Loading...
 
Mediterr J Rheumatol 2017;28(1):20-6
Lupus thrombocytopenia: pathogenesis and therapeutic implications
Authors Information

1: Outpatient Department of Rheumatology, University General Hospital of Evros (Alexandroupolis), Thrace, Greece

2: Department of Haematology, Democritus University of Thrace, Alexandroupolis, Greece
References
  1. Hepburn A L, Narat S, Mason J C. The management of peripheral blood cytopenias in systemic lupus erythematosus. Rheumatology (Oxford) 2010;49:2243-54.
  2. Fayyaz A, Igoe A, Kurien B T, Danda D, James J A, Stafford H A, et al. Haematological manifestations of lupus. Lupus Sci Med 2015;2:e000078.
  3. Feletar M, Ibanez D, Urowitz M B, Gladman D D. The impact of the 1997 update of the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus: what has been changed? Arthritis Rheum 2003;48:2067-9.
  4. Petri M, Orbai A M, Alarcon G S, Gordon C, Merrill J T, Fortin P R, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 2012;64:2677-86.
  5. Tan E M, Cohen A S, Fries J F, Masi A T, McShane D J, Rothfield N F, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7.
  6. Cervera R, Khamashta M A, Font J, Sebastiani G D, Gil A, Lavilla P, 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 (Baltimore) 2003;82:299-308.
  7. Mok C C, Lee K W, Ho C T, Lau C S, Wong R W. A prospective study of survival and prognostic indicators of systemic lupus erythematosus in a southern Chinese population. Rheumatology (Oxford) 2000;39:399-406.
  8. Vila L M, Alarcon G S, McGwin G, Jr., Friedman A W, Baethge B A, Bastian HM, et al. Early clinical manifestations, disease activity and damage of systemic lupus erythematosus among two distinct US Hispanic subpopulations. Rheumatology (Oxford) 2004;43:358-63.
  9. Mestanza-Peralta M, Ariza-Ariza R, Cardiel M H, Alcocer-Varela J. Thrombocytopenic purpura as initial manifestation of systemic lupus erythematosus. J Rheumatol 1997;24:867-70.
  10. Rabinowitz Y, Dameshek W. Systemic Lupus Erythematosus after “idiopathic” thrombocytopenic purpura: a review. A study of systemic lupus erythematosus occurring after 78 splenectomies for "idiopathic" thrombocytopenic purpura, with a review of the pertinent literature*†. Ann Intern Med 1960;52:1-28.
  11. Sultan S M, Begum S, Isenberg D A. Prevalence, patterns of disease and outcome in patients with systemic lupus erythematosus who develop severe haematological problems. Rheumatology (Oxford) 2003;42:230-4.
  12. Ziakas P D, Giannouli S, Zintzaras E, Tzioufas A G, Voulgarelis M. Lupus thrombocytopenia: clinical implications and prognostic significance. Ann Rheum Dis 2005;64:1366-9.
  13. Nesher G, Hanna V E, Moore T L, Hersh M, Osborn T G. Thrombotic microangiographic hemolytic anemia in systemic lupus erythematosus. Semin Arthritis Rheum 1994;24:165-72.
  14. Vaidya S, Abul-ezz S, Lipsmeyer E. Thrombotic thrombocytopenic purpura and systemic lupus erythematosus. Scand J Rheumatol 2001;30:308-10.
  15. Dhote R, Simon J, Papo T, Detournay B, Sailler L, Andre M H, et al. Reactive hemophagocytic syndrome in adult systemic disease: report of twenty-six cases and literature review. Arthritis Rheum 2003;49:633-9.
  16. Pistiner M, Wallace D J, Nessim S, Metzger A L, Klinenberg JR. Lupus erythematosus in the 1980s: a survey of 570 patients. Semin Arthritis Rheum 1991;21:55-64.
  17. Nossent J, Swaak A. Prevalence and Significance of Haematological Abnormalities in Patients with Systemic Lupus Erythematosus. QJM 1991;80:605-12.
  18. Miller M H, Urowitz M B, Gladman D D. The significance of thrombocytopenia in systemic lupus erythematosus. Arthritis Rheum 1983;26:1181-6.
  19. Alger M, Alarcon-Segovia D, Rivero S J. Hemolytic anemia and thrombocytopenic purpura: two related subsets of systemic lupus erythematosus. J Rheumatol 1977;4:351-7.
  20. Reveille J D, Bartolucci A, Alarcon G S. Prognosis in systemic lupus erythematosus. Negative impact of increasing age at onset, black race, and thrombocytopenia, as well as causes of death. Arthritis Rheum 1990;33:37-48.
  21. Sestak A L, Shaver T S, Moser K L, Neas B R, Harley J B. Familial aggregation of lupus and autoimmunity in an unusual multiplex pedigree. J Rheumatol 1999;26:1495-9.
  22. Scofield R H, Bruner G R, Kelly J A, Kilpatrick J, Bacino D, Nath S K, et al. Thrombocytopenia identifies a severe familial phenotype of systemic lupus erythematosus and reveals genetic linkages at 1q22 and 11p13. Blood 2003;101:992-7.
  23. Lipp E, von Felten A, Sax H, Muller D, Berchtold P. Antibodies against platelet glycoproteins and antiphospholipid antibodies in autoimmune thrombocytopenia. Eur J Haematol 1998;60:283-8.
  24. Michel M, Lee K, Piette J C, Fromont P, Schaeffer A, Bierling P, et al. Platelet autoantibodies and lupus-associated thrombocytopenia. Br J Haematol 2002;119:354-8.
  25. Ziakas P D, Routsias J G, Giannouli S, Tasidou A, Tzioufas A G, Voulgarelis M. Suspects in the tale of lupus-associated thrombocytopenia. Clin Exp Immunol 2006;145:71-80.
  26. Macchi L, Rispal P, Clofent-Sanchez G, Pellegrin J L, Nurden P, Leng B, et al. Anti-platelet antibodies in patients with systemic lupus erythematosus and the primary antiphospholipid antibody syndrome: their relationship with the observed thrombocytopenia. Br J Haematol 1997;98:336-41.
  27. Diz-Kucukkaya R, Hacihanefioglu A, Yenerel M, Turgut M, Keskin H, Nalcaci M, et al. Antiphospholipid antibodies and antiphospholipid syndrome in patients presenting with immune thrombocytopenic purpura: a prospective cohort study. Blood 2001;98:1760-4.
  28. Fureder W, Firbas U, Nichol J L, Pistillo J, Winkler S, Hiesberger H, et al. Serum thrombopoietin levels and anti-thrombopoietin antibodies in systemic lupus erythematosus. Lupus 2002;11:221-6.
  29. Kuwana M, Okazaki Y, Kajihara M, Kaburaki J, Miyazaki H, Kawakami Y, et al. Autoantibody to c-Mpl (thrombopoietin receptor) in systemic lupus erythematosus: relationship to thrombocytopenia with megakaryocytic hypoplasia. Arthritis Rheum 2002;46:2148-59.
  30. Kuwana M, Kaburaki J, Okazaki Y, Miyazaki H, Ikeda Y. Two types of autoantibody-mediated thrombocytopenia in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2006;45:851-4.
  31. Nojima J, Kuratsune H, Suehisa E, Futsukaichi Y, Yamanishi H, Machii T, et al. Association between the prevalence of antibodies to beta(2)-glycoprotein I, prothrombin, protein C, protein S, and annexin V in patients with systemic lupus erythematosus and thrombotic and thrombocytopenic complications. Clin Chem 2001;47:1008-15.
  32. Munoz-Rodriguez F J, Reverter J C, Font J, Tassies D, Cervera R, Espinosa G, et al. Prevalence and clinical significance of antiprothrombin antibodies in patients with systemic lupus erythematosus or with primary antiphospholipid syndrome. Haematologica 2000;85:632-7.
  33. Abu-Shakra M, Gladman D D, Urowitz M B, Farewell V. Anticardiolipin antibodies in systemic lupus erythematosus: clinical and laboratory correlations. Am J Med 1995;99:624-8.
  34. Rupin A, Gruel Y, Poumier-Gaschard P, Chassaigne M, Leroy J, Bardos P. Thrombocytopenia in systemic lupus erythematosus: association with antiplatelet and anticardiolipin antibodies. Clin Immunol Immunopathol 1990;55:418-26.
  35. Fabris F, Steffan A, Cordiano I, Borzini P, Luzzatto G, Randi M L, et al. Specific antiplatelet autoantibodies in patients with antiphospholipid antibodies and thrombocytopenia. Eur J Haematol 1994;53:232-6.
  36. Arnout J, Vermylen J. Current status and implications of autoimmune antiphospholipid antibodies in relation to thrombotic disease. J Thromb Haemost 2003;1:931-42.
  37. Nakamura M, Tanaka Y, Satoh T, Kawai M, Hirakata M, Kaburaki J, et al. Autoantibody to CD40 ligand in systemic lupus erythematosus: association with thrombocytopenia but not thromboembolism. Rheumatology (Oxford) 2006;45:150-6.
  38. Hepburn A L, Lampert I A, Boyle J J, Horncastle D, Ng W F, Layton M, et al. In vivo evidence for apoptosis in the bone marrow in systemic lupus erythematosus. Ann Rheum Dis 2007;66:1106-9.
  39. Jung J H, Soh M S, Ahn Y H, Um Y J, Jung J Y, Suh C H, et al. Thrombocytopenia in Systemic Lupus Erythematosus: Clinical Manifestations, Treatment, and Prognosis in 230 Patients. Medicine 2016;95:e2818.
  40. Badsha H, Kong K O, Lian T Y, Chan S P, Edwards C J, Chng H H. Low-dose pulse methylprednisolone for systemic lupus erythematosus flares is efficacious and has a decreased risk of infectious complications. Lupus 2002;11:508-13.
  41. Arnal C, Piette J C, Leone J, Taillan B, Hachulla E, Roudot-Thoraval F, et al. Treatment of severe immune thrombocytopenia associated with systemic lupus erythematosus: 59 cases. J Rheumatol 2002;29:75-83.
  42. Neunert C, Lim W, Crowther M, Cohen A, Solberg L, Crowther M A. The American Society of Hematology 2011 evidence-based practice guideline for immune thrombocytopenia. Blood 2011;117:4190-207.
  43. Zandman-Goddard G, Levy Y, Shoenfeld Y. Intravenous immunoglobulin therapy and systemic lupus erythematosus. Clin Rev Allergy Immunol 2005;29:219-28.
  44. Maeshima E, Kida Y, Goda M, Minami Y. A case of systemic lupus erythematosus expressing intractable thrombocytopenia remedied effectively by intermittent and continuous administrations of a small amount of immune globulin. Mod Rheumatol 2006;16:239-42.
  45. Khellaf M, Chabrol A, Mahevas M, Roudot-Thoraval F, Limal N, Languille L, et al. Hydroxychloroquine is a good second-line treatment for adults with immune thrombocytopenia and positive antinuclear antibodies. Am J Hematol 2014;89:194-8.
  46. Cervera H, Jara L J, Pizarro S, Enkerlin H L, Fernandez M, Medina F, et al. Danazol for systemic lupus erythematosus with refractory autoimmune thrombocytopenia or Evans' syndrome. J Rheumatol 1995;22:1867-71.
  47. Wong K L. Danazol in treatment of lupus thrombocytopenia. Asian Pac J Allergy Immunol 1991;9:125-9.
  48. Cines D B, Bussel J B. How I treat idiopathic thrombocytopenic purpura (ITP). Blood 2005;106:2244-51.
  49. Goebel K M, Gassel W D, Goebel F D. Evaluation of azathioprine in autoimmune thrombocytopenia and lupus erythematosus. Scand J Haematol 1973;10:28-34.
  50. Abu-Shakra M, Shoenfeld Y. Azathioprine therapy for patients with systemic lupus erythematosus. Lupus 2001;10:152-3.
  51. Manger K, Kalden J R, Manger B. Cyclosporin A in the treatment of systemic lupus erythematosus: results of an open clinical study. Br J Rheumatol 1996;35:669-75.
  52. Sekigawa I, Ogasawara H, Sugiyama M, Kaneko H, Hishikawa T, Tokano Y, et al. Extremely low dose treatment of cyclosporine for autoimmune diseases. Clin Exp Rheumatol 1998;16:352.
  53. Boumpas D T, Barez S, Klippel J H, Balow J E. Intermittent cyclophosphamide for the treatment of autoimmune thrombocytopenia in systemic lupus erythematosus. Ann Intern Med 1990;112:674-7.
  54. Park H J, Kang M I, Kang Y, Chung S J, Lee S W, Park Y B, et al. Two cases of refractory thrombocytopenia in systemic lupus erythematosus that responded to intravenous low-dose cyclophosphamide. J Korean Med Sci 2013;28:472-5.
  55. Chang H K. Successful treatment of refractory thrombocytopenia with mycophenolate mofetil in a patient with systemic lupus erythematosus. J Korean Med Sci 2005;20:883-5.
  56. Vasoo S, Thumboo J, Fong K Y. Refractory immune thrombocytopenia in systemic lupus erythematosus: response to mycophenolate mofetil. Lupus 2003;12:630-2.
  57. You Y N, Tefferi A, Nagorney D M. Outcome of splenectomy for thrombocytopenia associated with systemic lupus erythematosus. Ann Surg 2004;240:286-92.
  58. Vianelli N, Palandri F, Polverelli N, Stasi R, Joelsson J, Johansson E, et al. Splenectomy as a curative treatment for immune thrombocytopenia: a retrospective analysis of 233 patients with a minimum follow up of 10 years. Haematologica 2013;98:875-80.
  59. Alarcon-Segovia D. Splenectomy has a limited role in the management of lupus with thrombocytopenia. J Rheumatol 2002;29:1-2.
  60. Hall S, McCormick J L, Jr., Greipp P R, Michet C J, Jr., McKenna C H. Splenectomy does not cure the thrombocytopenia of systemic lupus erythematosus. Ann Intern Med 1985;102:325-8.
  61. Jiang B, Li T, Guo L, Shen H, Ye S, Chen S. Efficacy and Safety of Rituximab in Systemic Lupus Erythematosus and Sjogren Syndrome Patients With Refractory Thrombocytopenia: A Retrospective Study of 21 Cases. J Clin Rheumatol 2015;21:244-50.
  62. Gupta R K, Ezeonyeji A N, Thomas A S, Scully M A, Ehrenstein M R, Isenberg D A. A case of pure red cell aplasia and immune thrombocytopenia complicating systemic lupus erythematosus: response to rituximab and cyclophosphamide. Lupus 2011;20:1547-50.
  63. Lateef A, Lahiri M, Teng GG, Vasoo S. Use of rituximab in the treatment of refractory systemic lupus erythematosus: Singapore experience. Lupus 2010;19:765-70.
  64. Chen H, Zheng W, Su J, Xu D, Wang Q, Leng X, et al. Low-dose rituximab therapy for refractory thrombocytopenia in patients with systemic lupus erythematosus--a prospective pilot study. Rheumatology (Oxford) 2011;50:1640-4.
  65. Garcia-Carrasco M, Mendoza-Pinto C, Sandoval-Cruz M, Soto-Vega E, Beltran-Castillo A, Jimenez-Hernandez M, et al. Anti-CD20 therapy in patients with refractory systemic lupus erythematosus: a longitudinal analysis of 52 Hispanic patients. Lupus 2010;19:213-9.
  66. Reddy V, Cambridge G, Isenberg D A, Glennie M J, Cragg M S, Leandro M. Internalization of rituximab and the efficiency of B Cell depletion in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Rheumatol 2015;67:2046-55.
  67. Merrill J T, Neuwelt C M, Wallace D J, Shanahan J C, Latinis K M, Oates J C, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum 2010;62:222-33.
  68. Rovin B H, Furie R, Latinis K, Looney R J, Fervenza F C, Sanchez-Guerrero J, et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum 2012;64:1215-26.
  69. Ehrenstein M R, Wing C. The BAFFling effects of rituximab in lupus: danger ahead? Nat Rev Rheumatol 2016;12:367-72.
  70. Manzi S, Sanchez-Guerrero J, Merrill J T, Furie R, Gladman D, Navarra S V, et al. Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis 2012;71:1833-8.
  71. Cancro M P, D'Cruz D P, Khamashta M A. The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J Clin Invest 2009;119:1066-73.
  72. Wang B, Nichol J L, Sullivan J T. Pharmacodynamics and pharmacokinetics of AMG 531, a novel thrombopoietin receptor ligand. Clin Pharmacol Ther 2004;76:628-38.
  73. Bussel J B, Cheng G, Saleh M N, Psaila B, Kovaleva L, Meddeb B, et al. Eltrombopag for the treatment of chronic idiopathic thrombocytopenic purpura. N Engl J Med 2007;357:2237-47.
  74. Kuter D J, Bussel J B, Lyons R M, Pullarkat V, Gernsheimer T B, Senecal F M, et al. Efficacy of romiplostim in patients with chronic immune thrombocytopenic purpura: a double-blind randomised controlled trial. Lancet 2008;371:395-403.
  75. Gonzalez-Nieto J A, Martin-Suarez I, Quattrino S, Ortiz-Lopez E, Munoz-Beamud F R, Colchero-Fernandez J, et al. The efficacy of romiplostim in the treatment of severe thrombocytopenia associated to Evans syndrome refractory to rituximab. Lupus 2011;20:1321-3.
  76. Alkaabi J K, Alkindi S, Riyami N A, Zia F, Balla L M, Balla S M. Successful treatment of severe thrombocytopenia with romiplostim in a pregnant patient with systemic lupus erythematosus. Lupus 2012;21:1571-4.
  77. Tomov S, Lazarchick J, Self S E, Bruner E T, Budisavljevic M N. Kidney-limited thrombotic microangiopathy in patients with SLE treated with romiplostim. Lupus 2013;22:504-9.
  78. Maroun M C, Ososki R, Andersen J C, Dhar J P. Eltrombopag as steroid sparing therapy for immune thrombocytopenic purpura in systemic lupus erythematosus. Lupus 2015;24:746-50.
  79. Scheinberg P, Singulane C C, Barbosa L S, Scheinberg M. Successful platelet count recovery in lupus-associated thrombocytopenia with the thrombopoietin agonist eltrombopag. Clin Rheumatol 2014;33:1347-9.
  80. Cela I, Miller I J, Katz R S, Rizman A, Shammo J M. Successful treatment of amegakaryocytic thrombocytopenia with eltrombopag in a patient with systemic lupus erythematosus (SLE). Clin Adv Hematol Oncol 2010;8:806-9.
  81. Boulon C, Vircoulon M, Constans J. Eltrombopag in systemic lupus erythematosus with antiphospholipid syndrome: thrombotic events. Lupus 2016;25:331.