) 2278-2284
• 15 Katzav A, Shoenfeld Y, Chapman J. The pathogenesis of neural injury in animal models of the antiphospholipid syndrome. Clin Rev Allergy Immunol 2010; 38 (2–3) 196-200
• 16 Nowacki P, Ronin-Walknowska E, Ossowicka-Stepińska J. Central nervous system involvement in pregnant rabbits with experimental model of antiphospholipid syndrome. Folia Neuropathol 1998; 36 (1) 38-44
• 17 Nowacki P, Ronin-Walknowska E, Ossowicka-Stepińska J. Neuropathological changes within the brain of rabbits with experimental model of antiphospholipid syndrome in different time after immunization. Folia Neuropathol 1999; 37 (4) 269-272
• 18 Nowacki P, Ossowicka-Stepińska J, Ronin-Walkanowska E, Tabaka J. The antiphospholipid syndrome in pregnant rabbits and their offspring. Neuropathological aspects. Folia Neuropathol 2005; 43 (1) 15-22
• 19 Ziporen L, Polak-Charcon S, Korczyn DA , et al. Neurological dysfunction associated with antiphospholipid syndrome: histopathological brain findings of thrombotic changes in a mouse model. Clin Dev Immunol 2004; 11 (1) 67-75
• 20 Tanne D, Katzav A, Beilin O , et al. Interaction of inflammation, thrombosis, aspirin and enoxaparin in CNS experimental antiphospholipid syndrome. Neurobiol Dis 2008; 30 (1) 56-64
• 21 de Castro Ribeiro M, Badaut J, Price M , et al. Thrombin in ischemic neuronal death. Exp Neurol 2006; 198 (1) 199-203
• 22 Maggio N, Shavit E, Chapman J, Segal M. Thrombin induces long-term potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: toward understanding the functional consequences of cerebrovascular insults. J Neurosci 2008; 28 (3) 732-736
• 23 Xue M, Del Bigio MR. Acute tissue damage after injections of thrombin and plasmin into rat striatum. Stroke 2001; 32 (9) 2164-2169
• 24 Beilin O, Gurwitz D, Korczyn AD, Chapman J. Quantitative measurements of mouse brain thrombin-like and thrombin inhibition activities. Neuroreport 2001; 12 (11) 2347-2351
• 25 Beilin O, Karussis DM, Korczyn AD , et al. Increased thrombin inhibition in experimental autoimmune encephalomyelitis. J Neurosci Res 2005; 79 (3) 351-359
• 26 Beilin O, Karussis DM, Korczyn AD , et al. Increased KPI containing amyloid precursor protein in experimental autoimmune encephalomyelitis brains. Neuroreport 2007; 18 (6) 581-584
• 27 Caronti B, Calderaro C, Alessandri C , et al. Serum anti-beta2-glycoprotein I antibodies from patients with antiphospholipid antibody syndrome bind central nervous system cells. J Autoimmun 1998; 11 (5) 425-429
• 28 Caronti B, Pittoni V, Palladini G, Valesini G. Anti-beta 2-glycoprotein I antibodies bind to central nervous system. J Neurol Sci 1998; 156 (2) 211-219
• 29 Tang SC, Arumugam TV, Xu X , et al. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A 2007; 104 (34) 13798-13803
• 30 Myant NB. Reelin and apolipoprotein E receptor 2 in the embryonic and mature brain: effects of an evolutionary change in the apoER2 gene. Proc Biol Sci 2010; 277 (1680) 345-351
• 31 Chapman J, Cohen-Armon M, Shoenfeld Y, Korczyn AD. Antiphospholipid antibodies permeabilize and depolarize brain synaptoneurosomes. Lupus 1999; 8 (2) 127-133
• 32 Kent M, Alvarez F, Vogt E, Fyffe R, Ng AK, Rote N. Monoclonal antiphosphatidylserine antibodies react directly with feline and murine central nervous system. J Rheumatol 1997; 24 (9) 1725-1733
• 33 Kent MN, Alvarez FJ, Ng AK, Rote NS. Ultrastructural localization of monoclonal antiphospholipid antibody binding to rat brain. Exp Neurol 2000; 163 (1) 173-179
• 34 Meroni PL, Borghi MO, Raschi E, Tedesco F. Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat Rev Rheumatol 2011; 7 (6) 330-339
• 35 Aronovich R, Gurwitz D, Kloog Y, Chapman J. Antiphospholipid antibodies, thrombin and LPS activate brain endothelial cells and Ras-dependent pathways through distinct mechanisms. Immunobiology 2005; 210 (10) 781-788
• 36 Todorova M, Baleva M. Some recent insights into the prothrombogenic mechanisms of antiphospholipid antibodies. Curr Med Chem 2007; 14 (7) 811-826
• 37 Vega-Ostertag M, Casper K, Swerlick R, Ferrara D, Harris EN, Pierangeli SS. Involvement of p38 MAPK in the up-regulation of tissue factor on endothelial cells by antiphospholipid antibodies. Arthritis Rheum 2005; 52 (5) 1545-1554
• 38 Williams FM, Parmar K, Hughes GR, Hunt BJ. Systemic endothelial cell markers in primary antiphospholipid syndrome. Thromb Haemost 2000; 84 (5) 742-746
• 39 Berman J, Girardi G, Salmon JE. TNF-alpha is a critical effector and a target for therapy in antiphospholipid antibody-induced pregnancy loss. J Immunol 2005; 174 (1) 485-490
• 40 Forastiero RR, Martinuzzo ME, de Larrañaga GF. Circulating levels of tissue factor and proinflammatory cytokines in patients with primary antiphospholipid syndrome or leprosy related antiphospholipid antibodies. Lupus 2005; 14 (2) 129-136
• 41 Griffin JH, Zlokovic BV, Mosnier LO. Protein C anticoagulant and cytoprotective pathways. Int J Hematol 2012; 95 (4) 333-345
• 42 Urbanus RT, de Laat B. Antiphospholipid antibodies and the protein C pathway. Lupus 2010; 19 (4) 394-399
• 43 López-Pedrera C, Buendía P, Cuadrado MJ , et al. Antiphospholipid antibodies from patients with the antiphospholipid syndrome induce monocyte tissue factor expression through the simultaneous activation of NF-kappaB/Rel proteins via the p38 mitogen-activated protein kinase pathway, and of the MEK-1/ERK pathway. Arthritis Rheum 2006; 54 (1) 301-311
• 44 Vega-Ostertag ME, Ferrara DE, Romay-Penabad Z , et al. Role of p38 mitogen-activated protein kinase in antiphospholipid antibody-mediated thrombosis and endothelial cell activation. J Thromb Haemost 2007; 5 (9) 1828-1834
• 45 Blank M, Faden D, Tincani A , et al. Immunization with anticardiolipin cofactor (beta-2-glycoprotein I) induces experimental antiphospholipid syndrome in naive mice. J Autoimmun 1994; 7 (4) 441-455
• 46 Gharavi AE, Sammaritano LR, Wen J, Elkon KB. Induction of antiphospholipid autoantibodies by immunization with beta 2 glycoprotein I (apolipoprotein H). J Clin Invest 1992; 90 (3) 1105-1109
• 47 Katzav A, Pick CG, Korczyn AD , et al. Hyperactivity in a mouse model of the antiphospholipid syndrome. Lupus 2001; 10 (7) 496-499
• 48 Katzav A, Litvinjuk Y, Pick CG , et al. Genetic and immunological factors interact in a mouse model of CNS antiphospholipid syndrome. Behav Brain Res 2006; 169 (2) 289-293
• 49 Shrot S, Katzav A, Korczyn AD , et al. Behavioral and cognitive deficits occur only after prolonged exposure of mice to antiphospholipid antibodies. Lupus 2002; 11 (11) 736-743
• 50 Ziporen L, Shoenfeld Y, Levy Y, Korczyn AD. Neurological dysfunction and hyperactive behavior associated with antiphospholipid antibodies. A mouse model. J Clin Invest 1997; 100 (3) 613-619
• 51 Shoenfeld Y, Nahum A, Korczyn AD , et al. Neuronal-binding antibodies from patients with antiphospholipid syndrome induce cognitive deficits following intrathecal passive transfer. Lupus 2003; 12 (6) 436-442
• 52 Frauenknecht K, Katzav A, Grimm C, Chapman J, Sommer CJ. Neurological impairment in experimental antiphospholipid syndrome is associated with increased ligand binding to hippocampal and cortical serotonergic 5-HT1A receptors. Immunobiology 2013; 218 (4) 517-526
• 53 Krause I, Leibovici L, Blank M, Shoenfeld Y. Clusters of disease manifestations in patients with antiphospholipid syndrome demonstrated by factor analysis. Lupus 2007; 16 (3) 176-180
• 54 Shah NM, Khamashta MA, Atsumi T, Hughes GR. Outcome of patients with anticardiolipin antibodies: a 10 year follow-up of 52 patients. Lupus 1998; 7 (1) 3-6
• 55 Montalbán J, Rio J, Khamastha M , et al. Value of immunologic testing in stroke patients. A prospective multicenter study. Stroke 1994; 25 (12) 2412-2415
• 56 Hughes GR. Migraine, memory loss, and “multiple sclerosis”. Neurological features of the antiphospholipid (Hughes') syndrome. Postgrad Med J 2003; 79 (928) 81-83
• 57 Urbanus RT, Siegerink B, Roest M, Rosendaal FR, de Groot PG, Algra A. Antiphospholipid antibodies and risk of myocardial infarction and ischaemic stroke in young women in the RATIO study: a case-control study. Lancet Neurol 2009; 8 (11) 998-1005
• 58 Cervera R, Piette JC, Font J , et al; Euro-Phospholipid Project Group. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 2002; 46 (4) 1019-1027
• 59 Bucciarelli S, Espinosa G, Cervera R. The CAPS Registry: morbidity and mortality of the catastrophic antiphospholipid syndrome. Lupus 2009; 18 (10) 905-912
• 60 Levine SR, Salowich-Palm L, Sawaya KL , et al. IgG anticardiolipin antibody titer > 40 GPL and the risk of subsequent thrombo-occlusive events and death. A prospective cohort study. Stroke 1997; 28 (9) 1660-1665
• 61 Brey RL, Abbott RD, Curb JD , et al. beta(2)-Glycoprotein 1-dependent anticardiolipin antibodies and risk of ischemic stroke and myocardial infarction: the Honolulu Heart Program. Stroke 2001; 32 (8) 1701-1706
• 62 Gris JC, Bouvier S, Molinari N , et al. Comparative incidence of a first thrombotic event in purely obstetric antiphospholipid syndrome with pregnancy loss: the NOH-APS observational study. Blood 2012; 119 (11) 2624-2632
• 63 Rajamani K, Chaturvedi S, Jin Z , et al; PICSS-APASS Investigators. Patent foramen ovale, cardiac valve thickening, and antiphospholipid antibodies as risk factors for subsequent vascular events: the PICSS-APASS study. Stroke 2009; 40 (7) 2337-2342
• 64 Tanaka Y, Ueno Y, Miyamoto N , et al. Patent foramen ovale and atrial septal aneurysm can cause ischemic stroke in patients with antiphospholipid syndrome. J Neurol 2013; 260 (1) 189-196
• 65 Champion RH, Rook A. Livedo reticularis. Proc R Soc Med 1960; 53: 961-962
• 66 Schellong SM, Weissenborn K, Niedermeyer J , et al. Classification of Sneddon's syndrome. Vasa 1997; 26 (3) 215-221
• 67 Briley DP, Coull BM, Goodnight Jr SH. Neurological disease associated with antiphospholipid antibodies. Ann Neurol 1989; 25 (3) 221-227
• 68 Wiechens B, Schröder JO, Pötzsch B, Rochels R. Primary antiphospholipid antibody syndrome and retinal occlusive vasculopathy. Am J Ophthalmol 1997; 123 (6) 848-850
• 69 Nahum A, Levy Y, Shoenfeld Y. Ocular manifestations in the antiphospholipid syndrome [in Hebrew]. Harefuah 1999; 136 (1) 50-53
• 70 Giorgi D, Gabrieli CB, Bonomo L. The clinico-ophthalmological spectrum of antiphospholipid syndrome. Ocul Immunol Inflamm 1998; 6 (4) 269-273
• 71 Reino S, Muñoz-Rodriguez FJ, Cervera R, Espinosa G, Font J, Ingelmo M. Optic neuropathy in the “primary” antiphospholipid syndrome: report of a case and review of the literature. Clin Rheumatol 1997; 16 (6) 629-631
• 72 Giorgi D, Balacco Gabrieli C. Optic neuropathy in systemic lupus erythematosus and antiphospholipid syndrome (APS): clinical features, pathogenesis, review of the literature and proposed ophthalmological criteria for APS diagnosis. Clin Rheumatol 1999; 18 (2) 124-131
• 73 Peltola JT, Haapala A, Isojärvi JI , et al. Antiphospholipid and antinuclear antibodies in patients with epilepsy or new-onset seizure disorders. Am J Med 2000; 109 (9) 712-717
• 74 Liou HH, Wang CR, Chou HC , et al. Anticardiolipin antisera from lupus patients with seizures reduce a GABA receptor-mediated chloride current in snail neurons. Life Sci 1994; 54 (15) 1119-1125
• 75 Miesbach W, Chapman J, Scharrer I. Focal seizures after treatment with fluvastatin in a patient with a history of catastrophic antiphospholipid syndrome. J Neurol Sci 2005; 238 (1–2) 93-95
• 76 Jacobson MW, Rapport LJ, Keenan PA, Coleman RD, Tietjen GE. Neuropsychological deficits associated with antiphospholipid antibodies. J Clin Exp Neuropsychol 1999; 21 (2) 251-264
• 77 Mosek A, Yust I, Treves TA, Vardinon N, Korczyn AD, Chapman J. Dementia and antiphospholipid antibodies. Dement Geriatr Cogn Disord 2000; 11 (1) 36-38
• 78 Schmidt R, Auer-Grumbach P, Fazekas F, Offenbacher H, Kapeller P. Anticardiolipin antibodies in normal subjects. Neuropsychological correlates and MRI findings. Stroke 1995; 26 (5) 749-754
• 79 Whitelaw DA, Spangenberg JJ, Rickman R, Hugo FH, Roberts M. The association between the antiphospholipid antibody syndrome and neuropsychological impairment in SLE. Lupus 1999; 8 (6) 444-448
• 80 Menon S, Jameson-Shortall E, Newman SP, Hall-Craggs MR, Chinn R, Isenberg DA. A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum 1999; 42 (4) 735-741
• 81 Olazarán J, López-Longo J, Cruz I, Bittini A, Carreño L. Cognitive dysfunction in systemic lupus erythematosus: prevalence and correlates. Eur Neurol 2009; 62 (1) 49-55
• 82 Arvanitakis Z, Brey RL, Rand JH , et al. Antiphospholipid antibodies, brain infarcts, and cognitive and motor decline in aging (ABICMA): design of a community-based, longitudinal, clinical-pathological study. Neuroepidemiology 2013; 40 (2) 73-84
• 83 Cervera R, Asherson RA, Font J , et al. Chorea in the antiphospholipid syndrome. Clinical, radiologic, and immunologic characteristics of 50 patients from our clinics and the recent literature. Medicine (Baltimore) 1997; 76 (3) 203-212
• 84 Cavestro C, Micca G, Molinari F , et al. Migraineurs show a high prevalence of antiphospholipid antibodies. J Thromb Haemost 2011; 9 (7) 1350-1354
• 85 Tietjen GE, Day M, Norris L , et al. Role of anticardiolipin antibodies in young persons with migraine and transient focal neurologic events: a prospective study. Neurology 1998; 50 (5) 1433-1440
• 86 Sanna G, Bertolaccini ML, Cuadrado MJ, Khamashta MA, Hughes GR. Central nervous system involvement in the antiphospholipid (Hughes) syndrome. Rheumatology (Oxford) 2003; 42 (2) 200-213
• 87 Kao CH, Lan JL, Hsieh JF , et al. Evaluation of regional cerebral blood flow with 99mTc-HMPAO in primary antiphospholipid antibody syndrome. J Nucl Med 1999; 40 (9) 1446-1450
• 88 Maes M, Meltzer H, Jacobs J , et al. Autoimmunity in depression: increased antiphospholipid autoantibodies. Acta Psychiatr Scand 1993; 87 (3) 160-166
• 89 Raza H, Epstein SA, Pao M, Rosenstein DL. Mania: psychiatric manifestations of the antiphospholipid syndrome. Psychosomatics 2008; 49 (5) 438-441
• 90 Barros S, de Carvalho J. Pathological gambling and primary antiphospholipid (Hughes) syndrome: a unique neuropsychiatric association. Lupus 2011; 20 (10) 1086-1089
• 91 Avari JN, Young RC. A patient with bipolar disorder and antiphospholipid syndrome. J Geriatr Psychiatry Neurol 2012; 25 (1) 26-28
• 92 Shulman KI, Herrmann N. The nature and management of mania in old age. Psychiatr Clin North Am 1999; 22 (3) 649-665 , ix
• 93 Steffens DC, Krishnan KR. Structural neuroimaging and mood disorders: recent findings, implications for classification, and future directions. Biol Psychiatry 1998; 43 (10) 705-712
• 94 Lyness J, Caine E. Cerebrovascular risk factors and depression: data, deductions and directions. In: Chiu E, Ames D, Katona C, , eds. Vascular Disease and Affective Disorders. London, UK: Martin Dunitz Ltd; 2002: 161-170
• 95 Spyropoulou AC, Tsartsara EI, Angelopoulou A, Zervas IM. Psychiatric manifestations preceding fetal death in antiphospholipid syndrome. Gen Hosp Psychiatry 2010; 32 (2) 225-227
• 96 Canoso RT, de Oliveira RM, Nixon RA. Neuroleptic-associated autoantibodies. A prevalence study. Biol Psychiatry 1990; 27 (8) 863-870
• 97 Lillicrap DP, Pinto M, Benford K, Ford PM, Ford S. Heterogeneity of laboratory test results for antiphospholipid antibodies in patients treated with chlorpromazine and other phenothiazines. Am J Clin Pathol 1990; 93 (6) 771-775
• 98 Schwartz M, Silver H. Lymphocytes, autoantibodies and psychosis—coincidence versus etiological factor: an update. Isr J Psychiatry Relat Sci 2000; 37 (1) 32-36
• 99 Sirota P, Schild K, Firer M. The diversity of autoantibodies in schizophrenic patients and their first degree relatives: analysis of multiple case families. Biol Psychiatry 1990; 27 (Suppl. 01) 118A
• 100 Strous RD, Shoenfeld Y. Schizophrenia, autoimmunity and immune system dysregulation: a comprehensive model updated and revisited. J Autoimmun 2006; 27 (2) 71-80
• 101 Schwartz M, Rochas M, Weller B , et al. High association of anticardiolipin antibodies with psychosis. J Clin Psychiatry 1998; 59 (1) 20-23
• 102 Chengappa KN, Carpenter AB, Keshavan MS , et al. Elevated IGG and IGM anticardiolipin antibodies in a subgroup of medicated and unmedicated schizophrenic patients. Biol Psychiatry 1991; 30 (7) 731-735
• 103 Arolt V, Rothermundt M, Peters M, Leonard B. Immunological research in clinical psychiatry: report on the consensus debate during the 7th Expert Meeting on Psychiatry and Immunology. Mol Psychiatry 2002; 7 (8) 822-826
• 104 Lai JY, Wu PC, Chen HC, Lee MB. Early neuropsychiatric involvement in antiphospholipid syndrome. Gen Hosp Psychiatry 2012; 34 (5) 579 e571-573
• 105 Shabana M, Shalaby M, Alhumayed S, Alshehri A. Paediatric case report: primary antiphospholipid syndrome presented with non-thrombotic neurological picture psychosis; treat by antidepressants alone?. Int J Rheum Dis 2009; 12 (2) 170-173
• 106 Sokol DK, O'Brien RS, Wagenknecht DR, Rao T, McIntyre JA. Antiphospholipid antibodies in blood and cerebrospinal fluids of patients with psychosis. J Neuroimmunol 2007; 190 (1–2) 151-156
• 107 Borowoy AM, Pope JE, Silverman E , et al. Neuropsychiatric lupus: the prevalence and autoantibody associations depend on the definition: results from the 1000 faces of lupus cohort. Semin Arthritis Rheum 2012; 42 (2) 179-185
• 108 Bertsias GK, Ioannidis JP, Aringer M , et al. 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 Dis 2010; 69 (12) 2074-2082
• 109 Kesler A, Ellis MH, Reshef T, Kott E, Gadoth N. Idiopathic intracranial hypertension and anticardiolipin antibodies. J Neurol Neurosurg Psychiatry 2000; 68 (3) 379-380
• 110 Lavalle C, Pizarro S, Drenkard C, Sánchez-Guerrero J, Alarcón-Segovia D. Transverse myelitis: a manifestation of systemic lupus erythematosus strongly associated with antiphospholipid antibodies. J Rheumatol 1990; 17 (1) 34-37
• 111 Ruiz-Argüelles GJ, Guzmán-Ramos J, Flores-Flores J, Garay-Martínez J. Refractory hiccough heralding transverse myelitis in the primary antiphospholipid syndrome. Lupus 1998; 7 (1) 49-50
• 112 Kovacs B, Lafferty TL, Brent LH, DeHoratius RJ. Transverse myelopathy in systemic lupus erythematosus: an analysis of 14 cases and review of the literature. Ann Rheum Dis 2000; 59 (2) 120-124
• 113 Karussis D, Leker RR, Ashkenazi A, Abramsky O. A subgroup of multiple sclerosis patients with anticardiolipin antibodies and unusual clinical manifestations: do they represent a new nosological entity?. Ann Neurol 1998; 44 (4) 629-634
• 114 Tourbah A, Clapin A, Gout O , et al. Systemic autoimmune features and multiple sclerosis: a 5-year follow-up study. Arch Neurol 1998; 55 (4) 517-521
• 115 Szmyrka-Kaczmarek M, Pokryszko-Dragan A, Pawlik B , et al. Antinuclear and antiphospholipid antibodies in patients with multiple sclerosis. Lupus 2012; 21 (4) 412-420
• 116 Ahbeddou N, Ait Ben Haddou E, Hammi S , et al. [Multiple sclerosis associated with antiphospholipid syndrome: diagnostic and therapeutic difficulties]. Rev Neurol (Paris) 2012; 168 (1) 65-69
• 117 Stosic M, Ambrus J, Garg N , et al. MRI characteristics of patients with antiphospholipid syndrome and multiple sclerosis. J Neurol 2010; 257 (1) 63-71
• 118 Liedorp M, Sanchez E, van Hoogstraten IM , et al. No evidence of misdiagnosis in patients with multiple sclerosis and repeated positive anticardiolipin antibody testing based on magnetic resonance imaging and long term follow-up. J Neurol Neurosurg Psychiatry 2007; 78 (10) 1146-1148
• 119 Lim W, Crowther MA, Eikelboom JW. Management of antiphospholipid antibody syndrome: a systematic review. JAMA 2006; 295 (9) 1050-1057
• 120 Panichpisal K, Rozner E, Levine SR. The management of stroke in antiphospholipid syndrome. Curr Rheumatol Rep 2012; 14 (1) 99-106
• 121 Appenzeller S, Cendes F, Costallat LT. Acute psychosis in systemic lupus erythematosus. Rheumatol Int 2008; 28 (3) 237-243
• 122 Schneider C, Adamcova M, Jick SS , et al. Antimalarial chemoprophylaxis and the risk of neuropsychiatric disorders. Travel Med Infect Dis 2013; 11 (2) 71-80