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Clinical and Developmental Immunology
Volume 2013 (2013), Article ID 945945, 7 pages
http://dx.doi.org/10.1155/2013/945945
Review Article

Bone Effects of Biologic Drugs in Rheumatoid Arthritis

Rheumatology Clinic, Department of Medical and Surgical Sciences, University of Foggia, Ospedale “Col. D’Avanzo”, Viale degli Aviatori, 71100 Foggia, Italy

Received 3 April 2013; Accepted 2 June 2013

Academic Editor: Giorgio Mori

Copyright © 2013 Addolorata Corrado et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. D. Spector, G. M. Hall, E. V. McCloskey, and J. A. Kanis, “Risk of vertebral fracture in women with rheumatoid arthritis,” British Medical Journal, vol. 306, no. 6877, p. 558, 1993. View at Scopus
  2. A. K. S. Gough, J. Lilley, S. Eyre, R. L. Holder, and P. Emery, “Generalised bone loss in patients with early rheumatoid arthritis,” The Lancet, vol. 344, no. 8914, pp. 23–27, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. C. N. Bernstein, J. F. Blanchard, W. Leslie, A. Wajda, and B. N. Yu, “The incidence of fracture among patients with inflammatory bowel disease: a population-based cohort study,” Annals of Internal Medicine, vol. 133, no. 10, pp. 795–I50, 2000. View at Scopus
  4. I. E. M. Bultink, W. F. Lems, P. J. Kostense, B. A. C. Dijkmans, and A. E. Voskuyl, “Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 52, no. 7, pp. 2044–2050, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. A. E. Oostlander, V. Everts, T. Schoenmaker et al., “T cell-mediated increased osteoclast formation from peripheral blood as a mechanism for crohn's disease-associated bone loss,” Journal of Cellular Biochemistry, vol. 113, no. 1, pp. 260–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Colucci, G. Brunetti, F. P. Cantatore et al., “Lymphocytes and synovial fluid fibroblasts support osteoclastogenesis through RANKL, TNFα, and IL-7 in an in vitro model derived from human psoriatic arthritis,” Journal of Pathology, vol. 212, no. 1, pp. 47–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Wilkison, K. Gauss, Y. Ran, S. Searles, D. Taylor, and M. Meissner, “Type 1 interferons suppress accelerated osteoclastogenesis and prevent loss of bone mass during systemic inflammatory responses to Pneumocystis lung infection,” The American Journal of Pathology, vol. 81, pp. 151–162, 2012.
  8. R. Hardy and M. S. Cooper, “Bone loss in inflammatory disorders,” Journal of Endocrinology, vol. 201, no. 3, pp. 309–320, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Keffer, L. Probert, H. Cazlaris et al., “Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis,” EMBO Journal, vol. 10, no. 13, pp. 4025–4031, 1991. View at Scopus
  10. F. Eggelmeijer, S. E. Papapoulos, M. L. Westedt, H. C. van Paassen, B. A. C. Dijkmans, and F. C. Breedveld, “Bone metabolism in rheumatoid arthritis: relation to disease activity,” British Journal of Rheumatology, vol. 32, no. 5, pp. 387–391, 1993. View at Scopus
  11. P. N. Sambrook, “The skeleton in rheumatoid arthritis: common mechanisms for bone erosion and osteoporosis?” Journal of Rheumatology, vol. 27, no. 11, pp. 2541–2542, 2000. View at Scopus
  12. P. Sambrook, “Tumour necrosis factor blockade and the risk of osteoporosis: back to the future,” Arthritis Research and Therapy, vol. 9, no. 4, article 107, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Kruppa, B. Thoma, T. Machleidt, K. Wiegmann, and M. Krönke, “Inhibition of tumor necrosis factor (TNF)-mediated NF-κB activation by selective blockade of the human 55-kDa TNF receptor,” Journal of Immunology, vol. 148, no. 10, pp. 3152–3157, 1992. View at Scopus
  14. E. M. Gravallese, C. Manning, A. Tsay et al., “Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor,” Arthritis and Rheumatism, vol. 43, no. 2, pp. 250–258, 2000.
  15. J. Lam, S. Takeshita, J. E. Barker, O. Kanagawa, F. P. Ross, and S. L. Teitelbaum, “TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand,” Journal of Clinical Investigation, vol. 106, no. 12, pp. 1481–1488, 2000. View at Scopus
  16. K. Fuller, C. Murphy, B. Kirstein, S. W. Fox, and T. J. Chambers, “TNFα potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL,” Endocrinology, vol. 143, no. 3, pp. 1108–1118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Komine, A. Kukita, T. Kukita, Y. Ogata, T. Hotokebuchi, and O. Kohashi, “Tumor necrosis factor-α cooperates with receptor activator of nuclear factor κB ligand in generation of osteoclasts in stromal cell-depleted rat bone marrow cell culture,” Bone, vol. 28, no. 5, pp. 474–483, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Kobayashi, N. Takahashi, E. Jimi et al., “Tumor necrosis factor α stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction,” Journal of Experimental Medicine, vol. 191, no. 2, pp. 275–285, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. B. F. Boyce, E. M. Schwarz, and L. Xing, “Osteoclast precursors: cytokine-stimulated immunomodulators of inflammatory bone disease,” Current Opinion in Rheumatology, vol. 18, no. 4, pp. 427–432, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Gilbert, X. He, P. Farmer et al., “Inhibition of osteoblast differentiation by tumor necrosis factor-α,” Endocrinology, vol. 141, no. 11, pp. 3956–3964, 2000. View at Scopus
  21. E. Pascher, A. Perniok, A. Becker, and J. Feldkamp, “Effect of 1α,25(OH)2-vitamin D3 on TNFα-mediated apoptosis of human primary osteoblast-like cells in vitro,” Hormone and Metabolic Research, vol. 31, no. 12, pp. 653–656, 1999. View at Scopus
  22. L. Gilbert, X. He, P. Farmer, et al., “Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha,” The Journal of Biological Chemistry, vol. 277, no. 4, pp. 2695–2701, 2002.
  23. X. Lu, L. Gilbert, X. He, J. Rubin, and M. S. Nanes, “Transcriptional regulation of the osterix (Osx, Sp7) promoter by tumor necrosis factor identifies disparate effects of mitogen-activated protein kinase and NFκB pathways,” Journal of Biological Chemistry, vol. 281, no. 10, pp. 6297–6306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Diarra, M. Stolina, K. Polzer et al., “Dickkopf-1 is a master regulator of joint remodeling,” Nature Medicine, vol. 13, no. 2, pp. 156–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Kotake, T. Yago, M. Kawamoto, and Y. Nanke, “Role of osteoclasts and interleukin-17 in the pathogenesis of rheumatoid arthritis: crucial ‘human osteoclastology’,” Journal of Bone and Mineral Metabolism, vol. 30, no. 2, pp. 125–135, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. I. E. Adamopoulos, M. Tessmer, C.-C. Chao et al., “IL-23 is critical for induction of arthritis, osteoclast formation, and maintenance of bone mass,” Journal of Immunology, vol. 187, no. 2, pp. 951–959, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Maruotti, M. Grano, S. Colucci, F. d'Onofrio, and F. P. Cantatore, “Osteoclastogenesis and arthritis,” Clinical and Experimental Medicine, vol. 11, no. 3, pp. 137–145, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. B. le Goff, F. Blanchard, J.-M. Berthelot, D. Heymann, and Y. Maugars, “Role for interleukin-6 in structural joint damage and systemic bone loss in rheumatoid arthritis,” Joint Bone Spine, vol. 77, no. 3, pp. 201–205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Polzer, L. Joosten, J. Gasser et al., “Interleukin-1 is essential for systemic inflammatory bone loss,” Annals of the Rheumatic Diseases, vol. 69, no. 1, pp. 284–290, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Ma, S. Thornton, G. P. Boivin, D. Hirsh, R. Hirsh, and E. Hirsh, “Altered susceptibility to collagen-induced arthritis in transgenic mice with aberrant expression of interleukin-1 receptor antagonist,” Arthritis & Rheumatism, vol. 41, pp. 1798–1805, 1998.
  31. W. B. van den Berg, “Uncoupling of inflammatory and destructive mechanisms in arthritis,” Seminars in Arthritis and Rheumatism, vol. 30, no. 5, supplement 2, pp. 7–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. W. B. van den Berg, “Arguments for interleukin 1 as a target in chronic arthritis,” Annals of the Rheumatic Diseases, vol. 59, supplement 1, pp. i81–i84, 2000. View at Scopus
  33. F. A. Houssiau, J.-P. Devogelaer, J. van Damme, C. Nagant de Deuxchaisnes, and J. van Snick, “Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides,” Arthritis and Rheumatism, vol. 31, no. 6, pp. 784–788, 1988. View at Scopus
  34. G. Steiner, M. Tohidast-Akrad, G. Witzmann et al., “Cytokine production by synovial T cells in rheumatoid arthritis,” Rheumatology, vol. 38, no. 3, pp. 202–213, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Hashizume and M. Mihara, “The roles of interleukin-6 in the pathogenesis of rheumatoid arthritis,” Arthritis, vol. 2011, Article ID 765624, 8 pages, 2011. View at Publisher · View at Google Scholar
  36. M. A. Karsdal, G. Schett, P. Emery et al., “IL-6 receptor inhibition positively modulates bone balance in rheumatoid arthritis patients with an inadequate response to anti-tumor necrosis factor therapy: biochemical marker analysis of bone metabolism in the tocilizumab RADIATE study (NCT00106522),” Seminars in Arthritis and Rheumatism, vol. 42, no. 2, pp. 131–139, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Zwerina, B. Tuerk, K. Redlich, J. S. Smolen, and G. Schett, “Imbalance of local bone metabolism in inflammatory arthritis and its reversal upon tumor necrosis factor blockade: direct analysis of bone turnover in murine arthritis,” Arthritis Research & Therapy, vol. 8, no. 1, p. R22, 2006. View at Scopus
  38. M. Stolina, G. Schett, D. Dwyer et al., “RANKL inhibition by osteoprotegerin prevents bone loss without affecting local or systemic inflammation parameters in two rat arthritis models: comparison with anti-TNFα or anti-IL-1 therapies,” Arthritis Research and Therapy, vol. 11, no. 6, article R187, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Saidenberg-Kermanac'h, A. Corrado, D. Lemeiter, M. C. deVernejoul, M. C. Boissier, and M. E. Cohen-Solal, “TNF-α antibodies and osteoprotegerin decrease systemic bone loss associated with inflammation through distinct mechanisms in collagen-induced arthritis,” Bone, vol. 35, no. 5, pp. 1200–1207, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. C. T. Ritchlin, S. A. Haas-Smith, P. Li, D. G. Hicks, and E. M. Schwarz, “Mechanisms of TNF-α- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis,” Journal of Clinical Investigation, vol. 111, no. 6, pp. 821–831, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Torikai, Y. Kageyama, M. Takahashi et al., “The effect of infliximab on bone metabolism markers in patients with rheumatoid arthritis,” Rheumatology, vol. 45, no. 6, pp. 761–764, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Vis, E. A. Havaardsholm, G. Haugeberg et al., “Evaluation of bone mineral density, bone metabolism, osteoprotegerin and receptor activator of the NFκB ligand serum levels during treatment with infliximab in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 65, no. 11, pp. 1495–1499, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. U. Lange, J. Teichmann, U. Müller-Ladner, and J. Strunk, “Increase in bone mineral density of patients with rheumatoid arthritis treated with anti-TNF-α antibody: a prospective open-label pilot study,” Rheumatology, vol. 44, no. 12, pp. 1546–1548, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Chopin, P. Garnero, A. le Henanff et al., “Long-term effects of infliximab on bone and cartilage turnover markers in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 67, no. 3, pp. 353–357, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Haugeberg, P. G. Conaghan, M. Quinn, and P. Emery, “Bone loss in patients with active early rheumatoid arthritis: infliximab and methotrexate compared with methotrexate treatment alone. Explorative analysis from a 12-month randomised, double-blind, placebo-controlled study,” Annals of the Rheumatic Diseases, vol. 68, no. 12, pp. 1898–1901, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. D. A. Eekman, M. Vis, I. E. M. Bultink et al., “Stable bone mineral density in lumbar spine and hip in contrast to bone loss in the hands during long-term treatment with infliximab in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 70, no. 2, pp. 389–390, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. C. A. Wijbrandts, R. Klaasen, M. G. W. Dijkgraaf, D. M. Gerlag, B. L. F. van Eck-Smit, and P. P. Tak, “Bone mineral density in rheumatoid arthritis patients 1 year after adalimumab therapy: arrest of bone loss,” Annals of the Rheumatic Diseases, vol. 68, no. 3, pp. 373–376, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Vis, A. E. Voskuyl, G. J. Wolbink, B. A. C. Dijkmans, and W. F. Lems, “Bone mineral density in patients with rheumatoid arthritis treated with infliximab,” Annals of the Rheumatic Diseases, vol. 64, no. 2, pp. 336–337, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Marotte, B. Pallot-Prades, L. Grange, P. Gaudin, C. Alexandre, and P. Miossec, “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 Research and Therapy, vol. 9, no. 3, article R61, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. D. A. Eekman, M. Vis, I. E. M. Bultink et al., “Stable bone mineral density in lumbar spine and hip in contrast to bone loss in the hands during long-term treatment with infliximab in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 70, no. 2, pp. 389–390, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Güler-Yüksel, C. F. Allaart, Y. P. M. Goekoop-Ruiterman et al., “Changes in hand and generalised bone mineral density in patients with recent-onset rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 68, no. 3, pp. 330–336, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Dirven, M. Güler-Yüksel, W. M. de Beus et al., “Changes in hand bone mineral density and the association with the level of disease activity in patients with rheumatoid arthritis: bone mineral density measurements in a multicenter randomized clinical trial,” Arthritis Care and Research, vol. 63, no. 12, pp. 1691–1699, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Hoff, T. K. Kvien, J. Kälvesten, A. Elden, A. Kavanaugh, and G. Haugeberg, “Adalimumab reduces hand bone loss in rheumatoid arthritis independent of clinical response: subanalysis of the PREMIER study,” BMC Musculoskeletal Disorders, vol. 12, article 54, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. B. F. Ricciardi, J. Paul, A. Kim, L. A. Russell, and J. M. Lane, “Osteoporosis drug therapy strategies in the setting of disease-modifying agents for autoimmune disease,” Osteoporosis International, vol. 24, no. 2, pp. 423–432, 2013. View at Publisher · View at Google Scholar
  55. S. Y. Kim, S. Schneeweiss, J. Liu, and D. H. Solomon, “Effects of disease-modifying antirheumatic drugs on nonvertebral fracture risk in rheumatoid arthritis: a population-based cohort study,” Journal of Bone and Mineral Research, vol. 27, no. 4, pp. 789–796, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. J. M. Kremer, R. Blanco, M. Brzosko et al., “Tocilizumab inhibits structural joint damage in rheumatoid arthritis patients with inadequate responses to methotrexate: results from the double-blind treatment phase of a randomized placebo-controlled trial of tocilizumab safety and prevention of structural joint damage at one year,” Arthritis and Rheumatism, vol. 63, no. 3, pp. 609–621, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Garnero, E. Thompson, T. Woodworth, and J. S. Smolen, “Rapid and sustained improvement in bone and cartilage turnover markers with the anti-interleukin-6 receptor inhibitor tocilizumab plus methotrexate in rheumatoid arthritis patients with an inadequate response to methotrexate: results from a substudy of the multicenter double-blind, placebo-controlled trial of tocilizumab in inadequate responders to methotrexate alone,” Arthritis and Rheumatism, vol. 62, no. 1, pp. 33–43, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. L. A. B. Joosten, M. M. A. Helsen, T. Saxne, F. A. J. van de Loo, D. Heinegård, and W. B. van den Berg, “IL-1αβ blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-α blockade only ameliorates joint inflammation,” Journal of Immunology, vol. 163, no. 9, pp. 5049–5055, 1999. View at Scopus
  59. A. Bendele, T. McAbee, G. Sennello, J. Frazier, E. Chlipala, and D. McCabe, “Efficacy of sustained blood levels of interelukin-1 receptor antagonist in animal models of arthritis: comparison of efficacy in animal models with human clinical data,” Arthritis & Rheumatism, vol. 42, pp. 498–506, 1999.
  60. B. Bresnihan, J. M. Alvaro-Garcia, M. Cobby, et al., “Treatment of rheumatoid arthritis with recombinant human IL-1ra,” Arthritis & Rheumatism, vol. 41, no. 12, pp. 2196–2204, 1998.
  61. R. B. Kimble, J. L. Vannice, D. C. Bloedow et al., “Interleukin-1 receptor antagonist decreases bone loss and bone resorption in ovariectomized rats,” Journal of Clinical Investigation, vol. 93, no. 5, pp. 1959–1967, 1994. View at Scopus
  62. N. Charatcharoenwitthaya, S. Khosla, E. J. Atkinson, L. K. McCready, and B. L. Riggs, “Effect of blockade of TNF-α and interleukin-1 action on bone resorption in early postmenopausal women,” Journal of Bone and Mineral Research, vol. 22, no. 5, pp. 724–729, 2007. View at Publisher · View at Google Scholar · View at Scopus