Download PDF
Semin Thromb Hemost 2024; 50(06): 817-828
DOI: 10.1055/s-0043-1776910
Review Article

Risk Factors for Antiphospholipid Antibodies and Antiphospholipid Syndrome

Rodrigo Aguirre del-Pino 
1   Department of Rheumatology, Leiden University Medical Center (LUMC), Leiden, The Netherlands
2   Division of Rheumatology, A Coruña University Hospital (CHUAC), Galicia, Spain
,
Rory C. Monahan
1   Department of Rheumatology, Leiden University Medical Center (LUMC), Leiden, The Netherlands
3   Department of Clinical Epidemiology, Leiden University Medical Center (LUMC), Leiden, The Netherlands
,
Tom W.J. Huizinga
1   Department of Rheumatology, Leiden University Medical Center (LUMC), Leiden, The Netherlands
,
Jeroen Eikenboom
4   Division of Thrombosis and Hemostasis, Department of Internal Medicine, Leiden University Medical Center (LUMC), Leiden, The Netherlands
,
Gerda M. Steup-Beekman
1   Department of Rheumatology, Leiden University Medical Center (LUMC), Leiden, The Netherlands
5   Department of Rheumatology, Haaglanden Medical Center, The Hague, The Netherlands
› Author Affiliations Funding R.A. was funded by the 2022 EULAR Scientific training bursary for young rheumatologists.
› Further Information
   Permissions and Reprints

Abstract

Persistence of serum antiphospholipid antibodies (aPL) is associated with a high thrombotic risk, both arterial and venous, and with pregnancy complications. Due to the potential morbidity and mortality associated with the presence of aPL, identifying and recognizing risk factors for the development of aPL and thrombosis in aPL carriers may help to prevent and reduce the burden of disease. Multiple elements are involved in the pathomechanism of aPL development and aPL-related thrombosis such as genetics, malignancy, and infections. This review will address the role of both well-known risk factors and their evolution, and of emerging risk factors, including COVID-19, in the development of aPL and thrombosis in aPL carriers.

Keywords

antiphospholipid syndrome - antiphospholipid antibody - thrombosis - risk factor


Publication History

Article published online:
16 January 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 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 (02) 295-306
    CrossrefPubMedSearch in Google Scholar
  • 2 Moore GW. Testing for lupus anticoagulants. Semin Thromb Hemost 2022; 48 (06) 643-660
    Thieme ConnectPubMedSearch in Google Scholar
  • 3 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 (04) 1019-1027
    CrossrefPubMedSearch in Google Scholar
  • 4 Xourgia E, Tektonidou MG. An update on antiphospholipid syndrome. Curr Rheumatol Rep 2022; 23 (12) 84
    CrossrefPubMedSearch in Google Scholar
  • 5 Lackner KJ, Müller-Calleja N. Antiphospholipid antibodies: their origin and development. Antibodies (Basel) 2016; 5 (02) 15
    CrossrefPubMedSearch in Google Scholar
  • 6 Giannakopoulos B, Krilis SA. The pathogenesis of the antiphospholipid syndrome. N Engl J Med 2013; 368 (11) 1033-1044
    CrossrefPubMedSearch in Google Scholar
  • 7 Abdel-Wahab N, Tayar JH, Fa'ak F. et al. Systematic review of observational studies reporting antiphospholipid antibodies in patients with solid tumors. Blood Adv 2020; 4 (08) 1746-1755
    CrossrefPubMedSearch in Google Scholar
  • 8 Shi W, Krilis SA, Chong BH, Gordon S, Chesterman CN. Prevalence of lupus anticoagulant and anticardiolipin antibodies in a healthy population. Aust N Z J Med 1990; 20 (03) 231-236
    CrossrefPubMedSearch in Google Scholar
  • 9 Vila P, Hernández MC, López-Fernández MF, Batlle J. Prevalence, follow-up and clinical significance of the anticardiolipin antibodies in normal subjects. Thromb Haemost 1994; 72 (02) 209-213
    Thieme ConnectPubMedSearch in Google Scholar
  • 10 Long AA, Ginsberg JS, Brill-Edwards P. et al. The relationship of antiphospholipid antibodies to thromboembolic disease in systemic lupus erythematosus: a cross-sectional study. Thromb Haemost 1991; 66 (05) 520-524
    Thieme ConnectPubMedSearch in Google Scholar
  • 11 Love PE, Santoro SA. Antiphospholipid antibodies: anticardiolipin and the lupus anticoagulant in systemic lupus erythematosus (SLE) and in non-SLE disorders. Prevalence and clinical significance. Ann Intern Med 1990; 112 (09) 682-698
    CrossrefPubMedSearch in Google Scholar
  • 12 Bertin D, Camoin-Jau L, Veit V. et al. Single or triple positivity for antiphospholipid antibodies in “carriers” or symptomatic patients: Untangling the knot. J Thromb Haemost 2021; 19 (12) 3018-3030
    CrossrefPubMedSearch in Google Scholar
  • 13 Ortiz-Fernández L, Sawalha AH. Genetics of antiphospholipid syndrome. Curr Rheumatol Rep 2019; 21 (12) 65
    CrossrefPubMedSearch in Google Scholar
  • 14 Lee YH, Choi SJ, Ji JD, Song GG. Association between the valine/leucine247 polymorphism of β2-glycoprotein I and susceptibility to anti-phospholipid syndrome: a meta-analysis. Lupus 2012; 21 (08) 865-871
    CrossrefPubMedSearch in Google Scholar
  • 15 Canaud G, Bienaimé F, Tabarin F. et al. Inhibition of the mTORC pathway in the antiphospholipid syndrome. N Engl J Med 2014; 371 (04) 303-312
    CrossrefPubMedSearch in Google Scholar
  • 16 Müller-Calleja N, Rossmann H, Müller C. et al. Antiphospholipid antibodies in a large population-based cohort: genome-wide associations and effects on monocyte gene expression. Thromb Haemost 2016; 116 (01) 115-123
    PubMedSearch in Google Scholar
  • 17 Galli M, Luciani D, Bertolini G, Barbui T. Lupus anticoagulants are stronger risk factors for thrombosis than anticardiolipin antibodies in the antiphospholipid syndrome: a systematic review of the literature. Blood 2003; 101 (05) 1827-1832
    CrossrefPubMedSearch in Google Scholar
  • 18 García-Carrasco M, Galarza-Maldonado C, Mendoza-Pinto C, Escarcega RO, Cervera R. Infections and the antiphospholipid syndrome. Clin Rev Allergy Immunol 2009; 36 (2-3): 104-108
    CrossrefPubMedSearch in Google Scholar
  • 19 Abdel-Wahab N, Talathi S, Lopez-Olivo MA, Suarez-Almazor ME. Risk of developing antiphospholipid antibodies following viral infection: a systematic review and meta-analysis. Lupus 2018; 27 (04) 572-583
    CrossrefPubMedSearch in Google Scholar
  • 20 Ruff WE, Dehner C, Kim WJ. et al. Pathogenic autoreactive T and B cells cross-react with mimotopes expressed by a common human gut commensal to trigger autoimmunity. Cell Host Microbe 2019; 26 (01) 100-113.e8
    CrossrefPubMedSearch in Google Scholar
  • 21 Piette JC, Cacoub P. Antiphospholipid syndrome in the elderly: caution. Circulation 1998; 97 (22) 2195-2196
    CrossrefPubMedSearch in Google Scholar
  • 22 Barreno-Rocha SG, Guzmán-Silahua S, Rodríguez-Dávila SD. et al. Antiphospholipid antibodies and lipids in hematological malignancies. Int J Mol Sci 2022; 23 (08) 4151
    CrossrefPubMedSearch in Google Scholar
  • 23 Duarte-García A, Pham MM, Crowson CS. et al. The epidemiology of antiphospholipid syndrome: a population-based study. Arthritis Rheumatol 2019; 71 (09) 1545-1552
    CrossrefPubMedSearch in Google Scholar
  • 24 Dabit JY, Valenzuela-Almada MO, Vallejo-Ramos S, Duarte-García A. Epidemiology of antiphospholipid syndrome in the general population. Curr Rheumatol Rep 2022; 23 (12) 85
    CrossrefPubMedSearch in Google Scholar
  • 25 Ruiz-Irastorza G, Egurbide MV, Ugalde J, Aguirre C. High impact of antiphospholipid syndrome on irreversible organ damage and survival of patients with systemic lupus erythematosus. Arch Intern Med 2004; 164 (01) 77-82
    CrossrefPubMedSearch in Google Scholar
  • 26 Truglia S, Capozzi A, Mancuso S. et al. Relationship between gender differences and clinical outcome in patients with the antiphospholipid syndrome. Front Immunol 2022; 13: 932181
    CrossrefPubMedSearch in Google Scholar
  • 27 Lim W. Thrombotic risk in the antiphospholipid syndrome. Semin Thromb Hemost 2014; 40 (07) 741-746
    Thieme ConnectPubMedSearch in Google Scholar
  • 28 de Groot PG, Lutters B, Derksen RH, Lisman T, Meijers JC, Rosendaal FR. Lupus anticoagulants and the risk of a first episode of deep venous thrombosis. J Thromb Haemost 2005; 3 (09) 1993-1997
    CrossrefPubMedSearch in Google Scholar
  • 29 Gebhart J, Posch F, Koder S. et al. Increased mortality in patients with the lupus anticoagulant: the Vienna Lupus Anticoagulant and Thrombosis Study (LATS). Blood 2015; 125 (22) 3477-3483
    CrossrefPubMedSearch in Google Scholar
  • 30 Tektonidou MG, Andreoli L, Limper M. et al. EULAR recommendations for the management of antiphospholipid syndrome in adults. Ann Rheum Dis 2019; 78 (10) 1296-1304
    CrossrefPubMedSearch in Google Scholar
  • 31 Chayoua W, Kelchtermans H, Moore GW. et al. Identification of high thrombotic risk triple-positive antiphospholipid syndrome patients is dependent on anti-cardiolipin and anti-β2glycoprotein I antibody detection assays. J Thromb Haemost 2018; 16 (10) 2016-2023
    CrossrefPubMedSearch in Google Scholar
  • 32 Pengo V, Biasiolo A, Pegoraro C, Cucchini U, Noventa F, Iliceto S. Antibody profiles for the diagnosis of antiphospholipid syndrome. Thromb Haemost 2005; 93 (06) 1147-1152
    Thieme ConnectPubMedSearch in Google Scholar
  • 33 Garcia D, Erkan D. Diagnosis and management of the antiphospholipid syndrome. N Engl J Med 2018; 378 (21) 2010-2021
    CrossrefPubMedSearch in Google Scholar
  • 34 Hughes GRV, Khamashta MA. Seronegative antiphospholipid syndrome. Ann Rheum Dis 2003; 62 (12) 1127
    CrossrefPubMedSearch in Google Scholar
  • 35 Tortosa C, Cabrera-Marante O, Serrano M. et al. Incidence of thromboembolic events in asymptomatic carriers of IgA anti ß2 glycoprotein-I antibodies. PLoS One 2017; 12 (07) e0178889
    CrossrefPubMedSearch in Google Scholar
  • 36 Bizzaro N, Ghirardello A, Zampieri S. et al. Anti-prothrombin antibodies predict thrombosis in patients with systemic lupus erythematosus: a 15-year longitudinal study. J Thromb Haemost 2007; 5 (06) 1158-1164
    CrossrefPubMedSearch in Google Scholar
  • 37 Truglia S, Mancuso S, Capozzi A. et al. ‘Non-criteria antiphospholipid antibodies’: bridging the gap between seropositive and seronegative antiphospholipid syndrome. Rheumatology (Oxford) 2022; 61 (02) 826-833
    CrossrefPubMedSearch in Google Scholar
  • 38 Pires da Rosa G, Bettencourt P, Rodríguez-Pintó I, Cervera R, Espinosa G. “Non-criteria” antiphospholipid syndrome: a nomenclature proposal. Autoimmun Rev 2020; 19 (12) 102689
    CrossrefPubMedSearch in Google Scholar
  • 39 Sciascia S, Sanna G, Murru V, Roccatello D, Khamashta MA, Bertolaccini ML. The global anti-phospholipid syndrome score in primary APS. Rheumatology (Oxford) 2015; 54 (01) 134-138
    CrossrefPubMedSearch in Google Scholar
  • 40 Zuily S, de Laat B, Mohamed S. et al; TAC(I)T Investigators. Validity of the global anti-phospholipid syndrome score to predict thrombosis: a prospective multicentre cohort study. Rheumatology (Oxford) 2015; 54 (11) 2071-2075
    CrossrefPubMedSearch in Google Scholar
  • 41 Cervera R, Tektonidou MG, Espinosa G. et al. Task force on catastrophic antiphospholipid syndrome (APS) and non-criteria APS manifestations (II): thrombocytopenia and skin manifestations. Lupus 2011; 20 (02) 174-181
    CrossrefPubMedSearch in Google Scholar
  • 42 Unlu O, Erkan D, Barbhaiya M. et al; AntiPhospholipid Syndrome Alliance for Clinical Trials and InternatiOnal Networking Investigators. The impact of systemic lupus erythematosus on the clinical phenotype of antiphospholipid antibody-positive patients: results from the AntiPhospholipid Syndrome Alliance for Clinical Trials and InternatiOnal Clinical Database and Repository. Arthritis Care Res (Hoboken) 2019; 71 (01) 134-141
    CrossrefPubMedSearch in Google Scholar
  • 43 Sammaritano LR. Antiphospholipid syndrome. Best Pract Res Clin Rheumatol 2020; 34 (01) 101463
    CrossrefPubMedSearch in Google Scholar
  • 44 Harris EN, Chan JK, Asherson RA, Aber VR, Gharavi AE, Hughes GR. Thrombosis, recurrent fetal loss, and thrombocytopenia. Predictive value of the anticardiolipin antibody test. Arch Intern Med 1986; 146 (11) 2153-2156
    CrossrefPubMedSearch in Google Scholar
  • 45 Pablo RD, Cacho PM, López-Hoyos M, Calvo-Río V, Riancho-Zarrabeitia L, Martínez-Taboada VM. Risk factors for the development of the disease in antiphospholipid antibodies carriers: a long-term follow-up study. Clin Rev Allergy Immunol 2022; 62 (02) 354-362
    CrossrefPubMedSearch in Google Scholar
  • 46 Comellas-Kirkerup L, Hernández-Molina G, Cabral AR. Antiphospholipid-associated thrombocytopenia or autoimmune hemolytic anemia in patients with or without definite primary antiphospholipid syndrome according to the Sapporo revised classification criteria: a 6-year follow-up study. Blood 2010; 116 (16) 3058-3063
    CrossrefPubMedSearch in Google Scholar
  • 47 Hisada R, Kato M, Sugawara E. et al. Thrombotic risk stratification by platelet count in patients with antiphospholipid antibodies: a longitudinal study. J Thromb Haemost 2017; 15 (09) 1782-1787
    CrossrefPubMedSearch in Google Scholar
  • 48 Vreede AP, Bockenstedt PL, McCune WJ, Knight JS. Cryptic conspirators: a conversation about thrombocytopenia and antiphospholipid syndrome. Curr Opin Rheumatol 2019; 31 (03) 231-240
    CrossrefPubMedSearch in Google Scholar
  • 49 Ames PRJ, Merashli M, Bucci T. et al. Antiphospholipid antibodies and autoimmune haemolytic anaemia: a systematic review and meta-analysis. Int J Mol Sci 2020; 21 (11) 4120
    CrossrefPubMedSearch in Google Scholar
  • 50 Tektonidou MG, Ioannidis JP, Boki KA, Vlachoyiannopoulos PG, Moutsopoulos HM. Prognostic factors and clustering of serious clinical outcomes in antiphospholipid syndrome. QJM 2000; 93 (08) 523-530
    CrossrefPubMedSearch in Google Scholar
  • 51 Ordi-Ros J, Sáez-Comet L, Pérez-Conesa M. et al. Rivaroxaban versus vitamin K antagonist in antiphospholipid syndrome: a randomized noninferiority trial. Ann Intern Med 2019; 171 (10) 685-694
    CrossrefPubMedSearch in Google Scholar
  • 52 Shen Y, Chen XW, Sun CY, Dai M, Yan YC, Yang CD. Association between anti-beta2 glycoprotein I antibodies and renal glomerular C4d deposition in lupus nephritis patients with glomerular microthrombosis: a prospective study of 155 cases. Lupus 2010; 19 (10) 1195-1203
    CrossrefPubMedSearch in Google Scholar
  • 53 Tektonidou MG, Sotsiou F, Nakopoulou L, Vlachoyiannopoulos PG, Moutsopoulos HM. Antiphospholipid syndrome nephropathy in patients with systemic lupus erythematosus and antiphospholipid antibodies: prevalence, clinical associations, and long-term outcome. Arthritis Rheum 2004; 50 (08) 2569-2579
    CrossrefPubMedSearch in Google Scholar
  • 54 McRae S, Tran H, Schulman S, Ginsberg J, Kearon C. Effect of patient's sex on risk of recurrent venous thromboembolism: a meta-analysis. Lancet 2006; 368 (9533) 371-378
    CrossrefPubMedSearch in Google Scholar
  • 55 Huang Y, Liu H, Qi W. et al. Sex differences in clinical characteristics and prognosis in primary thrombotic antiphospholipid syndrome. Front Cardiovasc Med 2022; 9: 895098
    CrossrefPubMedSearch in Google Scholar
  • 56 Matyja-Bednarczyk A, Swadźba J, Iwaniec T. et al. Risk factors for arterial thrombosis in antiphospholipid syndrome. Thromb Res 2014; 133 (02) 173-176
    CrossrefPubMedSearch in Google Scholar
  • 57 Sciascia S, Sanna G, Khamashta MA. et al; APS Action. The estimated frequency of antiphospholipid antibodies in young adults with cerebrovascular events: a systematic review. Ann Rheum Dis 2015; 74 (11) 2028-2033
    CrossrefPubMedSearch in Google Scholar
  • 58 Roldan JF, Brey RL. Neurologic manifestations of the antiphospholipid syndrome. Curr Rheumatol Rep 2007; 9 (02) 109-115
    CrossrefPubMedSearch in Google Scholar
  • 59 Fujieda Y, Atsumi T, Amengual O. et al. Predominant prevalence of arterial thrombosis in Japanese patients with antiphospholipid syndrome. Lupus 2012; 21 (14) 1506-1514
    CrossrefPubMedSearch in Google Scholar
  • 60 Niznik S, Rapoport MJ, Avnery O, Ellis MH, Hajyahia S, Agmon-Levin N. Ethnicity and antiphospholipid syndrome in Israel. Arthritis Care Res (Hoboken) 2022; 74 (11) 1917-1923
    CrossrefPubMedSearch in Google Scholar
  • 61 Manzano-Gamero V, Pardo-Cabello AJ, Vargas-Hitos JA. et al; Spanish Autoimmune Diseases Study Group (GEAS). Effect of ethnicity on clinical presentation and risk of antiphospholipid syndrome in Roma and Caucasian patients with systemic lupus erythematosus: a multicenter cross-sectional study. Int J Rheum Dis 2018; 21 (11) 2028-2035
    CrossrefPubMedSearch in Google Scholar
  • 62 Abu-Zeinah G, Oromendia C, DeSancho MT. Thrombotic risk factors in patients with antiphospholipid syndrome: a single center experience. J Thromb Thrombolysis 2019; 48 (02) 233-239
    CrossrefPubMedSearch in Google Scholar
  • 63 da Silva FF, Levy RA, de Carvalho JF. Cardiovascular risk factors in the antiphospholipid syndrome. J Immunol Res 2014; 2014: 621270
    CrossrefPubMedSearch in Google Scholar
  • 64 Ribeiro AR, Carvalho JF. Fatores de risco tradicionais para doença cardiovascular na síndrome antifosfolípide 36 primária comparada à secundária: um estudo de 96 pacientes. Acta Reumatol Port 2010; 35 (01) 36-41
    PubMedSearch in Google Scholar
  • 65 Bilora F, Boccioletti V, Girolami B. et al. Are antiphospholipid antibodies an independent risk factor for atherosclerosis?. Clin Appl Thromb Hemost 2002; 8 (02) 103-113
    CrossrefPubMedSearch in Google Scholar
  • 66 Ogata Y, Fujieda Y, Sugawara M. et al. Morbidity and mortality in antiphospholipid syndrome based on cluster analysis: a 10-year longitudinal cohort study. Rheumatology (Oxford) 2021; 60 (03) 1331-1337
    CrossrefPubMedSearch in Google Scholar
  • 67 Yelnik CM, Martin C, Ledoult E. et al. Dyslipidemia is insufficiently treated in antiphospholipid syndrome patients. Lupus 2022; 31 (11) 1379-1384
    CrossrefPubMedSearch in Google Scholar
  • 68 Celermajer DS, Sorensen KE, Georgakopoulos D. et al. Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults. Circulation 1993; 88 (5, Pt 1): 2149-2155
    CrossrefPubMedSearch in Google Scholar
  • 69 Mustonen P, Lehtonen KV, Javela K, Puurunen M. Persistent antiphospholipid antibody (aPL) in asymptomatic carriers as a risk factor for future thrombotic events: a nationwide prospective study. Lupus 2014; 23 (14) 1468-1476
    CrossrefPubMedSearch in Google Scholar
  • 70 de Carvalho JF, Pasoto SG, Appenzeller S. Seizures in primary antiphospholipid syndrome: the relevance of smoking to stroke. Clin Dev Immunol 2012; 2012: 981519
    CrossrefPubMedSearch in Google Scholar
  • 71 Zuo Y, Fan J, Sarode R. et al. Identifying additional risk factors for thrombosis and pregnancy morbidities among antiphospholipid antibodies carriers. Clin Appl Thromb Hemost 2018; 24 (06) 980-985
    CrossrefPubMedSearch in Google Scholar
  • 72 Mesa M, Saldarriaga C, Aguilar C. et al. Síndrome antifosfolípido: descripción de una cohorte de pacientes colombianos y evaluación de los factores de riesgo para trombosis. Revista Colombiana de Reumatologia 2012; 19 (04) 208-217
    CrossrefPubMedSearch in Google Scholar
  • 73 Navarro-Carpentieri D, Del Carmen Castillo-Hernandez M, Majluf-Cruz K. et al. Impact of classical risk factors for arterial or venous thrombosis in patients with antiphospholipid syndrome. Clin Appl Thromb Hemost 2018; 24 (05) 834-840
    CrossrefPubMedSearch in Google Scholar
  • 74 Di Minno MND, Scalera A, Tufano A. et al. The association of adjusted Global AntiphosPholipid Syndrome Score (aGAPSS) with cardiovascular disease in subjects with antiphospholipid antibodies. Atherosclerosis 2018; 278: 60-65
    CrossrefPubMedSearch in Google Scholar
  • 75 Kato M, Hisada R, Atsumi T. Clinical profiles and risk assessment in patients with antiphospholipid antibodies. Expert Rev Clin Immunol 2019; 15 (01) 73-81
    CrossrefPubMedSearch in Google Scholar
  • 76 Jiménez S, García-Criado MA, Tàssies D. et al. Preclinical vascular disease in systemic lupus erythematosus and primary antiphospholipid syndrome. Rheumatology (Oxford) 2005; 44 (06) 756-761
    CrossrefPubMedSearch in Google Scholar
  • 77 Evangelatos G, Kravvariti E, Konstantonis G, Tentolouris N, Sfikakis PP, Tektonidou MG. Atherosclerosis progression in antiphospholipid syndrome is comparable to diabetes mellitus: a 3 year prospective study. Rheumatology (Oxford) 2022; 61 (08) 3408-3413
    CrossrefPubMedSearch in Google Scholar
  • 78 Ambrosino P, Lupoli R, Di Minno A, Iervolino S, Peluso R, Di Minno MND. Markers of cardiovascular risk in patients with antiphospholipid syndrome: a meta-analysis of literature studies. Ann Med 2014; 46 (08) 693-702
    CrossrefPubMedSearch in Google Scholar
  • 79 Tektonidou MG. Cardiovascular disease risk in antiphospholipid syndrome: thrombo-inflammation and atherothrombosis. J Autoimmun 2022; 128: 102813
    CrossrefPubMedSearch in Google Scholar
  • 80 Kolitz T, Shiber S, Sharabi I, Winder A, Zandman-Goddard G. Cardiac manifestations of antiphospholipid syndrome with focus on its primary form. Front Immunol 2019; 10: 941
    CrossrefPubMedSearch in Google Scholar
  • 81 Whittier M, Bautista Sanchez R, Arora S, Manadan AM. Systemic lupus erythematosus and antiphospholipid antibody syndrome as risk factors for acute coronary syndrome in young patients: analysis of the National Inpatient Sample. J Clin Rheumatol 2022; 28 (03) 143-146
    CrossrefPubMedSearch in Google Scholar
  • 82 Bolla E, Tentolouris N, Sfikakis PP, Tektonidou MG. Cardiovascular risk management in antiphospholipid syndrome: trends over time and comparison with rheumatoid arthritis and diabetes mellitus. Lupus Sci Med 2021; 8 (01) e000579
    CrossrefPubMedSearch in Google Scholar
  • 83 Urowitz MB, Gladman DD. Contributions of observational cohort studies in systemic lupus erythematosus: the University of Toronto Lupus Clinic experience. Rheum Dis Clin North Am 2005; 31 (02) 211-221 , v
    CrossrefPubMedSearch in Google Scholar
  • 84 Erkan D. Lupus and thrombosis. J Rheumatol 2006; 33 (09) 1715-1717
    PubMedSearch in Google Scholar
  • 85 Tektonidou MG, Wang Z, Ward MM. Brief report: trends in hospitalizations due to acute coronary syndromes and stroke in patients with systemic lupus erythematosus, 1996 to 2012. Arthritis Rheumatol 2016; 68 (11) 2680-2685
    CrossrefPubMedSearch in Google Scholar
  • 86 Cervera R, Khamashta MA, Font J. et al; European Working Party on Systemic Lupus Erythematosus. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003; 82 (05) 299-308
    CrossrefPubMedSearch in Google Scholar
  • 87 Cervera R, Khamashta MA, Hughes GR. The Euro-lupus project: epidemiology of systemic lupus erythematosus in Europe. Lupus 2009; 18 (10) 869-874
    CrossrefPubMedSearch in Google Scholar
  • 88 Amoroso A, Mitterhofer AP, Del Porto F. et al. Antibodies to anionic phospholipids and anti-beta2-GPI: association with thrombosis and thrombocytopenia in systemic lupus erythematosus. Hum Immunol 2003; 64 (02) 265-273
    CrossrefPubMedSearch in Google Scholar
  • 89 Wahl DG, Guillemin F, de Maistre E, Perret C, Lecompte T, Thibaut G. Risk for venous thrombosis related to antiphospholipid antibodies in systemic lupus erythematosus – a meta-analysis. Lupus 1997; 6 (05) 467-473
    CrossrefPubMedSearch in Google Scholar
  • 90 Riancho-Zarrabeitia L, Martínez-Taboada V, Rúa-Figueroa I. et al. Antiphospholipid syndrome (APS) in patients with systemic lupus erythematosus (SLE) implies a more severe disease with more damage accrual and higher mortality. Lupus 2020; 29 (12) 1556-1565
    CrossrefPubMedSearch in Google Scholar
  • 91 Andrianova IA, Ponomareva AA, Mordakhanova ER. et al. In systemic lupus erythematosus anti-dsDNA antibodies can promote thrombosis through direct platelet activation. J Autoimmun 2020; 107: 102355
    CrossrefPubMedSearch in Google Scholar
  • 92 Fauchais AL, Lambert M, Launay D. et al. Antiphospholipid antibodies in primary Sjögren's syndrome: prevalence and clinical significance in a series of 74 patients. Lupus 2004; 13 (04) 245-248
    CrossrefPubMedSearch in Google Scholar
  • 93 Merashli M, Alves J, Ames PRJ. Clinical relevance of antiphospholipid antibodies in systemic sclerosis: a systematic review and meta-analysis. Semin Arthritis Rheum 2017; 46 (05) 615-624
    CrossrefPubMedSearch in Google Scholar
  • 94 Olech E, Merrill JT. The prevalence and clinical significance of antiphospholipid antibodies in rheumatoid arthritis. Curr Rheumatol Rep 2006; 8 (02) 100-108
    CrossrefPubMedSearch in Google Scholar
  • 95 Wolf P, Gretler J, Aglas F, Auer-Grumbach P, Rainer F. Anticardiolipin antibodies in rheumatoid arthritis: their relation to rheumatoid nodules and cutaneous vascular manifestations. Br J Dermatol 1994; 131 (01) 48-51
    CrossrefPubMedSearch in Google Scholar
  • 96 Jeleniewicz R, Majdan M, Targońska-Stępniak B, Dryglewska M. Prevalence of antiphospholipid antibodies in rheumatoid arthritis patients and relationship with disease activity. Pol Arch Med Wewn 2012; 122 (10) 480-486
    CrossrefPubMedSearch in Google Scholar
  • 97 Sherer Y, Livneh A, Levy Y, Shoenfeld Y, Langevitz P. Dermatomyositis and polymyositis associated with the antiphospholipid syndrome-a novel overlap syndrome. Lupus 2000; 9 (01) 42-46
    CrossrefPubMedSearch in Google Scholar
  • 98 Petri M, Kim MY, Kalunian KC. et al; OC-SELENA Trial. Combined oral contraceptives in women with systemic lupus erythematosus. N Engl J Med 2005; 353 (24) 2550-2558
    CrossrefPubMedSearch in Google Scholar
  • 99 Girolami A, Zanon E, Zanardi S, Saracino MA, Simioni P. Thromboembolic disease developing during oral contraceptive therapy in young females with antiphospholipid antibodies. Blood Coagul Fibrinolysis 1996; 7 (04) 497-501
    CrossrefPubMedSearch in Google Scholar
  • 100 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
    CrossrefPubMedSearch in Google Scholar
  • 101 Conard J, Plu-Bureau G, Bahi N, Horellou MH, Pelissier C, Thalabard JC. Progestogen-only contraception in women at high risk of venous thromboembolism. Contraception 2004; 70 (06) 437-441
    CrossrefPubMedSearch in Google Scholar
  • 102 Sammaritano LR. Which hormones and contraception for women with APS? Exogenous hormone use in women with APS. Curr Rheumatol Rep 2021; 23 (06) 44
    CrossrefPubMedSearch in Google Scholar
  • 103 Sammaritano LR. Contraception in patients with systemic lupus erythematosus and antiphospholipid syndrome. Lupus 2014; 23 (12) 1242-1245
    CrossrefPubMedSearch in Google Scholar
  • 104 Asscheman H, Giltay EJ, Megens JA, de Ronde WP, van Trotsenburg MA, Gooren LJ. A long-term follow-up study of mortality in transsexuals receiving treatment with cross-sex hormones. Eur J Endocrinol 2011; 164 (04) 635-642
    CrossrefPubMedSearch in Google Scholar
  • 105 Goldstein Z, Khan M, Reisman T, Safer JD. Managing the risk of venous thromboembolism in transgender adults undergoing hormone therapy. J Blood Med 2019; 10: 209-216
    CrossrefPubMedSearch in Google Scholar
  • 106 Weinand JD, Safer JD. Hormone therapy in transgender adults is safe with provider supervision; a review of hormone therapy sequelae for transgender individuals. J Clin Transl Endocrinol 2015; 2 (02) 55-60
    PubMedSearch in Google Scholar
  • 107 Park J, Armstrong GW, Cestari DM. Spontaneous superior ophthalmic vein thrombosis in a transgender man with systemic lupus erythematosus. LGBT Health 2019; 6 (04) 202-204
    CrossrefPubMedSearch in Google Scholar
  • 108 Garcia D, Akl EA, Carr R, Kearon C. Antiphospholipid antibodies and the risk of recurrence after a first episode of venous thromboembolism: a systematic review. Blood 2013; 122 (05) 817-824
    CrossrefPubMedSearch in Google Scholar
  • 109 Niznik S, Rapoport MJ, Avnery O. et al. Patterns of recurrent thrombosis in primary antiphospholipid syndrome-multicenter, real-life long-term follow-up. Front Immunol 2022; 13: 843718
    CrossrefPubMedSearch in Google Scholar
  • 110 Tincani A, Taraborelli M, Cattaneo R. Antiphospholipid antibodies and malignancies. Autoimmun Rev 2010; 9 (04) 200-202
    CrossrefPubMedSearch in Google Scholar
  • 111 Pusterla S, Previtali S, Marziali S. et al. Antiphospholipid antibodies in lymphoma: prevalence and clinical significance. Hematol J 2004; 5 (04) 341-346
    CrossrefPubMedSearch in Google Scholar
  • 112 Pham C, Shen YM. Antiphospholipid antibodies and malignancy. Hematol Oncol Clin North Am 2008; 22 (01) 121-130 , vii
    CrossrefPubMedSearch in Google Scholar
  • 113 Yoon KH, Wong A, Shakespeare T, Sivalingam P. High prevalence of antiphospholipid antibodies in Asian cancer patients with thrombosis. Lupus 2003; 12 (02) 112-116
    CrossrefPubMedSearch in Google Scholar
  • 114 Favaloro EJ, Henry BM, Lippi G. Is lupus anticoagulant a significant feature of COVID-19? A critical appraisal of the literature. Semin Thromb Hemost 2022; 48 (01) 55-71
    Thieme ConnectPubMedSearch in Google Scholar
  • 115 Novelli L, Motta F, De Santis M, Ansari AA, Gershwin ME, Selmi C. The JANUS of chronic inflammatory and autoimmune diseases onset during COVID-19 - a systematic review of the literature. J Autoimmun 2021; 117: 102592
    CrossrefPubMedSearch in Google Scholar
  • 116 Gazzaruso C, Mariani G, Ravetto C. et al. Lupus anticoagulant and mortality in patients hospitalized for COVID-19. J Thromb Thrombolysis 2021; 52 (01) 85-91
    CrossrefPubMedSearch in Google Scholar
  • 117 Favaloro EJ, Henry BM, Lippi G. COVID-19 and antiphospholipid antibodies: time for a reality check?. Semin Thromb Hemost 2022; 48 (01) 72-92
    Thieme ConnectPubMedSearch in Google Scholar
  • 118 Hamadé A, Woehl B, Harzallah I, Talbot M, Tousch J, Jambert L. Antiphospholipid antibodies in patients with coronavirus disease 2019 infection hospitalized in conventional unit. Blood Coagul Fibrinolysis 2021; 32 (02) 73-79
    CrossrefPubMedSearch in Google Scholar
  • 119 Le Joncour A, Frere C, Martin-Toutain I. et al. Antiphospholipid antibodies and thrombotic events in COVID-19 patients hospitalized in medicine ward. Autoimmun Rev 2021; 20 (02) 102729
    CrossrefPubMedSearch in Google Scholar
  • 120 Štok U, Čučnik S, Sodin-Šemrl S, Žigon P. Extracellular vesicles and antiphospholipid syndrome: state-of-the-art and future challenges. Int J Mol Sci 2021; 22 (09) 4689
    CrossrefPubMedSearch in Google Scholar
  • 121 Riancho-Zarrabeitia L, Cubería M, Muñoz P. et al. Vitamin D and antiphospholipid syndrome: a retrospective cohort study and meta-analysis. Semin Arthritis Rheum 2018; 47 (06) 877-882
    CrossrefPubMedSearch in Google Scholar
  • 122 Andreoli L, Piantoni S, Dall'Ara F, Allegri F, Meroni PL, Tincani A. Vitamin D and antiphospholipid syndrome. Lupus 2012; 21 (07) 736-740
    CrossrefPubMedSearch in Google Scholar
  • 123 Bełtowski J, Atanassova P, Chaldakov GN, Jamroz-Wiśniewska A, Kula W, Rusek M. Opposite effects of pravastatin and atorvastatin on insulin sensitivity in the rat: role of vitamin D metabolites. Atherosclerosis 2011; 219 (02) 526-531
    CrossrefPubMedSearch in Google Scholar
  • 124 Rosa Dos Santos AP, de Oliveira Vaz C, Hounkpe BW. et al. Association between interferon-I producing plasmacytoid dendritic cells and thrombotic antiphospholipid syndrome. Lupus 2022; 31 (09) 1067-1077
    CrossrefPubMedSearch in Google Scholar
  • 125 Xourgia E, Tektonidou MG. Type I interferon gene expression in antiphospholipid syndrome: pathogenetic, clinical and therapeutic implications. J Autoimmun 2019; 104: 102311
    CrossrefPubMedSearch in Google Scholar