High prevalence of prothrombotic abnormalities in multifocal osteonecrosis: Description of a series and review of the literature

Medicine (United States)

Volumn 92, Issue 6, 2013, Pages 295-304

  Gómez Puerta, Jose A ^a,c   Peris, Pilar ^a   Reverter, Joan Carles ^a   Espinosa, Gerard ^b   Martinez Ferrer, Angeles ^a   Monegal, Ana ^a   Monteagudo, Juan ^a   Tàssies, Dolors ^a   Guañabens, Nuria ^a  

^a HOSPITAL CLÍNIC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; ANTITHROMBIN; ANTITHROMBOCYTIC AGENT; BLOOD CLOTTING FACTOR 5 LEIDEN; BLOOD CLOTTING FACTOR 8; CARDIOLIPIN ANTIBODY; CORTICOSTEROID; FIBRINOGEN; LUPUS ANTICOAGULANT; PHOSPHOLIPID ANTIBODY; PLASMINOGEN; PREDNISONE; PROTEIN C; PROTEIN S; PROTHROMBIN;

ABNORMAL LABORATORY RESULT; ACTIVATED PROTEIN C RESISTANCE; ADULT; AGED; ANKLE; ANKLE RADIOGRAPHY; ARTICLE; BLOOD CLOTTING DISORDER; BLOOD CLOTTING TEST; BONE NECROSIS; CLINICAL ARTICLE; CLINICAL FEATURE; CORTICOSTEROID THERAPY; DRUG MEGADOSE; GENE MUTATION; HIP; HIP ARTHROPLASTY; HUMAN; INFARCTION; KNEE; KNEE ARTHROPLASTY; KNEE RADIOGRAPHY; LOWER EXTREMITY DEEP VEIN THROMBOSIS; MEDICAL HISTORY; MEDICAL LITERATURE; MULTIFOCAL OSTEONECROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PARTIAL THROMBOPLASTIN TIME; PREVALENCE; PRIORITY JOURNAL; PROTHROMBIN TIME; RETROSPECTIVE STUDY; SHOULDER; THROMBOSIS;

ADULT; AGED; AGED, 80 AND OVER; BLOOD COAGULATION DISORDERS; FEMALE; HUMANS; MALE; MIDDLE AGED; OSTEONECROSIS; PREVALENCE; RETROSPECTIVE STUDIES; THROMBOSIS;

EID: 84887850835     PISSN: 00257974     EISSN: 15365964     Source Type: Journal    
DOI: 10.1097/MD.0000000000000007     Document Type: Article

References (63)

1. Alijotas J, Argemi M, Barquinero J. Kienbock's disease and antiphospholipid antibodies. Clin Exp Rheumatol. 1990;8:297-298
2. Anonymous. Symptomatic multifocal osteonecrosis. A multicenter study. Collaborative Osteonecrosis Group. Clin Orthop Relat Res. 1999;369:312-326.
3. Asherson RA, Khamashta MA, Ordi-Ros J, Derksen RH, Machin SJ, Barquinero J, Outt HH, Harris EN, Vilardell-Torres M, Hughes GR. The "primary" antiphospholipid syndrome: major clinical and serological features. Medicine (Baltimore). 1989;68:366-374.
4. Assouline-Dayan Y, Chang C, Greenspan A, Shoenfeld Y, Gershwin ME. Pathogenesis and natural history of osteonecrosis. Semin Arthritis Rheum. 2002;32:94-124.
5. Blanche P, Si-Larbi AG, Jouve P. Femoral head necrosis and hyperhomocysteinemia. J Rheumatol. 2001;28:1469.
6. Celik A, Tekis D, Saglam F, Tunali S, Kabakci N, Ozaksoy D, Manisali M, Ozcan MA, Meral M, Gulay H, Camsari T. Association of corticosteroids and factor V, prothrombin, and MTHFR gene mutations with avascular osteonecrosis in renal allograft recipients. Transplant Proc. 2006;38:512-516.
7. Cenni E, Fotia C, Rustemi E, Yuasa K, Caltavuturo G, Giunti A, Baldini N. Idiopathic and secondary osteonecrosis of the femoral head show different thrombophilic changes and normal or higher levels of platelet growth factors. Acta Orthop. 2011;82:42-49.
8. Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, Jacobsen S, Lakos G, Tincani A, Kontopoulou-Griva I, Galeazzi M, Meroni PL, Derksen RH, de Groot PG, Gromnica-Ihle E, Baleva M, Mosca M, Bombardieri S, Houssiau F, Gris JC, Quere I, Hachulla E, Vasconcelos C, Roch B, Fernandez-Nebro A, Boffa MC, Hughes GR, Ingelmo M. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1, 000 patients. Arthritis Rheum. 2002;46:1019-1027.
9. Chotanaphuti T, Heebthamai D, Chuwong M, Kanchanaroek K. The prevalence of thrombophilia in idiopathic osteonecrosis of the hip. J Med Assoc Thai. 2009;92(Suppl 6):S141-146.
10. de Larranaga G, Bottaro E, Martinuzzo M, Figueroa R, Iglesias Varela ML, Peres Wingeyer S, Forastiero R, Adamczuk Y, Corti M, Puga L, Benetucci J. Thrombophilia in human immunodeficiency virus-infected patients with osteonecrosis: is there a real connection? The first case-control study. Clin Appl Thromb Hemost. 2009;15:340-347.
11. Egan RM, Munn RK. Catastrophic antiphospholipid antibody syndrome presenting with multiple thromboses and sites of avascular necrosis. J Rheumatol. 1994;21:2376-2379.
12. Erkan D, Harrison MJ, Levy R, Peterson M, Petri M, Sammaritano L, Unalp-Arida A, Vilela V, Yazici Y, Lockshin MD. Aspirin for primary thrombosis prevention in the antiphospholipid syndrome: a randomized, double-blind, placebo-controlled trial in asymptomatic antiphospholipid antibody-positive individuals. Arthritis Rheum. 2007;56:2382-2391.
13. Erkan D, Yazici Y, Sobel R, Lockshin MD. Primary antiphospholipid syndrome: functional outcome after 10 years. J Rheumatol. 2000;27:2817-2821.
14. Flouzat-Lachaniete CH, Roussignol X, Poignard A, Mukasa MM, Manicom O, Hernigou P. Multifocal joint osteonecrosis in sickle cell disease. Open Orthop J. 2009;3:32-35.
15. Garcia-Gala JM, Alvarez V, Pinto CR, Soto I, Urgelles MF, Menendez MJ, Carracedo C, Lopez-Larrea C, Coto E. Factor V Leiden (R506Q) and risk of venous thromboembolism: a case-control study based on the Spanish population. Clin Genet. 1997;52:206-210.
16. Gattorno M, Falcini F, Ravelli A, Zulian F, Buoncompagni A, Martini G, Resti M, Picco P, Martini A. Outcome of primary antiphospholipid syndrome in childhood. Lupus. 2003;12:449-453.
17. Glueck CJ, Fontaine RN, Gruppo R, Stroop D, Sieve-Smith L, Tracy T, Wang P. The plasminogen activator inhibitor-1 gene, hypofibrinolysis, and osteonecrosis. Clin Orthop Relat Res. 1999;366:133-146.
18. Glueck CJ, Freiberg RA, Boppana S, Wang P. Thrombophilia, hypofibrinolysis, the eNOS T-786C polymorphism, and multifocal osteonecrosis. J Bone Joint Surg Am. 2008;90:2220-2229.
19. Glueck CJ, Freiberg RA, Boriel G, Khan Z, Brar A, Padda J, Wang P. The role of the factor V Leiden mutation in osteonecrosis of the hip. Clin Appl Thromb Hemost. 2013;19:499-503.
20. Glueck CJ, Freiberg RA, Oghene J, Fontaine RN, Wang P. Association between the T-786C eNOS polymorphism and idiopathic osteonecrosis of the head of the femur. J Bone Joint Surg Am. 2007;89:2460-2468.
21. Glueck CJ, Freiberg RA, Wang P. Heritable thrombophilia-hypofibrinolysis and osteonecrosis of the femoral head. Clin Orthop Relat Res. 2008;466:1034-1040.
22. Glueck CJ, McMahon RE, Bouquot JE, Tracy T, Sieve-Smith L, Wang P. A preliminary pilot study of treatment of thrombophilia and hypofibrinolysis and amelioration of the pain of osteonecrosis of the jaws. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1998;85:64-73.
23. Gomez-Puerta JA, Martin H, Amigo MC, Aguirre MA, Camps MT, Cuadrado MJ, Hughes GR, Khamashta MA. Long-term follow-up in 128 patients with primary antiphospholipid syndrome: do they develop lupus? Medicine (Baltimore). 2005;84:225-230.
24. Gomez-Puerta JA, Peris P, Guanabens N. Osteonecrosis multiple. Patogenesis, caracteristicas clinicas y tratamiento. Semin Fund Esp Reumatol. 2007;8:185-192.
25. Gomez-Puerta JA, Pons-Estel GJ. Skeletal involvement in antiphospholipid syndrome. Curr Rheumatol Rev. 2010;6:25-31.
26. Jones L. Osteonecrosis (avascular necrosis of bone). UpToDate (www.uptodate.com); 2012.
27. Jones LC, Mont MA, Le TB, Petri M, Hungerford DS, Wang P, Glueck CJ. Procoagulants and osteonecrosis. J Rheumatol. 2003;30:783-791.
28. Kamphuisen PW, Houwing-Duistermaat JJ, van Houwelingen HC, Eikenboom JC, Bertina RM, Rosendaal FR. Familial clustering of factor VIII and von Willebrand factor levels. Thromb Haemost. 1998;79:323-327.
29. Kang JH, Lin HC. Increased risk for coronary heart disease after avascular necrosis of femoral head: a 3-year follow-up study. Am Heart J. 2010;159:803-808 e1.
30. Koo KH, Lee JS, Lee YJ, Kim KJ, Yoo JJ, Kim HJ. Endothelial nitric oxide synthase gene polymorphisms in patients with nontraumatic femoral head osteonecrosis. J Orthop Res. 2006;24:1722-1728.
31. Koshy A, Jeyakumari M. High FVIII level is associated with idiopathic portal vein thrombosis in South India. Am J Med. 2007;120:552 e9-11.
32. Koster T, Blann AD, Briet E, Vandenbroucke JP, Rosendaal FR. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet. 1995;345:152-155.
33. Kyrle PA, Minar E, Hirschl M, Bialonczyk C, Stain M, Schneider B, Weltermann A, Speiser W, Lechner K, Eichinger S. High plasma levels of factor VIII and the risk of recurrent venous thromboembolism. N Engl J Med. 2000;343:457-462.
34. LaPorte DM, Mont MA, Mohan V, Jones LC, Hungerford DS. Multifocal osteonecrosis. J Rheumatol. 1998;25:1968-1974.
35. Livesey JA, Manning RA, Meek JH, Jackson JE, Kulinskaya E, Laffan MA, Shovlin CL. Low serum iron levels are associated with elevated plasma levels of coagulation factor VIII and pulmonary emboli/deep venous thromboses in replicate cohorts of patients with hereditary haemorrhagic telangiectasia. Thorax. 2012;67:328-333.
36. Mammen EF. Sticky platelet syndrome. Semin Thromb Hemost. 1999;25:361-365.
37. Mehsen N, Barnetche T, Redonnet-Vernhet I, Guerin V, Bentaberry F, Gonnet-Gracia C, Schaeverbeke T. Coagulopathies frequency in aseptic osteonecrosis patients. Joint Bone Spine. 2009;76:166-169.
38. Mejia-Romero R, Garcia-Carrasco M, Galarza-Maldonado C, Santos P, Mendoza-Pinto C, Escarcega RO, Salinas-Saldivar S, Soto-Vega E, Lopez-Colombo A, Cervera R. Primary antiphospholipid syndrome in Latin American mestizo patients: clinical and immunologic characteristics and comparison with European patients. Clin Rheumatol. 2008;27:891-897.
39. Miller KD, Masur H, Jones EC, Joe GO, Rick ME, Kelly GG, Mican JM, Liu S, Gerber LH, Blackwelder WC, Falloon J, Davey RT, Polis MA, Walker RE, Lane HC, Kovacs JA. High prevalence of osteonecrosis of the femoral head in HIV-infected adults. Ann Intern Med. 2002;137:17-25.
40. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, PG DEG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost. 2006;4:295-306.
41. Mont MA, Hungerford DS. Non-traumatic avascular necrosis of the femoral head. J Bone Joint Surg Am. 1995;77:459-474.
42. Mont MA, Ulrich SD, Seyler TM, Smith JM, Marker DR, McGrath MS, Hungerford DS, Jones LC. Bone scanning of limited value for diagnosis of symptomatic oligofocal and multifocal osteonecrosis. J Rheumatol. 2008;35:1629-1634.
43. Morse CG, Mican JM, Jones EC, Joe GO, Rick ME, Formentini E, Kovacs JA. The incidence and natural history of osteonecrosis in HIV-infected adults. Clin Infect Dis. 2007;44:739-748.
44. Mundo J, Peris P, Monegal A, Navasa M, Cervera R, Guaniabens N. Multifocal avascular necrosis after liver transplantation: an unusual presentation of the antiphospholipid syndrome. Lupus. 2006;15:304-307.
45. Nguyen BY, Reveille JD. Rheumatic manifestations associated with HIV in the highly active antiretroviral therapy era. Curr Opin Rheumatol. 2009;21:404-410.
46. O'Donnell J, Mumford AD, Manning RA, Laffan M. Elevation of FVIII:C in venous thromboembolism is persistent and independent of the acute phase response. Thromb Haemost. 2000;83:10-13.
47. O'Donnell J, Tuddenham EG, Manning R, Kemball-Cook G, Johnson D, Laffan M. High prevalence of elevated factor VIII levels in patients referred for thrombophilia screening: role of increased synthesis and relationship to the acute phase reaction. Thromb Haemost. 1997;77:825-828.
48. Ota S, Yamada N, Ogihara Y, Tsuji A, Ishikura K, Nakamura M, Wada H, Ito M. High plasma level of factor VIII: an important risk factor for venous thromboembolism. Circ J. 2011;75:1472-1475.
49. Pengo V, Ruffatti A, LegnaniC, Gresele P, Barcellona D, Erba N, Testa S, Marongiu F, Bison E, Denas G, Banzato A, Padayattil Jose S, Iliceto S. Clinical course of high-risk patients diagnosed with antiphospholipid syndrome. J Thromb Haemost. 2010;8:237-242.
50. Robinson AB, Rabinovich CE. Avascular necrosis of the metacarpals in juvenile dermatomyositis. J Clin Rheumatol. 2010;16:233-236.
51. Ryan K, O'Donnell JS. Elevated plasma factor VIII levels in patients with venous thrombosisVconstitutional risk factor or secondary epiphenomenon? Thromb Res. 2012;129:105-106.
52. Schambeck CM, Hinney K, Haubitz I, Mansouri Taleghani B, Wahler D, Keller F. Familial clustering of high factor VIII levels in patients with venous thromboembolism. Arterioscler Thromb Vasc Biol. 2001;21:289-292.
53. Sorice M, Griggi T, Arcieri P, Circella A, d'Agostino F, Ranieri M, Modrzewska R, Lenti L, Mariani G. Protein S and HIV infection. The role of anticardiolipin and anti-protein S antibodies. Thromb Res. 1994;73:165-175.
54. Steinberg ME. Early diagnosis of avascular necrosis of the femoral head. Instr Course Lect. 1988;37:51-57.
55. Stulberg BN, Bauer TW, Belhobek GH, Levine M, Davis A. A diagnostic algorithm for osteonecrosis of the femoral head. Clin Orthop Relat Res. 1989;249:176-182.
56. Tektonidou MG, Malagari K, Vlachoyiannopoulos PG, Kelekis DA, Moutsopoulos HM. Asymptomatic avascular necrosis in patients with primary antiphospholipid syndrome in the absence of corticosteroid use: a prospective study by magnetic resonance imaging. Arthritis Rheum. 2003;48:732-736.
57. Tichelaar V, Mulder A, Kluin-Nelemans H, Meijer K. The acute phase reaction explains only a part of initially elevated factor VIII:C levels: a prospective cohort study in patients with venous thrombosis. Thromb Res. 2012;129:183-186.
58. Tuthill JI, Khamashta MA. Management of antiphospholipid syndrome. J Autoimmun. 2009;33:92-98.
59. van der Meer FJ, Koster T, Vandenbroucke JP, Briet E, Rosendaal FR. The Leiden Thrombophilia Study (LETS). Thromb Haemost. 1997;78:631-635.
60. Vianna JL, Khamashta MA, Ordi-Ros J, Font J, Cervera R, Lopez-Soto A, Tolosa C, Franz J, Selva A, Ingelmo M, et al. Comparison of the primary and secondary antiphospholipid syndrome: a European multicenter study of 114 patients. Am J Med. 1994;96:3-9.
61. Yamaguchi R, Yamamoto T, Motomura G, Ikemura S, Iwasaki K, Zhao G, Iwamoto Y. Effects of an anti-platelet drug on the prevention of steroid-induced osteonecrosis in rabbits. Rheumatology (Oxford). 2012;51:789-793.
62. Yoo WH. Multiple rib infarcts: a rare form of osteonecrosis in antiphospholipid syndrome. Ann Rheum Dis. 2004;63:457-458.
63. Zalavras CG, Vartholomatos G, Dokou E, Malizos KN. Factor V Leiden and prothrombin gene mutations in femoral head osteonecrosis. Thromb Haemost. 2002;87:1079-1080.