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Volume 2012 (2012), Article ID 428269, 6 pages
Thrombosis in Systemic Lupus Erythematosus: A Review Article
College of Medicine, Imam Muhammad Ibn Saud Islamic University, P.O. Box 75227, Riyadh 11578, Saudi Arabia
Received 19 April 2012; Accepted 20 June 2012
Academic Editors: M. G. Danieli, J. Ioannou, G. Murdaca, and B. Ongphiphadhanakul
Copyright © 2012 Ibrahim A. Al-Homood. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- I. O. Tassiulas and D. T. Boumpas, “Clinical features and treatment of systemic lupus erythematosus,” in Textbook of Rheumatology, G. S. Firestein and W. N. Kelley, Eds., Saunders/Elsevier, Philadelphia, Pa, USA, 8th edition, 2009.
- S. P. Ballou, M. A. Khan, and I. Kushner, “Clinical features of systemic lupus erythematosus. Differences related to race and age of onset,” Arthritis and Rheumatism, vol. 25, no. 1, pp. 55–60, 1982.
- R. C. Lawrence, C. G. Helmick, F. C. Arnett et al., “Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States,” Arthritis and Rheumatism, vol. 41, no. 5, pp. 778–799, 1998.
- A. S. Al-Arfaj, S. R. Al-Balla, A. N. Al-Dalaan et al., “Prevalence of systemic lupus erythematosus in central Saudi Arabia,” Saudi Medical Journal, vol. 23, no. 1, pp. 87–89, 2002.
- A. Afeltra, M. Vadacca, L. Conti et al., “Thrombosis in systemic lupus erythematosus: congenital and acquired risk factors,” Arthritis Care and Research, vol. 53, no. 3, pp. 452–459, 2005.
- C. C. Mok, S. S. K. Tang, C. H. To, and M. Petri, “Incidence and risk factors of thromboembolism in systemic lupus erythematosus: a comparison of three ethnic groups,” Arthritis and Rheumatism, vol. 52, no. 9, pp. 2774–2782, 2005.
- Z. S. Sarabi, E. Chang, R. Bobba et al., “Incidence rates of arterial and venous thrombosis after diagnosis of systemic lupus erythematosus.,” Arthritis and Rheumatism, vol. 53, no. 4, pp. 609–612, 2005.
- J. Romero-Díaz, I. García-Sosa, and J. Sánchez-Guerrero, “Thrombosis in systemic lupus erythematosus and other autoimmune diseases of recent onset,” Journal of Rheumatology, vol. 36, no. 1, pp. 68–75, 2009.
- R. Cervera, M. A. Khamashta, J. Font et al., “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, vol. 82, no. 5, pp. 299–308, 2003.
- K. Manger, B. Manger, R. Repp et al., “Definition of risk factors for death, end stage renal disease, and thromboembolic events in a monocentric cohort of 338 patients with systemic lupus erythematosus,” Annals of the Rheumatic Diseases, vol. 61, no. 12, pp. 1065–1070, 2002.
- P. E. Love and S. A. Santoro, “Antiphospholipid antibodies: anticardiolipin and the lupus anticoagulant in systemic lupus erythematosus (SLE) and in non-SLE disorders. Prevalence and clinical significance,” Annals of Internal Medicine, vol. 112, no. 9, pp. 682–698, 1990.
- M. Petri, “The lupus anticoagulant is a risk factor for myocardial infarction (but not atherosclerosis): Hopkins Lupus Cohort,” Thrombosis Research, vol. 114, no. 5-6, pp. 593–595, 2004.
- C. C. Mok, C. S. Lau, and R. W. S. Wong, “Neuropsychiatric manifestations and their clinical associations in southern Chinese patients with systemic lupus erythematosus,” Journal of Rheumatology, vol. 28, no. 4, pp. 766–771, 2001.
- A. Amoroso, A. P. Mitterhofer, F. Del Porto et al., “Antibodies to anionic phospholipids and anti-β2-GPI: association with thrombosis and thrombocytopenia in systemic lupus erythematosus,” Human Immunology, vol. 64, no. 2, pp. 265–273, 2003.
- C. T. Esmon, “The impact of the inflammatory response on coagulation,” Thrombosis Research, vol. 114, no. 5-6, pp. 321–327, 2004.
- T. S. Edgington, N. Mackman, K. Brand, and W. Ruf, “The structural biology of expression and function of tissue factor,” Thrombosis and Haemostasis, vol. 66, no. 1, pp. 67–79, 1991.
- J. Cermak, N. S. Key, R. R. Bach, J. Balla, H. S. Jacob, and G. M. Vercellotti, “C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor,” Blood, vol. 82, no. 2, pp. 513–520, 1993.
- C. Dosquet, D. Weill, and J. L. Wautier, “Cytokines and thrombosis,” Journal of Cardiovascular Pharmacology, vol. 25, no. 2, pp. S13–S19, 1995.
- S. Devaraj, D. Y. Xu, and I. Jialal, “C-reactive protein increases plasminogen activator inhibitor-1 expression and activity in human aortic endothelial cells: implications for the metabolic syndrome and atherothrombosis.,” Circulation, vol. 107, no. 3, pp. 398–404, 2003.
- S. R. Lentz, M. Tsiang, and J. E. Sadler, “Regulation of thrombomodulin by tumor necrosis factor-α: comparison of transcriptional and posttranscriptional mechanisms,” Blood, vol. 77, no. 3, pp. 542–550, 1991.
- K. L. Moore, C. T. Esmon, and N. L. Esmon, “Tumor necrosis factor leads to the internalization and degradation of thrombomodulin from the surface of bovine aortic endothelium cells in culture,” Blood, vol. 73, no. 1, pp. 159–165, 1989.
- E. M. Conway and R. D. Rosenberg, “Tumor necrosis factor suppresses transcription of the thrombomodulin gene in endothelial cells,” Molecular and Cellular Biology, vol. 8, no. 12, pp. 5588–5592, 1988.
- R. Kerr, D. Stirling, and C. A. Ludlam, “Interleukin 6 and haemostasis,” British Journal of Haematology, vol. 115, no. 1, pp. 3–12, 2001.
- B. K. Mahmoodi, M. K. Ten Kate, F. Waanders et al., “High absolute risks and predictors of venous and arterial thromboembolic events in patients with nephrotic syndrome: results from a large retrospective cohort study,” Circulation, vol. 117, no. 2, pp. 224–230, 2008.
- P. Bucciarelli, F. R. Rosendaal, A. Tripodi et al., “Risk of venous thromboembolism and clinical manifestations in carriers of antithrombin, protein C, protein S deficiency, or activated protein C resistance: a multicenter collaborative family study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 19, no. 4, pp. 1026–1033, 1999.
- D. A. Lane, P. M. Mannucci, K. A. Bauer et al., “Inherited thrombophilia: part 1,” Thrombosis and Haemostasis, vol. 76, no. 5, pp. 651–662, 1996.
- B. Dahlback, M. Carlsson, and P. J. Svensson, “Familial thrombophilia due to a previously unrecognized mechanism characterized by poor anticoagulant response to activated protein C: prediction of a cofactor to activated protein C,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 3, pp. 1004–1008, 1993.
- V. De Stefano, I. Martinelli, P. M. Mannucci et al., “The risk of recurrent deep venous thrombosis among heterozygous carriers of both factor V Leiden and the G20210A prothrombin mutation,” New England Journal of Medicine, vol. 341, no. 11, pp. 801–806, 1999.
- I. Martinelli, P. Bucciarelli, M. Margaglione, V. De Stefano, G. Castaman, and P. M. Mannucci, “The risk of venous thromboembolism in family members with mutations in the genes of factor V or prothrombin or both,” British Journal of Haematology, vol. 111, no. 4, pp. 1223–1229, 2000.
- S. Ehrenforth, K. P. Radtke, and I. Scharrer, “Acquired activated protein C-resistance in patients with lupus anticoagulants,” Thrombosis and Haemostasis, vol. 74, no. 2, pp. 797–798, 1995.
- M. Martinuzzo, R. Forastiero, Y. Adamczuk, G. Cerrato, and L. O. Carreras, “Activated protein C resistance in patients with anti-β2 glycoprotein I antibodies,” Blood Coagulation and Fibrinolysis, vol. 7, no. 7, pp. 702–704, 1996.
- G. J. Ruiz-Argüelles, J. Garcés-Eisele, D. Alarcón-Segovia, and A. Ruiz-Argüelles, “Activated protein C resistance phenotype and genotype in patients with primary antiphospholipid syndrome,” Blood Coagulation and Fibrinolysis, vol. 7, no. 3, pp. 344–348, 1996.
- J. Aznar, P. Villa, F. España, A. Estellés, S. Grancha, and C. Falcó, “Activated protein C resistance phenotype in patients with antiphospholipid antibodies,” Journal of Laboratory and Clinical Medicine, vol. 130, no. 2, pp. 202–208, 1997.
- U. Picillo, D. De Lucia, E. Palatiello et al., “Association of primary antiphospholipid syndrome with inherited activated protein C resistance,” Journal of Rheumatology, vol. 25, no. 6, pp. 1232–1234, 1998.
- C. Male, L. Mitchell, J. Julian et al., “Acquired activated protein C resistance is associated with lupus anticoagulants and thrombotic events in pediatric patients with systemic lupus erythematosus,” Blood, vol. 97, no. 4, pp. 844–849, 2001.
- S. S. Shapiro and S. E. F. Spurgeon, “Hematology: coagulation problems,” in Systemic Lupus Erythematosus, R. G. Lahita, Ed., vol. 7, pp. 1144–1145, Elsevier Academic Press, San Diego, Calif, USA, 4th edition, 2004.
- S. R. Poort, F. R. Rosendaal, P. H. Reitsma, and R. M. Bertina, “A common genetic variation in the 3'-untranslated region of the prothrombin gene is associated with elevated plasma prothrombin levels and an increase in venous thrombosis,” Blood, vol. 88, no. 10, pp. 3698–3703, 1996.
- M. Den Heijer and M. B. A. J. Keijzer, “Hyperhomocysteinemia as a risk factor for venous thrombosis,” Clinical Chemistry and Laboratory Medicine, vol. 39, no. 8, pp. 710–713, 2001.
- K. K. Sallai, E. Nagy, I. Bodó, A. Mohl, and P. Gergely, “Thrombosis risk in systemic lupus erythematosus: the role of thrombophilic risk factors,” Scandinavian Journal of Rheumatology, vol. 36, no. 3, pp. 198–205, 2007.
- N. O. Ghaussy, W. L. Sibbitt, A. D. Bankhurst, and C. R. Qualls, “Cigarette smoking and disease activity in systemic lupus erythematosus,” Journal of Rheumatology, vol. 30, no. 6, pp. 1215–1221, 2003.
- M. M. Ward and S. Studenski, “Clinical prognostic factors in lupus nephritis: the importance of hypertension and smoking,” Archives of Internal Medicine, vol. 152, no. 10, pp. 2082–2088, 1992.
- I. Turchin, S. Bernatsky, A. E. Clarke, Y. St-Pierre, and C. A. Pineau, “Cigarette smoking and cutaneous damage in systemic lupus erythematosus,” Journal of Rheumatology, vol. 36, no. 12, pp. 2691–2693, 2009.
- S. J. Jay and S. R. Kahn, “Cigarette smoking: risk factor for venous thromboembolic disease?” Archives of Internal Medicine, vol. 159, no. 10, p. 1144, 1999.
- S. R. Kahn, “The clinical diagnosis of deep venous thrombosis: integrating incidence, risk factors, and symptoms and signs,” Archives of Internal Medicine, vol. 158, no. 21, pp. 2315–2323, 1998.
- P. O. Hansson, H. Eriksson, L. Welin, K. Svärdsudd, and L. Wilhelmsen, “Smoking and abdominal obesity: risk factors for venous thromboembolism among middle-aged men: “The study of men born in 1913”,” Archives of Internal Medicine, vol. 159, no. 16, pp. 1886–1890, 1999.
- A. Danowski, M. N. L. De Azevedo, J. A. D. S. Papi, and M. Petri, “Determinants of risk for venous and arterial thrombosis in primary antiphospholipid syndrome and in antiphospholipid syndrome with systemic lupus erythematosus,” Journal of Rheumatology, vol. 36, no. 6, pp. 1195–1199, 2009.
- M. Petri, “Thrombosis and systemic lupus erythematosus: the hopkins lupus cohort perspective,” Scandinavian Journal of Rheumatology, vol. 25, no. 4, pp. 191–193, 1996.
- S. M. A. Toloza, A. G. Uribe, G. McGwin et al., “Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXIII. Baseline predictors of vascular events,” Arthritis and Rheumatism, vol. 50, no. 12, pp. 3947–3957, 2004.
- J. Calvo-Alén, S. M. A. Toloza, M. Fernández et al., “Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXV. Smoking, older age, disease activity, lupus anticoagulant, and glucocorticoid dose as risk factors for the occurrence of venous thrombosis in lupus patients,” Arthritis and Rheumatism, vol. 52, no. 7, pp. 2060–2068, 2005.
- M. J. Roman, B. A. Shanker, A. Davis et al., “Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus,” New England Journal of Medicine, vol. 349, no. 25, pp. 2399–2406, 2003.
- V. Bykerk, J. Sampalis, J. M. Esdaile et al., “A randomized study of the effect of withdrawing hydroxychloroquine sulfate in systemic lupus erythematosus,” New England Journal of Medicine, vol. 324, no. 3, pp. 150–154, 1991.
- K. H. Yoon, “Sufficient evidence to consider hydroxychloroquine as an adjunct therapy in antiphospholipid antibody (Hughes') syndrome,” Journal of Rheumatology, vol. 29, no. 7, pp. 1574–1575, 2002.
- M. H. Edwards, S. Pierangeli, X. Liu, J. H. Barker, G. Anderson, and E. Nigel Harris, “Hydroxychloroquine reverses thrombogenic properties of antiphospholipid antibodies in mice,” Circulation, vol. 96, no. 12, pp. 4380–4384, 1997.
- S. S. Pierangeli, M. Vega-Ostertag, and E. Nigel Harris, “Intracellular signaling triggered by antiphospholipid antibodies in platelets and endothelial cells: a pathway to targeted therapies,” Thrombosis Research, vol. 114, no. 5-6, pp. 467–476, 2004.
- M. G. Tektonidou, K. Laskari, D. B. Panagiotakos, and H. M. Moutsopoulos, “Risk factors for thrombosis and primary thrombosis prevention in patients with systemic lupus erythematosus with or without antiphospholipid antibodies,” Arthritis Care and Research, vol. 61, no. 1, pp. 29–36, 2009.
- T. Tarr, G. Lakos, H. P. Bhattoa et al., “Clinical thrombotic manifestations in SLE patients with and without antiphospholipid antibodies: a 5-year follow-up,” Clinical Reviews in Allergy and Immunology, vol. 32, no. 2, pp. 131–137, 2007.
- D. Erkan, Y. Yazici, M. G. Peterson, L. Sammaritano, and M. D. Lockshin, “A cross-sectional study of clinical thrombotic risk factors and preventive treatments in antiphospholipid syndrome,” Rheumatology, vol. 41, no. 8, pp. 924–929, 2002.
- G. K. Bertsias, J. P. A. Ioannidis, M. Aringer 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,” Annals of the Rheumatic Diseases, vol. 69, no. 12, pp. 2074–2082, 2010.
- R. H. W. M. Derksen, P. G. De Groot, L. Kater, and H. K. Nieuwenhuis, “Patients with antiphospholipid antibodies and venous thrombosis should receive long term anticoagulant treatment,” Annals of the Rheumatic Diseases, vol. 52, no. 9, pp. 689–692, 1993.
- G. Finazzi, V. Brancaccio, P. Schinco et al., “A randomized clinical trial of high-intensity warfarin vs. conventional antithrombotic therapy for the prevention of recurrent thrombosis in patients with the antiphospholipid syndrome (WAPS),” Journal of Thrombosis and Haemostasis, vol. 3, no. 5, pp. 848–853, 2005.
- M. A. Crowther, J. S. Ginsberg, J. Julian et al., “A comparison of two intensities of warfarin for the prevention of recurrent thrombosis in patients with the antiphospholipid antibody syndrome,” New England Journal of Medicine, vol. 349, no. 12, pp. 1133–1138, 2003.
- G. Ruiz-Irastorza, B. J. Hunt, and M. A. Khamashta, “A systematic review of secondary thromboprophylaxis in patients with antiphospholipid antibodies,” Arthritis Care and Research, vol. 57, no. 8, pp. 1487–1495, 2007.