Antiphospholipid syndrome: Laboratory testing and diagnostic strategies

American Journal of Hematology

Volumn 87, Issue SUPPL. 1, 2012, Pages

  Ortel, Thomas L ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVITAMIN K; AUTOANTIBODY; BETA2 GLYCOPROTEIN 1; BLOOD CLOTTING FACTOR 10A INHIBITOR; CARDIOLIPIN; CARDIOLIPIN ANTIBODY; FONDAPARINUX; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; LA ANTIBODY; LIPOCORTIN 5; LOW MOLECULAR WEIGHT HEPARIN; PHOSPHOLIPID ANTIBODY; THROMBIN INHIBITOR; WARFARIN;

ANTIBODY BLOOD LEVEL; ANTIBODY DETECTION; ANTICOAGULATION; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; ASSAY; BLOOD CLOTTING TEST; BLOOD CLOTTING TIME; CLINICAL FEATURE; DISEASE CLASSIFICATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; KIDNEY DISEASE; LABORATORY DIAGNOSIS; LABORATORY TEST; LIVEDO RETICULARIS; LUPUS ERYTHEMATOSUS CELL TEST; PARTIAL THROMBOPLASTIN TIME; PRIORITY JOURNAL; PROTHROMBIN TIME; RISK ASSESSMENT; SERODIAGNOSIS; STANDARDIZATION; SYPHILIS; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOCYTOPENIA; VALVULAR HEART DISEASE; VEIN THROMBOSIS;

ANTIBODIES, ANTICARDIOLIPIN; ANTICOAGULANTS; ANTIPHOSPHOLIPID SYNDROME; EMBRYO LOSS; FEMALE; HEMATOLOGIC TESTS; HUMANS; LUPUS COAGULATION INHIBITOR; MALE; PREGNANCY; RECURRENCE; THROMBOEMBOLISM;

EID: 84860009240     PISSN: 03618609     EISSN: 10968652     Source Type: Journal    
DOI: 10.1002/ajh.23196     Document Type: Article

References (81)

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: 295-306.
2. Cervera R, Piette JC, Font J, et al. Antiphospholipid syndrome: Clinical and immunologic manifestations and patterns of disease expression in a cohort of 1, 000 patients. Arthritis Rheum 2002; 46: 1019-1027.
3. 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: 1309-1311.
4. Arad A, Proulle V, Furie RA, et al. beta-Glycoprotein-1 autoantibodies from patients with antiphospholipid syndrome are sufficient to potentiate arterial thrombus formation in a mouse model. Blood 2011; 117: 3453-3459.
5. Wasserman A. Uber die Entwicklung und den gegenwartigen Stand der Serodiagnostik gegenuber Syphilis. Berl Klin Wchnschr 1907; 44: 1599-1634.
6. Moore JE, Mohr CF. Biologically false positive serologic tests for syphilis: Type, incidence, and cause. J Am Med Assoc 1952; 150: 467-473.
7. Moore JE, Lutz WB. The natural history of systemic lupus erythematosus: An approach to its study through chronic biologic false positive reactors. J Chronic Dis 1955; 1: 297-316.
8. Conley CL, Hartmann RC. A hemorrhagic disorder caused by circulating anticoagulant in patients with disseminated lupus erythematosus. J Clin Invest 1952; 31: 621-622.
9. Lee SL, Sanders M. A disorder of blood coagulation in systemic lupus erythematosus. J Clin Invest 1955; 34: 1814-1822.
10. Pangborn MC. Isolation and purification of a serologically active phospholipid from beef heart. J Biol Chem 1942; 143: 247-256.
11. Laurell AB, Nilsson IM. Hypergammaglobulinemia, circulating anticoagulant, and biologic false positive Wassermann reaction: A study in two cases. J Lab Clin Med 1957; 49: 694-707.
12. Bowie EJ, Thompson JHJr, Pascuzzi CA, Owen CAJr. Thrombosis in systemic lupus erythematosus despite circulating anticoagulants. J Lab Clin Med 1963; 62: 416-430.
13. Manoharan A, Gibson L, Rush B, Feery BJ. Recurrent venous thrombosis with a "lupus" coagulation inhibitor in the absence of systemic lupus. Aust N Z J Med 1977; 7: 422-426.
14. Mueh JR, Herbst KD, Rapaport SI. Thrombosis in patients with the lupus anticoagulant. Ann Intern Med 1980; 92(2, Part 1): 156-159.
15. Feinstein DI, Rapaport SI. Acquired inhibitors of blood coagulation. Prog Hemost Thromb 1972; 1: 75-95.
16. Harris EN, Gharavi AE, Boey ML, et al. Anticardiolipin antibodies: Detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet 1983; 2: 1211-1214.
17. Loizou S, McCrea JD, Rudge AC, et al. Measurement of anti-cardiolipin antibodies by an enzyme-linked immunosorbent assay (ELISA): Standardization and quantitation of results. Clin Exp Immunol 1985; 62: 738-745.
18. Harris EN, Gharavi AE, Patel SP, Hughes GR. Evaluation of the anti-cardiolipin antibody test: Report of an international workshop held 4 April 1986. Clin Exp Immunol 1987; 68: 215-222.
19. Lakos G, Favaloro EJ, Harris EN, et al. International consensus guidelines on anticardiolipin and anti-beta(2) glycoprotein I testing: A report from the APL task force at the 13(th) international congress on antiphospholipid antibodies. Arthritis Rheum 2012; 64: 1-10.
20. Exner T, Triplett DA, Taberner D, Machin SJ. Guidelines for testing and revised criteria for lupus anticoagulants. SSC subcommittee for the standardization of lupus anticoagulants. Thromb Haemost 1991; 65: 320-322.
21. Brandt JT, Triplett DA, Alving B, Scharrer I. Criteria for the diagnosis of lupus anticoagulants: An update. On behalf of the subcommittee on lupus anticoagulant/antiphospholipid antibody of the scientific and standardisation committee of the ISTH. Thromb Haemost 1995; 74: 1185-1190.
22. Pengo V, Tripodi A, Reber G, et al. Update of the guidelines for lupus anticoagulant detection. Subcommittee on lupus anticoagulant/antiphospholipid antibody of the scientific and standardisation committee of the international society on thrombosis and haemostasis. J Thromb Haemost 2009; 7: 1737-1740.
23. Lupus Anticoagulant Working Party. Guidelines on testing for the lupus anticoagulant. J Clin Pathol 1991; 44: 885-889.
24. Loeliger A. Prothrombin as cofactor of circulating anticoagulant in systemic lupus erythematosus. Thromb Diath Haemorrh 1959; 3: 237-256.
25. Schleider MA, Nachman RL, Jaffe EA, Coleman M. A clinical study of the lupus anticoagulant. Blood 1976; 48: 499-509.
26. McNeil HP, Chesterman CN, Krilis SA. Anticardiolipin antibodies and lupus anticoagulants comprise separate antibody subgroups with different phospholipid binding characteristics. Br J Haematol 1989; 73: 506-513.
27. 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 USA 1990; 87: 4120-4124.
28. Galli M, Comfurius P, Maassen C, et al. Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet 1990; 335: 1544-1547.
29. Matsuura E, Igarashi Y, Fujimoto M, et al. Anticardiolipin cofactor(s) and differential diagnosis of autoimmune disease. Lancet 1990; 336: 177-178.
30. Schultze HE, Heide H, Haupt H. Naturwissenschaften 1961; 48: 719.
31. Lozier J, Takahashi N, Putnam FW. Complete amino acid sequence of human plasma beta 2-glycoprotein I. Proc Natl Acad Sci USA 1984; 81: 3640-3644.
32. Schwarzenbacher R, Zeth K, Diederichs K, et al. Crystal structure of human beta2-glycoprotein I: Implications for phospholipid binding and the antiphospholipid syndrome. EMBO J 1999; 18: 6228-6239.
33. Bu C, Gao L, Xie W, et al. beta2-glycoprotein i is a cofactor for tissue plasminogen activator-mediated plasminogen activation. Arthritis Rheum 2009; 60: 559-568.
34. Hulstein JJ, Lenting PJ, de Laat B, et al. beta2-Glycoprotein I inhibits von Willebrand factor dependent platelet adhesion and aggregation. Blood 2007; 110: 1483-1491.
35. Maiti SN, Balasubramanian K, Ramoth JA, Schroit AJ. Beta-2-glycoprotein 1-dependent macrophage uptake of apoptotic cells. Binding to lipoprotein receptor-related protein receptor family members. J Biol Chem 2008; 283: 3761-3766.
36. Bancsi LF, van der Linden IK, Bertina RM. Beta 2-glycoprotein I deficiency and the risk of thrombosis. Thromb Haemost 1992; 67: 649-653.
37. Yasuda S, Tsutsumi A, Chiba H, et al. beta(2)-glycoprotein I deficiency: Prevalence, genetic background and effects on plasma lipoprotein metabolism and hemostasis. Atherosclerosis 2000; 152: 337-346.
38. Tsutsumi A, Matsuura E, Ichikawa K, et al. Antibodies to beta 2-glycoprotein I and clinical manifestations in patients with systemic lupus erythematosus. Arthritis Rheum 1996; 39: 1466-1474.
39. Gomez-Pacheco L, Villa AR, Drenkard C, et al. Serum anti-beta2-glycoprotein-I and anticardiolipin antibodies during thrombosis in systemic lupus erythematosus patients. Am J Med 1999; 106: 417-423.
40. Alijotas-Reig J, Ferrer-Oliveras R, Rodrigo-Anoro MJ, et al. Anti-beta(2)-glycoprotein-I and anti-phosphatidylserine antibodies in women with spontaneous pregnancy loss. Fertil Steril 2010; 93: 2330-2336.
41. Sailer T, Zoghlami C, Kurz C, et al. Anti-beta2-glycoprotein I antibodies are associated with pregnancy loss in women with the lupus anticoagulant. Thromb Haemost 2006; 95: 796-801.
42. Iverson GM, Victoria EJ, Marquis DM. Anti-beta2 glycoprotein I (beta2GPI) autoantibodies recognize an epitope on the first domain of beta2GPI. Proc Natl Acad Sci USA 1998; 95: 15542-15546.
43. Giles IP, Isenberg DA, Latchman DS, Rahman A. How do antiphospholipid antibodies bind beta2-glycoprotein I? Arthritis Rheum 2003; 48: 2111-2121.
44. de Laat B, Derksen RH, Urbanus RT, de Groot PG. IgG antibodies that recognize epitope Gly40-Arg43 in domain I of beta 2-glycoprotein I cause LAC, and their presence correlates strongly with thrombosis. Blood 2005; 105: 1540-1545.
45. Bevers EM, Galli M, Barbui T, et al. Lupus anticoagulant IgG's (LA) are not directed to phospholipids only, but to a complex of lipid-bound human prothrombin. Thromb Haemost 1991; 66: 629-632.
46. Oosting JD, Derksen RH, Bobbink IW, et al. Antiphospholipid antibodies directed against a combination of phospholipids with prothrombin, protein C, or protein S: An explanation for their pathogenic mechanism? Blood 1993; 81: 2618-2625.
47. Alarcon-Segovia D, Perez-Vazquez ME, Villa AR, et al. Preliminary classification criteria for the antiphospholipid syndrome within systemic lupus erythematosus. Semin Arthritis Rheum 1992; 21: 275-286.
48. Branch DW, Andres R, Digre KB, et al. The association of antiphospholipid antibodies with severe preeclampsia. Obstet Gynecol 1989; 73: 541-545.
49. Tektonidou MG, Sotsiou F, Nakopoulou L, et al. Antiphospholipid syndrome nephropathy in patients with systemic lupus erythematosus and antiphospholipid antibodies: Prevalence, clinical associations, and long-term outcome. Arthritis Rheum 2004; 50: 2569-2579.
50. Nochy D, Daugas E, Droz D, et al. The intrarenal vascular lesions associated with primary antiphospholipid syndrome. J Am Soc Nephrol 1999; 10: 507-518.
51. Dunn AS, Kaboli P, Halfdanarson T, et al. Do patients followed in anticoagulation clinics for antiphospholipid syndrome meet criteria for the disorder? Thromb Haemost 2005; 94: 548-554.
52. Out HJ, de Groot PG, Hasselaar P, et al. Fluctuations of anticardiolipin antibody levels in patients with systemic lupus erythematosus: A prospective study. Ann Rheum Dis 1989; 48: 1023-1038.
53. Ortel TL. Laboratory diagnosis of the lupus anticoagulant. Curr Rheumatol Rep 2012; 14: 64-70.
54. Teruya J, West AG, Suell MN. Lupus anticoagulant assays: Questions answered and to be answered. Arch Pathol Lab Med 2007; 131: 885-889.
55. Ip BK, Thomson AR, Moriarty HT. A comparison of the sensitivity of APTT reagents to the effects of enoxaparin, a low-molecular weight heparin. Pathology 2001; 33: 347-352.
56. Liestol S, Wisloff F. Effect of subcutaneous administration of dalteparin on lupus anticoagulant assays. Thromb Res 2005; 115: 509-517.
57. Linkins LA, Julian JA, Rischke J, et al. In vitro comparison of the effect of heparin, enoxaparin and fondaparinux on tests of coagulation. Thromb Res 2002; 107: 241-244.
58. Gosselin RC, King JH, Janatpur KA, et al. Effects of pentasaccharide (fondaparinux) and direct thrombin inhibitors on coagulation testing. Arch Pathol Lab Med 2004; 128: 1142-1145.
59. Tripodi A, Chantarangkul V, Clerici M, Mannucci PM. Laboratory diagnosis of lupus anticoagulants for patients on oral anticoagulant treatment. Performance of dilute Russell viper venom test and silica clotting time in comparison with Staclot LA. Thromb Haemost 2002; 88: 583-586.
60. Olteanu H, Downes KA, Patel J, et al. Warfarin does not interfere with lupus anticoagulant detection by dilute Russell's viper venom time. Clin Lab 2009; 55: 138-142.
61. Genzen JR, Miller JL. Presence of direct thrombin inhibitors can affect the results and interpretation of lupus anticoagulant testing. Am J Clin Pathol 2005; 124: 586-593.
62. Garcia D, Libby E, Crowther MA. The new oral anticoagulants. Blood 2010; 115: 15-20.
63. Hillarp A, Baghaei F, Fagerberg Blixter I, et al. Effects of the oral, direct factor Xa inhibitor rivaroxaban on commonly used coagulation assays. J Thromb Haemost 2011; 9: 133-139.
64. Merriman E, Kaplan Z, Butler J, et al. Rivaroxaban and false positive lupus anticoagulant testing. Thromb Haemost 2011; 105: 385-386.
65. van Os GM, de Laat B, Kamphuisen PW, et al. Detection of lupus anticoagulant in the presence of rivaroxaban using Taipan snake venom time. J Thromb Haemost 2011; 9: 1657-1659.
66. Male C, Foulon D, Hoogendoorn H, et al. Predictive value of persistent versus transient antiphospholipid antibody subtypes for the risk of thrombotic events in pediatric patients with systemic lupus erythematosus. Blood 2005; 106: 4152-4158.
67. Pengo V, Biasiolo A, Pegoraro C, et al. Antibody profiles for the diagnosis of antiphospholipid syndrome. Thromb Haemost 2005; 93: 1147-1152.
68. Neville C, Rauch J, Kassis J, et al. Thromboembolic risk in patients with high titre anticardiolipin and multiple antiphospholipid antibodies. Thromb Haemost 2003; 90: 108-115.
69. Pengo V, Ruffatti A, Legnani C, et al. Incidence of a first thromboembolic event in asymptomatic carriers of high-risk antiphospholipid antibody profile: A multicenter prospective study. Blood 2011; 118: 4714-4718.
70. de Laat B, Pengo V, Pabinger I, et al. The association between circulating antibodies against domain I of beta2-glycoprotein I and thrombosis: An international multicenter study. J Thromb Haemost 2009; 7: 1767-1773.
71. Bertolaccini ML, Amengual O, Atsumi T, et al. 'Non-criteria' aPL tests: Report of a task force and preconference workshop at the 13th International Congress on Antiphospholipid Antibodies, Galveston, TX, USA, April 2010. Lupus 2011; 20: 191-205.
72. Devreese K, Peerlinck K, Arnout J, Hoylaerts MF. Laboratory detection of the antiphospholipid syndrome via calibrated automated thrombography. Thromb Haemost 2009; 101: 185-196.
73. Liestol S, Sandset PM, Mowinckel MC, Wisloff F. Activated protein C resistance determined with a thrombin generation-based test is associated with thrombotic events in patients with lupus anticoagulants. J Thromb Haemost 2007; 5: 2204-2210.
74. Devreese K, Peerlinck K, Hoylaerts MF. Thrombotic risk assessment in the antiphospholipid syndrome requires more than the quantification of lupus anticoagulants. Blood 2010; 115: 870-878.
75. Voges D, Berendes R, Burger A, et al. Three-dimensional structure of membrane-bound annexin V. A correlative electron microscopy-X-ray crystallography study. J Mol Biol 1994; 238: 199-213.
76. Reviakine II, Bergsma-Schutter W, Brisson A. Growth of protein 2-D crystals on supported planar lipid bilayers imaged in situ by AFM. J Struct Biol 1998; 121: 356-361.
77. Andree HA, Stuart MC, Hermens WT, et al. Clustering of lipid-bound annexin V may explain its anticoagulant effect. J Biol Chem 1992; 267: 17907-17912.
78. Rand JH, Wu XX, Quinn AS, et al. Human monoclonal antiphospholipid antibodies disrupt the annexin A5 anticoagulant crystal shield on phospholipid bilayers: Evidence from atomic force microscopy and functional assay. Am J Pathol 2003; 163: 1193-1200.
79. Rand JH, Wu XX, Andree HA, et al. Antiphospholipid antibodies accelerate plasma coagulation by inhibiting annexin-V binding to phospholipids: A "lupus procoagulant" phenomenon. Blood 1998; 92: 1652-1660.
80. Rand JH, Wu XX, Lapinski R, et al. Detection of antibody-mediated reduction of annexin A5 anticoagulant activity in plasmas of patients with the antiphospholipid syndrome. Blood 2004; 104: 2783-2790.
81. de Laat B, Wu XX, van Lummel M, et al. Correlation between antiphospholipid antibodies that recognize domain I of beta2-glycoprotein I and a reduction in the anticoagulant activity of annexin A5. Blood 2007; 109: 1490-1494.