Prevention of bone mineral density loss in patients with rheumatoid arthritis treated with anti-TNFα therapy

Biologics: Targets and Therapy

Volumn 2, Issue 4, 2008, Pages 663-669

  Marotte, Hubert ^a   Miossec, Pierre ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

Bone mineral density; Infliximab; Rheumatoid arthritis; TNFa

Indexed keywords

EID: 77953994146     PISSN: 11775475     EISSN: 11775491     Source Type: Journal    
DOI: None     Document Type: Review

References (94)

1. Al-Awadhi A, Olusi S, Al-Zaid N, et al. 1999. Serum concentrations of interleukin 6, osteocalcin, intact parathyroid hormone, and markers of bone resorption in patients with rheumatoid arthritis. J Rheumatol, 26:1250-6.
2. Allali F, Breban M, Porcher R, et al. 2003. Increase in bone mineral density of patients with spondyloarthropathy treated with anti-tumour necrosis factor alpha. Ann Rheum Dis, 62:347-9.
3. Ammann P, Rizzoli R, Bonjour JP, et al. 1997. Transgenic mice expressing soluble tumor necrosis factor-receptor are protected against bone loss caused by estrogen deficiency. J Clin Invest, 99:1699-703.
4. Bekker PJ, Holloway D, Nakanishi A, et al. 2001. The effect of a single dose of osteoprotegerin in postmenopausal women. J Bone Miner Res, 16:348-60.
5. Bernstein M, Irwin S, Greenberg GR. 2005. Maintenance infliximab treatment is associated with improved bone mineral density in Crohn's disease. Am J Gastroenterol, 100:2031-5.
6. Bertolini DR, Nedwin GE, Bringman TS, et al. 1986. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature, 319:516-8.
7. Bonnet J, Zerath E, Picaud N, et al. 1993. Bone morphometric changes in adjuvant-induced polyarthritic osteopenia in rats:evidence for an early bone formation defect. J Bone Miner Res, 8:659-68.
8. Brennan FM, Browne KA, Green PA, et al. 1997. Reduction of serum matrix metalloproteinase 1 and matrix metalloproteinase 3 in rheumatoid arthritis patients following anti-tumour necrosis factor-alpha (cA2) therapy. Br J Rheumatol, 36:643-50.
9. Briot K, Garnero P, Le Henanff A, et al. 2005. Body weight, body composition, and bone turnover changes in patients with spondyloarthropathy receiving anti-tumour necrosis factor {alpha} treatment. Ann Rheum Dis, 64:1137-40.
10. Bucay N, Sarosi I, Dunstan CR, et al. 1998. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev, 12:1260-8.
11. Cenci S, Weitzmann MN, Roggia C, et al. 2000. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest, 106:1229-37.
12. Charles P, Elliott MJ, Davis D, et al. 1999. Regulation of cytokines, cytokine inhibitors, and acute-phase proteins following anti-TNF-alpha therapy in rheumatoid arthritis. J Immunol, 163:1521-8.
13. Chopin F, Garnero P, Le Henanff A, et al. 2007. Long term effects of Infliximab on bone and cartilage turnover markers in patients with rheumatoid arthritis. Ann Rheum Dis.
14. Collin-Osdoby P, Rothe L, Anderson F, et al. 2001. Receptor activator of NF-kappa B and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. J Biol Chem, 276:20659-72.
15. Cooper C, Coupland C, Mitchell M. 1995. Rheumatoid arthritis, corticosteroid therapy and hip fracture. Ann Rheum Dis, 54:49-52.
16. Cortet B, Cortet C, Blanckaert F, et al. 2001. Quantitative ultrasound of bone and markers of bone turnover in Cushing's syndrome. Osteoporos Int, 12:117-23.
17. Cortet B, Flipo RM, Pigny P, et al. 1997. How useful are bone turnover markers in rheumatoid arthritis? Influence of disease activity and corticosteroid therapy. Rev Rhum Engl Ed, 64:153-9.
18. Cortet B, Guyot MH, Solau E, et al. 2000. Factors influencing bone loss in rheumatoid arthritis:a longitudinal study. Clin Exp Rheumatol, 18:683-90.
19. Emery JG, McDonnell P, Burke MB, et al. 1998. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J Biol Chem, 273:14363-7.
20. Forslind K, Keller C, Svensson B, et al. 2003. Reduced bone mineral density in early rheumatoid arthritis is associated with radiological joint damage at baseline and after 2 years in women. J Rheumatol, 30:2590-6.
21. Garnero P, Delmas PD. 2004. Noninvasive techniques for assessing skeletal changes in inflammatory arthritis:bone biomarkers. Curr Opin Rheumatol, 16:428-34.
22. Garnero P, Ferreras M, Karsdal MA, et al. 2003. The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J Bone Miner Res, 18:859-67.
23. Garnero P, Jouvenne P, Buchs N, et al. 1999. Uncoupling of bone metabolism in rheumatoid arthritis patients with or without joint destruction: assessment with serum type I collagen breakdown products. Bone, 24:381-5.
24. Genant HK, Engelke K, Fuerst T, et al. 1996. Noninvasive assessment of bone mineral and structure:state of the art. J Bone Miner Res, 11:707-30.
25. Genovese MC, Bathon JM, Martin RW, et al. 2002. Etanercept versus methotrexate in patients with early rheumatoid arthritis:two-year radiographic and clinical outcomes. Arthritis Rheum, 46:1443-50.
26. Gilbert L, He X, Farmer P, et al. 2000. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology, 141:3956-64.
27. Gilbert L, He X, Farmer P, et al. 2002. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem, 277:2695-701.
28. Goldring SR, Gravallese EM. 2000. Mechanisms of bone loss in inflammatory arthritis:diagnosis and therapeutic implications. Arthritis Res, 2:33-7.
29. Gough AK, Lilley J, Eyre S, et al. 1994. Generalised bone loss in patients with early rheumatoid arthritis. Lancet, 344:23-7.
30. Gravallese EM. 2002. Bone destruction in arthritis. Ann Rheum Dis, 61(Suppl 2):ii84-6.
31. Gravallese EM, Harada Y, Wang JT, et al. 1998. Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am J Pathol, 152:943-51.
32. Gravallese EM, Manning C, Tsay A, et al. 2000. Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor. Arthritis Rheum, 43:250-8.
33. Green MJ, Deodhar AA. 2001. Bone changes in early rheumatoid arthritis. Best Pract Res Clin Rheumatol, 15:105-23.
34. Guler-Yuksel M, Bijsterbosch J, Goekoop-Ruiterman YP, et al. 2007. Changes in bone mineral density in patients with recent onset, active rheumatoid arthritis. Ann Rheum Dis, 67:823-8.
35. Hall GM, Spector TD, Griffin AJ, et al. 1993. The effect of rheumatoid arthritis and steroid therapy on bone density in postmenopausal women. Arthritis Rheum, 36:1510-6.
36. Haugeberg G, Orstavik RE, Uhlig T, et al. 2002. Bone loss in patients with rheumatoid arthritis:results from a population-based cohort of 366 patients followed up for two years. Arthritis Rheum, 46:1720-8.
37. Hill PA, Tumber A, Meikle MC. 1997. Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology, 138:3849-58.
38. Hofbauer LC, Dunstan CR, Spelsberg TC, et al. 1998. Osteoprotegerin production by human osteoblast lineage cells is stimulated by vitamin D, bone morphogenetic protein-2, and cytokines. Biochem Biophys Res Commun, 250:776-81.
39. Hofbauer LC, Heufelder AE. 2001. The role of osteoprotegerin and receptor activator of nuclear factor kappaB ligand in the pathogenesis and treatment of rheumatoid arthritis. Arthritis Rheum, 44:253-9.
40. Hoshino K, Hanyu T, Arai K, et al. 2001. Mineral density and histomorphometric assessment of bone changes in the proximal tibia early after induction of type II collagen-induced arthritis in growing and mature rats. J Bone Miner Metab, 19:76-83.
41. Huusko TM, Korpela M, Karppi P, et al. 2001. Threefold increased risk of hip fractures with rheumatoid arthritis in Central Finland. Ann Rheum Dis, 60:521-2.
42. Inui T, Ishibashi O, Inaoka T, et al. 1997. Cathepsin K antisense oligodeoxynucleotide inhibits osteoclastic bone resorption. J Biol Chem, 272:8109-12.
43. Ishikawa H, Ohno O, Hirohata K. 1984. An electron microscopic study of the synovial-bone junction in rheumatoid arthritis. Rheumatol Int, 4:1-8.
44. Jensen T, Klarlund M, Hansen M, et al. 2004. Bone loss in unclassified polyarthritis and early rheumatoid arthritis is better detected by digital x ray radiogrammetry than dual x ray absorptiometry:relationship with disease activity and radiographic outcome. Ann Rheum Dis, 63:15-22.
45. Jilka RL, Weinstein RS, Bellido T, et al. 1998. Osteoblast programmed cell death (apoptosis):modulation by growth factors and cytokines. J Bone Miner Res, 13:793-802.
46. Joosten LA, Helsen MM, Saxne T, et al. 1999. IL-1 alpha beta blockade prevents cartilage and bone destruction in murine type II collageninduced arthritis, whereas TNF-alpha blockade only ameliorates joint inflammation. J Immunol, 163:5049-55.
47. Kanematsu M, Sato T, Takai H, et al. 2000. Prostaglandin E2 induces expression of receptor activator of nuclear factor-kappa B ligand/osteoprotegrin ligand on pre-B cells:implications for accelerated osteoclastogenesis in estrogen deficiency. J Bone Miner Res, 15:1321-9.
48. Keystone EC, Kavanaugh AF, Sharp JT, et al. 2004. Radiographic, clinical, and functional outcomes of treatment with adalimumab (a human anti-tumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy: a randomized, placebo-controlled, 52-week trial. Arthritis Rheum, 50:1400-11.
49. Kong YY, Boyle WJ, Penninger JM. 2000. Osteoprotegerin ligand:a regulator of immune responses and bone physiology. Immunol Today, 21:495-502.
50. Kong YY, Feige U, Sarosi I, et al. 1999. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature, 402:304-9.
51. Kroot EJ, Nieuwenhuizen MG, De Waal Malefijt, MC, et al. 2001. Change in bone mineral density in patients with rheumatoid arthritis during the first decade of the disease. Arthritis Rheum, 44:1254-60.
52. Kuroki T, Shingu M, Koshihara Y, et al. 1994. Effects of cytokines on alkaline phosphatase and osteocalcin production, calcification and calcium release by human osteoblastic cells. Br J Rheumatol, 33:224-30.
53. Laan RF, Buijs WC, Verbeek AL, et al. 1993. Bone mineral density in patients with recent onset rheumatoid arthritis:influence of disease activity and functional capacity. Ann Rheum Dis, 52:21-6.
54. Lange U, Teichmann J, Muller-Ladner U, et al. 2005. Increase in bone mineral density of patients with rheumatoid arthritis treated with anti-TNF-alpha antibody:a prospective open-label pilot study. Rheumatology (Oxford), 44:1546-8.
55. Lipsky PE, Van Der Heijde DM, St Clair EW, et al. 2000. Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. N Engl J Med, 343:1594-602.
56. Maini R, St Clair EW, Breedveld F, et al. 1999. Infliximab (chimeric antitumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate:a randomised phase III trial. ATTRACT Study Group. Lancet, 354:1932-9.
57. Marotte H, Maslinski W, Miossec P. 2005. Circulating tumour necrosis factor-alpha bioactivity in rheumatoid arthritis patients treated with infliximab:link to clinical response. Arthritis Res Ther, 7:R149-55.
58. Marotte H, Pallot-Prades B, Grange L, et al. 2007. A 1-year case-control study in patients with rheumatoid arthritis indicates prevention of loss of bone mineral density in both responders and nonresponders to infliximab. Arthritis Res Ther, 9:R61.
59. McClung MR, Lewiecki EM, Cohen SB, et al. 2006. Denosumab in postmenopausal women with low bone mineral density. N Engl J Med, 354:821-31.
60. Mikuls TR. 2003. Co-morbidity in rheumatoid arthritis. Best Pract Res Clin Rheumatol, 17:729-52.
61. Min H, Morony S, Sarosi I, et al. 2000. Osteoprotegerin reverses osteoporosis by inhibiting endosteal osteoclasts and prevents vascular calcification by blocking a process resembling osteoclastogenesis. J Exp Med, 192:463-74.
62. Morony S, Capparelli C, Lee R, et al. 1999. A chimeric form of osteoprotegerin inhibits hypercalcemia and bone resorption induced by IL-1beta, TNF-alpha, PTH, PTHrP, and 1, 25(OH)2D3. J Bone Miner Res, 14:1478-85.
63. Nakase T, Takaoka K, Masuhara K, et al. 1997. Interleukin-1 beta enhances and tumor necrosis factor-alpha inhibits bone morphogenetic protein-2-induced alkaline phosphatase activity in MC3T3-E1 osteoblastic cells. Bone, 21:17-21.
64. Nakashima T, Kobayashi Y, Yamasaki S, et al. 2000. Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand:modulation of the expression by osteotropic factors and cytokines. Biochem Biophys Res Commun, 275:768-75.
65. Nguyen L, Dewhirst FE, Hauschka PV, et al. 1991. Interleukin-1 beta stimulates bone resorption and inhibits bone formation in vivo. Lymphokine Cytokine Res, 10:15-21.
66. Pacifici R, Avioli LV. 1993. The effect of natural and surgical menopause on the secretion of cytokines from human blood monocytes. Osteoporos Int, 3(Suppl 1):106-7.
67. Page G, Miossec, P. 2005. RANK and RANKL expression as markers of dendritic cell-T cell interactions in paired samples of rheumatoid synovium and lymph nodes. Arthritis Rheum, 52:2307-12.
68. Peel NF, Moore DJ, Barrington NA, et al. 1995. Risk of vertebral fracture and relationship to bone mineral density in steroid treated rheumatoid arthritis. Ann Rheum Dis, 54:801-6.
69. Pettit AR, Ji H, Von Stechow D, et al. 2001. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol, 159:1689-99.
70. Redlich K, Hayer S, Maier A, et al. 2002a. Tumor necrosis factor alphamediated joint destruction is inhibited by targeting osteoclasts with osteoprotegerin. Arthritis Rheum, 46:785-92.
71. Redlich K, Hayer S, Ricci R, et al. 2002b. Osteoclasts are essential for TNFalpha-mediated joint destruction. J Clin Invest, 110:1419-27.
72. Ritchlin CT, Haas-Smith SA, Li P, et al. 2003. Mechanisms of TNF-alphaand RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest, 111:821-31.
73. Romas E, Sims NA, Hards DK, et al. 2002. Osteoprotegerin reduces osteoclast numbers and prevents bone erosion in collagen-induced arthritis. Am J Pathol, 161:1419-27.
74. Saidenberg-Kermanac H N, Corrado A, Lemeiter D, et al. 2004. TNF-alpha antibodies and osteoprotegerin decrease systemic bone loss associated with inflammation through distinct mechanisms in collagen-induced arthritis. Bone, 35:1200-7.
75. Sambrook PN, Eisman JA, Champion GD, et al. 1987. Determinants of axial bone loss in rheumatoid arthritis. Arthritis Rheum, 30:721-8.
76. Sassi ML, Eriksen H, Risteli L, et al. 2000. Immunochemical characterization of assay for carboxyterminal telopeptide of human type I collagen: loss of antigenicity by treatment with cathepsin K. Bone, 26:367-73.
77. Seriolo B, Ferretti V, Sulli A, et al. 2002. Serum osteocalcin levels in premenopausal rheumatoid arthritis patients. Ann N Y Acad Sci, 966:502-7.
78. Shenstone BD, Mahmoud A, Woodward R, et al. 1994. Longitudinal bone mineral density changes in early rheumatoid arthritis. Br J Rheumatol, 33:541-5.
79. Shigeyama Y, Pap T, Kunzler P, et al. 2000. Expression of osteoclast differentiation factor in rheumatoid arthritis. Arthritis Rheum, 43:2523-30.
80. Smolen JS, Han C, Bala M, et al. 2005. Evidence of radiographic benefit of treatment with infliximab plus methotrexate in rheumatoid arthritis patients who had no clinical improvement:a detailed subanalysis of data from the anti-tumor necrosis factor trial in rheumatoid arthritis with concomitant therapy study. Arthritis Rheum, 52:1020-30.
81. Spector TD, Hall GM, McCloskey EV, et al. 1993. Risk of vertebral fracture in women with rheumatoid arthritis. BMJ, 306:558.
82. Taichman RS, Hauschka PV. 1992. Effects of interleukin-1 beta and tumor necrosis factor-alpha on osteoblastic expression of osteocalcin and mineralized extracellular matrix in vitro. Inflammation, 16:587-601.
83. Takayanagi H, Iizuka H, Juji T, et al. 2000. Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum, 43:259-69.
84. Torikai E, Kageyama Y, Takahashi M, et al. 2006. The effect of infliximab on bone metabolism markers in patients with rheumatoid arthritis. Rheumatology (Oxford), 45:761-4.
85. Van Staa TP, Geusens P, Bijlsma JW, et al. 2006. Clinical assessment of the long-term risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum, 54:3104-12.
86. Vergely N, Lafage-Proust MH, Caillot-Augusseau A, et al. 2002. Hypercorticism blunts circadian variations of osteocalcin regardless of nutritional status. Bone, 30:428-35.
87. Vis M, Havaardsholm EA, Haugeberg G, et al. 2006. Evaluation of bone mineral density, bone metabolism, osteoprotegerin and receptor activator of the NFkappaB ligand serum levels during treatment with infliximab in patients with rheumatoid arthritis. Ann Rheum Dis, 65:1495-9.
88. Vis M, Voskuyl AE, Wolbink GJ, et al. 2005. Bone mineral density in patients with rheumatoid arthritis treated with infliximab. Ann Rheum Dis, 64:336-7.
89. Vis M, Wolbink GJ, Lodder MC, et al. 2003. Early changes in bone metabolism in rheumatoid arthritis patients treated with infliximab. Arthritis Rheum, 48:2996-7.
90. Warzocha K, Ribeiro P, Bienvenu J, et al. 1998. Genetic polymorphisms in the tumor necrosis factor locus influence non-Hodgkin's lymphoma outcome. Blood, 91:3574-81.
91. Weinblatt ME, Kremer JM, Bankhurst AD, et al. 1999. A trial of etanercept, a recombinant tumor necrosis factor receptor:Fc fusion protein, in patients with rheumatoid arthritis receiving methotrexate. N Engl J Med, 340:253-9.
92. Westhovens R, Dequeker J. 2000. Rheumatoid arthritis and osteoporosis. Z Rheumatol, 59(Suppl 1):33-8.
93. Yudoh K, Matsuno H, Osada R, et al. 2000. Decreased cellular activity and replicative capacity of osteoblastic cells isolated from the periarticular bone of rheumatoid arthritis patients compared with osteoarthritis patients. Arthritis Rheum, 43:2178-88.
94. Ziolkowska M, Kurowska M, Radzikowska A, et al. 2002. High levels of osteoprotegerin and soluble receptor activator of nuclear factor kappa B ligand in serum of rheumatoid arthritis patients and their normalization after anti-tumor necrosis factor alpha treatment. Arthritis Rheum, 46:1744-53.