Risk factors for osteonecrosis in systemic lupus erythematosus

Journal of Rheumatology

Volumn 24, Issue 4, 1997, Pages 654-662

  Mont, Michael A ^a   Glueck, Charles J ^a   Pacheco, Ivan H ^b   Wang, Ping ^c   Hungerford, David S ^a   Petri, Michelle ^a  

^a Department of Orthopaedics ^*

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Jewish Hospital Cholesterol Center   (United States)

Author keywords

Anticardiolipin antibodies; Corticosteroids; Lipoprotein(a); Osteonecrosis; Systemic lupus erythematosus

Indexed keywords

CARDIOLIPIN ANTIBODY; CORTICOSTEROID; LIPOPROTEIN A; PREDNISONE;

ADULT; AGED; ARTICLE; BONE NECROSIS; CONTROLLED STUDY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RISK FACTOR; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADOLESCENT; ADULT; AGED; ANTI-INFLAMMATORY AGENTS; ANTIBODIES, ANTICARDIOLIPIN; BIOLOGICAL MARKERS; CONTINENTAL POPULATION GROUPS; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LIPOPROTEIN(A); LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; OSTEONECROSIS; PREDNISONE; RISK FACTORS;

EID: 0030960719     PISSN: 0315162X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (117)

1. Mont MA, Hungerford DS: Non-traumatic avascular necrosis of the femoral head. J Bone Joint Surg 1995;77A:459-74.
2. Mankin HJ: Nontraumatic necrosis of bone (osteonecrosis). N Engl J Med 1992;326:1473-9.
3. National Center for Health Statistics: 1990 and 1991 National Hospital Discharge Survey. Rosemont, Illinois: The American Academy of Orthopaedic Surgeons Department of Research and Scientific Affairs, 1994.
4. Coventry MB, Beckenbaugh RD, Nolan DR, Ilstrup DM: 2,012 total hip arthoplasties: A study of postoperative course and early complications. J Bone Joint Surg 1974;56A:273-84.
5. Hanssen AD, Cabanela ME, Michet CJ Jr: Hip arthroplasty in patients with systemic lupus erythematosus. J Bone Joint Surg 1987;69A:807-14.
6. Huo MH, Salvati EA, Browne MG, Pellici PM, Sculco TP, Johanson NA: Primary total hip arthroplasty in systemic lupus erythematosus. J Arthroplasty 1992;7:51-6.
7. Prupas HM, Patzakis M, Quismorio FP Jr: Total hip arthroplasty for avascular necrosis of the femur in systemic lupus erythematosus. Clin Orthop 1981;161:186-90.
8. Mont MA, Fairbank AC, Petri M, Hungerford DS: Core decompression for avascular necrosis of the femoral head in systemic lupus erythematosus. Long-term report of risk factors for clinical progression. Clin Orthop 1997;334:91-7.
9. Chang CC, Greenspan A, Gershwin ME: Osteonecrosis: Current perspectives on pathogenesis and treatment. Semin Arthritis Rheum 1993;23:47-69.
10. Glueck CJ, Brandt G, Gruppo R, et al: Homozygous and heterozygous resistance to activated protein S, Legg-Perthes disease, and thrombosis (abstr). J Invest Med 1995;43:457A.
11. Glueck CJ, Freiberg R, Glueck HI, Tracy T, Stroop D, Hamer T: Idiopathic osteonecrosis, hypofibrinolysis, high plasminogen activator inhibitor, high lipoprotein(a) and therapy with stanozolol. Am J Hematol 1995;48:213-20.
12. Mont MA, Carbone JJ, Fairbank AC: Core decompression versus non-operative management for avascular necrosis of the femoral head. Clin Orthop 1995;322:1-11.
13. Abeles M, Urman JD, Rothfield NF: Aseptic necrosis of bone in systemic lupus erythematosus: Relationship to corticosteroid therapy. Arch Intern Med 1978;138:750-4.
14. Asherson RA, Lioté F, Page B, et al: Avascular necrosis of bone and antiphospholipid antibodies in systemic lupus erythematosus. J Rheumatol 1993;20:284-8.
15. Bergstein JM, Wiens C, Fish AJ, et al: Avascular necrosis of bone in systemic lupus erythematosus. J Pediatrics 1974;85:31-7.
16. Cruess RL: Steroid-induced osteonecrosis: A review. Can J Surg 1981;24:561-71.
17. Cruess RL: Cortisone-induced avascular necrosis of the femoral head. J Bone Joint Surg 1977;59-B:308-17.
18. Dubois EL, Cozen L: Avascular (aseptic) bone necrosis associated with systemic lupus erythematosus. J Am Med Assoc 1960;174:966-70.
19. Herndon JH, Aufranc OE: Avascular necrosis of the femoral head in the adult. A review of its incidence in a variety of conditions. Clin Orthop 1972;86:43-50.
20. Hungerford DS, Zizic TM II: Treatment of ischemie necrosis of bone in systemic lupus erythematosus. Medicine 1980;59:143-8.
21. Jacobs B: Epidemiology of traumatic and nontraumatic osteonecrosis. Clin Orthop 1978;130:51-67.
22. Kalla AA, Learmonth ID, Klemp P: Early treatment of avascular necrosis in systemic lupus erythematosus. Ann Rheum Dis 1986;45:649-55.
23. Loventhal GH, Dorfman HD: Aseptic necrosis of bone in systemic lupus erythematosus. Semin Arthritis Rheum 1974;40:73-80.
24. Masuyama J, Umino T, Murata M, et al: A systemic lupus erythematosus patient with multiple aseptic bone necroses, thrombosis of superior mesenteric artery and anti-phospholipid antibody. (Japanese). Ryumachi 1992;32:502-7.
25. Migliaresi S, Picillo U, Ambrosone I, et al: Avascular osteonecrosis in patients with SLE: Relation to corticosteroid therapy and anticardiolipin antibodies. Lupus 1994;3:37-41.
26. Nagasawa K, Ishii Y, Mayumi T, et al: Avascular necrosis of bone in systemic lupus erythematosus: Possible role of haemostatic abnormalities. Ann Rheum Dis 1989;48:672-6.
27. Ono K, Sugioka Y: Epidemiology and risk factors in avascular necrosis of the femoral head. In: Schoutens A, Arlet J, Gardeniers JWM, Hughes SPF, eds. Bone Circulation and Vascularization in Normal and Pathological Conditions. New York: Plenum Press, 1993:241-8.
28. Ono K, Tohjima T, Komazawa T: Risk factors of avascular necrosis of the femoral head in patients with systemic lupus erythematosus under high-dose corticosteroid therapy. Clin Orthop 1992;277:89-97.
29. Petri M: Musculoskeletal complications of systemic lupus erythematosus in the Hopkins Lupus Cohort: An update. Arthritis Care Res 1995;8:137-45.
30. Petri M, Baker J, Goldman D: Risk factors for osteonecrosis in SLE (abstr). Arthritis Rheum 1992;35(suppl 9):S110.
31. Weiner ES, Abeles M: Aseptic necrosis and glucocorticosteroids in systemic lupus erythematosus. A reevaluation. J Rheumatol 1989;16:604-8.
32. Wang T-Y, Avlonitis EG, Relkin R: Systemic necrotizing vasculitis causing bone necrosis. Am J Med 1988;84:1085-6.
33. Zelicof SB, Aranow C, Weinstein A, et al: The natural history of clinically occult avascular necrosis of the hip in systemic lupus erythematosus. Read at the Annual Meeting of The American Academy of Orthopaedic Surgeons, New Orleans, Louisiana, Feb. 26, 1994.
34. Zizic TM, Hungerford DS: Avascular necrosis of bone. In: Kelley WN, Harris ED, Ruddy S, Sledge C, eds. Textbook of Rheumatology. 2nd ed. Philadelphia: W.B. Saunders, 1985:1689-710.
35. Zizic TM, Hungerford DS, Stevens MB: Ischemic bone necrosis in systemic lupus erythematosus. I. The early diagnosis of ischemic necrosis of bone. Medicine 1980;59:134-42.
36. Hungerford DS, Lennox DW: Diagnosis and treatment of ischemic necrosis of the femoral head. In: Evarts C McC, ed. Surgery of the Musculoskeletal System. 2nd ed. New York: Churchill Livingstone, 1990:2757-94.
37. Petri M: Clinical features of systemic lupus erythematosus. Curr Opin Rheumatol 1994;6:481-6.
38. Cohen AS, Reynolds WE, Franklin EC, et al: Preliminary criteria for the classification of systemic lupus erythematosus. Bull Rheum Dis 1971;21:643.
39. Ficat RP, Arlet J: Functional investigation of bone under normal conditions. In: Hungerford DS, ed. Ischemia and Necrosis of Bone. Baltimore: Williams and Wilkins, 1980:29-52.
40. Goldberger E, Elder RC, Schwartz RA, Phillips PE: Vasculitis in the antiphospholipid syndrome. A cause of ischemia responding to corticosteroids (see comments). Arthritis Rheum 1992;35:569-72.
41. Gruppo R, Glueck CJ, McMahon RE, et al: The physiology of alveolar osteonecrosis of the jaw: Anticardiolipin antibodies, thrombophilia, and hypofibrinolysis. J Lab Clin Med 1996;127:481-8.
42. Harris EN, Gharavi AE, Hughes GRV: Antiphospholipid antibodies. Clin Rheum Dis 1985;11:591-609.
43. Edelberg J, Pizzo SV: Why is lipoprotein(a) relevant to thrombosis? Am J Clin Nutrition 1992;(suppl)56:791-2.
44. Instruction Manual: Antibody reagent test for lipoprotein(a) SPQ test system. Quantitative determination of lipoprotein(a) by immunoprecipitin analysis. Catalog 86084. Inctar Corp., Stillwater, Minnesota.
45. Silberman S, Armentrout M, Vella F, Saha A: Macra lipoprotein(a) for quantitation of human lipoprotein(a) by enzymes. Clin Chem 1990;36:961-5. [Macra Lp(a) Enzyme Immunoassay Kit: catalog No. D306; Terumo Medical Corp., Elkton, Maryland].
46. Glueck CJ, Kelley W, Gartside PS, Wang P: Coronary heart disease events and risk factors in 804 Cincinnati firelighters, a 10 year prospective study. Am J Ind Med 1996;30:331-40.
47. Shapiro SS, Wilk MB: An analysis of variance test for normality (complete samples). Biometrika 1965;52:591-611.
48. Snedecor GW, Cochran WG: Statistical Methods. 7th ed. Ames, Iowa: Iowa State University Press, 1980.
49. Jones JP Jr: Etiology and pathogenesis of osteonecrosis. Semin Arthritis Rheum 1991;2:160-8.
50. Hulman G: Pathogenesis of non-traumatic fat embolism. Lancet 1988;1:1366-7.
51. Glueck CJ, Crawford A, Roy D, Freiberg R, Glueck HI, Stroop D: Association of antithrombotic factor deficiencies and hypofibrinolysis with Legg-Perthes disease. J Bone Joint Surg 1996;78A:3-13.
52. Glueck CJ, Glueck HI, Greenfield D, et al: Protein C and S deficiency, thrombophilia, and hypofibrinolysis: Pathophysiologic causes of Legg-Perthes disease. Pediatr Res 1994;35:383-8.
53. Glueck CJ, Glueck HI, Tracy T, Speirs J, McCray C, Stroop D: Relationship between lipoprotein(a), lipids, apolipoproteins, basal and stimulated fibrinolytic regulators, and D-dimer. Metabolism 1993;42:236-46.
54. Glueck CJ, McMahon RE, Bouquot J, Stroop D, Tracy T, Wang P: Pathophysiology of osteonecrosis of the jaw: Thrombophilia and hypofibrinolysis. Oral Surg Oral Med Oral Path 1996;81:557-466.
55. Alarcón-Segovia D, Delezé M, Oria CV, et al: Antiphospholipid antibodies and the antiphospholipid syndrome in systemic lupus erythematosus: A prospective analysis of 500 consecutive patients. Medicine 1989;68:353-74.
56. 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;112:682-98.
57. Out HJ, de Groot PH, Hasselaar P, Van Vliet M, Derksen RHWM: Fluctuations of anticardiolipin antibody levels in patients with systemic lupus erythematosus: A prospective study. Ann Rheum Dis 1989;48:1023-8.
58. Petri M: Diagnosis of antiphospholipid antibodies. Rheum Dis Clin N Am 1994;20:443-69.
59. Petri M, Hochberg M, Hellman D, Bell W, Goldman D, Corash L: Race and disease activity are associated with the presence of antiphospholipid antibody in systemic lupus erythematosus: A five-year prospective study (abstr). Arthritis Rheum 1991; (suppl)34:S130.
60. Viard J-P, Amoura Z, Bach J-F: Association of anti-62 glycoprotein I antibodies with lupus-type circulating anticoagulant and thrombosis in systemic lupus erythematosus. Am J Med 1992;93:181-6.
61. Asherson RA, Khamashta MA, Ordi-Ros J, et al: The "primary" antiphospholipid syndrome: Major clinical and serological features. Medicine (Baltimore) 1989;68:366-74.
62. Bick RL, Baker WF Jr: Anticardiolipin antibodies and thrombosis. Hematol Oncol Clin N Am 1992;6:1287-99.
63. Bick RL, Baker WF Jr: The antiphospholipid and thrombosis syndromes. Med Clin N Am 1994;78:667-84.
64. Colaco CB, Male DK: Anti-phospholipid antibodies in syphilis and a thrombotic subset of SLE: Distinct profiles of epitope specificity. Clin Exp Immunol 1985;59:445-56.
65. Gladman DD, Urowitz MB: Venous syndromes and pulmonary embolus in systemic lupus erythematosus. Ann Rheum Dis 1980;39:340-2.
66. 2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci USA 1990;87:4120-4.
67. 2-glycoprotein I structure recognized by anticardiolipin antibodies. Lupus 1995;(suppl)4:13-7.
68. Carreras LO, Vermylen JG: "Lupus" anticoagulant and thrombosis - possible role of inhibition of prostacyclin formation. Thromb Haemost 1982;48:38-40.
69. Petraiuolo W, Bovill E, Hoak J: The lupus anticoagulant stimulates the release of prostacyclin from human endothelial cells. Thromb Res 1988;50:847-55.
70. Bokarewa MI, Blomback M, Egberg N, Rosen S: A new variant of interaction between phospholipid antibodies and the protein C system. Blood Coag Fibrin 1994;5:37-41.
71. Cariou R, Tobelem G, Soria C, Caen J: Inhibition of protein C activation by endothelial cells in the presence of lupus anticoagulant. N Engl J Med 1986;314:1193-4.
72. Smirnov MD, Triplett DT, Comp PC, Esmon NC: On the role of phosphatidyl ethanolamine in the inhibition of activated protein C activity by antiphospholipid antibodies. J Clin Invest 1995;95:309-16.
73. Palacios-Boix A, Alarcón-Segovia D: Antibodies to endothelial cells: New clues for the study of vascular damage in the autoimmune disease: In: Cervera R, Munther A, Khamashta A, Grahan RV, eds. Systemic Lupus Erythematosus. Boca Raton: CRC Press, 1994:1-16.
74. Vismara A, Meroni PL, Tincani A, et al: Relationship between anti-cardiolipin and anti-endothelial cell antibodies in systemic lupus erythematosus. Clin Exp Immunol 1988;74:247-53.
75. Freyssinet JM, Wiesel ML, Gauchy J. Boneu B, Cazenave JP: An IgM lupus anticoagulant that neutralizes the enhancing effect of phospholipid on purified endothelial thrombomodulin activity - a mechanism for thrombosis. Thromb Haemost 1986;55:309-13.
76. Khamashta MA, Harris EN, Gharavi AE, et al: Immune mediated mechanism for thrombosis: Antiphospholipid antibody binding to platelet membranes. Ann Rheum Dis 1988;47:849-55.
77. 2-glycoprotein-I. Biochim Biophys Acta 1986;884:142-9.
78. 2-glycoprotein-I (apo-H) inhibits the release reaction of human platelets during ADP induced aggregation. Atherosclerosis 1987;63:109-14.
79. 2-glycoprotein I is a requirement for anticardiolipin antibodies binding to activated platelets: Differences with lupus anticoagulants. Blood 1993;81:1255-62.
80. Fort JG, Cowchock FS, Abruzzo JL, Smith JB: Anticardiolipin antibodies in patients with rheumatic diseases. Arthritis Rheum 1987;30:752-60.
81. Glueck HI, Kant KS, Weiss MA, Pollak VE, Miller MA, Coots M: Thrombosis in systemic lupus erythematosus. Arch Intern Med 1985;145:1389-95.
82. Harris EN, Boey ML, Mackworth-Young CG, et al: Anticardiolipin antibodies: Detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet 1983;2:1211-4.
83. Howard MA, Firkin BG, Healy DL, Choong SC: Lupus anticoagulant in women with multiple spontaneous miscarriage. Am J Hematol 1987;26:175-8.
84. Hunt JE, Adelstein S, Krilis SA: New basic aspects of the antiphospholipid syndrome. Clin Exp Rheumatol 1994;12:661-8.
85. Lubbe WF, Palmer SJ, Butler WS, Laggis GC: Fetal survival after prednisolone suppression of maternal lupus anticoagulant. Lancet 1983;1:1361-3.
86. McGee GS, Pearce WH, Sharma L, et al: Antiphospholipid antibodies and arterial thrombosis. Case reports and a review of the literature. Arch Surg 1992;127:342-6.
87. McHugh NJ, Maymo J, Skinner RP, James I, Maddison PJ: Anticardiolipin antibodies, livedo reticularis, and major cerebrovascular and renal disease in systemic lupus erythematosus. Ann Rheum Dis 1988;47:110-5.
88. Ordi-Ros J, Pérez-Pemán P, Monasterio J: Clinical and therapeutic aspects associated to phospholipid binding antibodies (lupus anticoagulant and anticardiolipin antibodies). Haemostasis 1994;24:165-74.
89. Petri M: Antiphospholipid antibodies: Lupus anticoagulant and anticardiolipin antibody. Curr Probl Dermatol 1992;4:171-201.
90. Triplett DA: Antiphospholipid antibodies and thrombosis: A consequence, coincidence, or cause? Arch Pathol Lab Med 1993;117:78-88.
91. Bouquot JE: Neuralgia-inducing cavitational osteonecrosis. In: Neville BW, Damm DD, Allen CM, Bouquot JE, eds. Oral and Maxillofacial Pathology. Philadelphia: W.B. Saunders, 1995:631-2.
92. Bouquot JE, Roberts AM, Person P, Christian J: Neuralgia-inducing cavitational osteonecrosis. Osteomyelitis in 224 jawbone samples from patients with facial neuralgia. Oral Surg Oral Med Oral Path 1992;73:307-19.
93. Glueck CJ, McMahon RE, Bouquot J, et al: The pathophysiology of idiopathic osteonecrosis of the jaws: Thrombophilia and hypofibrinolysis (abstr). J Invest Med 1995;(suppl 2)43:234A.
94. Glueck CJ, Freiberg R, Glueck HI, et al: Hypofibrinolysis: A common, major cause of osteonecrosis. Am J Hematol 1994;45:156-66.
95. Glueck CJ, Glueck HI, Welch M, et al: Familial idiopathic osteonecrosis mediated by familial hypofibrinolysis with high levels of plasminogen activator inhibitor. Thromb Haemost 1994;71:195-8.
96. Alijotas J, Argemi M, Barquinero J: Kienböck's disease and antiphospholipid antibodies. Clin Exp Rheumatol 1990;8:297-8.
97. Egan RM, Munn RK: Catastrophic antiphospholipid antibody syndrome presenting with multiple thromboses and sites of avascular necrosis. J Rheumatol 1994;21:2376-9.
98. Seleznick MJ, Silveira LH, Espinoza K: Avascular necrosis associated with anticardiolipin antibodies. J Rheumatol 1991;18:1416-7.
99. Vela P, Battle E, Salas E, Marco P: Primary antiphospholipid syndrome and osteonecrosis (letter). Clin Exp Rheumatol 1991;9:545-9.
100. Kalunian KC, Peter JB, Middlekauf HR, et al: Clinical significance of a single test for anti-cardiolipin antibodies in patients with systemic lupus erythematosus. Am J Med 1988;85:602-8.
101. Kerleau JM, Lévesque H, Delpech A, et al: Prevalence and evolution of anticardiolipin antibodies in giant cell arteritis during corticosteroid therapy. A prospective study of 20 consecutive cases. Br J Rheumatol 1994;33:648-50.
102. Pérez-Vázquez ME, Villa AR, Drenkard C, Cabiedes J, Alarcón-Segovia D: Influence of disease duration, continued follow-up and further antiphospholipid testing on the frequency and classification category of antiphospholipid syndrome in a cohort of patients with systemic lupus erythematosus. J Rheumatol 1993;20:417-21.
103. Lioté F, Meyer O: Osteoarticular manifestations in the antiphospholipid syndrome. In: Asherson RA, ed. The Antiphospholipid Syndrome. CRC Press, 1996:195-200.
104. Jones JP Jr: Alcoholism, hypercortisonism, fat embolism, and osseous avascular necrosis. In: Zinn WM, ed. Idiopathic Ischemic Necrosis of the Femoral Head in Adults. Stuttgart: Georg Thieme, 1971:112-21.
105. Jones JP Jr: Intravascular coagulation and osteonecrosis. Clin Orthop 1992;277:41-53.
106. Jones JP Jr: Concepts of etiology and early pathogenesis of osteonecrosis. In: Schafer M, ed. Instructional Course Lectures. Rosemont, Illinois: American Academy of Orthopaedic Surgeons, 1994;43:499-512.
107. Boettcher WG, Bonfiglio H, Hamilton HH, Sheets RF, Smith K: Non-traumatic necrosis of the femoral head. Part I. Relation of altered hemostasis to etiology. J Bone Joint Surg 1970;52A:312-21.
108. Saito S, Inoue A, Ono K: Intramedullary hemorrhage as a possible cause of avascular necrosis of the femoral head. The histology of 16 femoral heads at the silent stage. J Bone Joint Surg 1987;69B:346-51.
109. Saito S, Ohzono K, Ono K: Early arteriopathy and postulated pathogenesis of osteonecrosis of the femoral head. The intracapital arterioles. Clin Orthop 1992;277:98-110.
110. Van Veldhuizen PJ, Neff J, Murphey MD, Bodensteiner D, Skikne BS: Decreased fibrinolytic potential in patients with idiopathic avascular necrosis and transient osteoporosis of the hip. Am J Hematol 1993;44:243-8.
111. Comp PC, Esmon CT: Recurrent venous thromboembolism in patients with a partial deficiency of protein S. N Engl J Med 1984;311:1525-8.
112. Allaart CF, Poort SR, Rosendaal FR, Reitsma PH, Bertina RM, Briët E: Increased risk of venous thrombosis in carriers of hereditary protein C deficiency defect. Lancet 1993;341:134-8.
113. Beauchamp NJ, Daly ME, Hampton KK, Cooper PC, Preston FE, Peake IR: High prevalence of a mutation in the factor V gene within the U.K. population: Relationship to activated protein C resistance and familial thrombosis. Br J Hematol 1994;88:219-22.
114. Bertina RM, Koeleman BP, Koster T, et al: Mutation in blood coagulation factor V associated with resistance to activated protein C. Nature (London) 1994;369:64-7.
115. Dahlbäck B: Inherited thrombophilia: Resistance to activated protein C as a pathogenic factor of venous thromboembolism. Blood 1995;85:607-14.
116. Dahlbäck B: Factor V gene mutation causing inherited resistance to activated protein C as a basis for venous thromboembolism. J Int Med 1995;237:221-7.
117. Matsuda J, Gohchi K, Tsukamoto M, Gotoh M, Saitoh N, Kawasugi K: Resistance to activated protein C in systemic lupus erythematosus patients with antiphospholipid antibodies (letter). Eur J Haem 1994;53:188-9.