Osteoporosis International

, Volume 24, Issue 2, pp 423–432 | Cite as

Osteoporosis drug therapy strategies in the setting of disease-modifying agents for autoimmune disease

  • B. F. Ricciardi
  • J. Paul
  • A. Kim
  • L. A. Russell
  • J. M. Lane
Review

Abstract

The purpose of this systematic review is to evaluate the effects of methotrexate (MTX) and tumor necrosis factor-alpha (TNF-α) inhibitors on bone mineral properties in the clinical literature. A systematic review of the literature identifying relevant case reports, population-based studies, cohort studies, case control studies, and randomized controlled trials in Pubmed and Web of Science databases from inception to December 31, 2011 was conducted. The following keywords were used: “bone turnover,” “bone mineral density,” “TNF-α inhibitors,” “infliximab,” “adalimumab,” “etanercept,” and “MTX.” The bibliographies of all retrieved studies were also reviewed to identify additional articles. Based on these results, a rational drug therapy strategy was suggested for treating osteoporosis in patients with inflammatory disease. MTX and TNF-α inhibitors do not appear to have an adverse effect on BMD in patients with inflammatory disease. Their negative effects on BMD and bone turnover in pre-clinical models appear to be outweighed by their anti-disease effects in clinical studies. Treatment with MTX or TNF-α inhibitors has no adverse effect on BMD in patients with inflammatory disease. Future studies will focus on developing optimal drug strategies when combining DMARDs with anti-osteoporotic agents in this patient population.

Keywords

Bone mineral density Disease-modifying agents Methotrexate Osteoporosis Tumor necrosis factor-alpha inhibitors 

References

  1. 1.
    Feely MG, Erickson A, O'Dell JR (2009) Therapeutic options for rheumatoid arthritis. Expert Opin Pharmacother 10(13):2095–2106CrossRefPubMedGoogle Scholar
  2. 2.
    Minaur NJ, Kounali D, Vedi S, Compston JE, Beresford JN, Bhalla AK (2002) Methotrexate in the treatment of rheumatoid arthritis. II. In vivo effects on bone mineral density. Rheumatology (Oxford) 41:714–749CrossRefGoogle Scholar
  3. 3.
    Fan C, Cool JC, Scherer MA, Foster BK, Shandala T, Tapp H, Xian CJ (2009) Damaging effects of chronic low-dose methotrexate usage on primary bone formation in young rats and potential protective effects of folinic acid supplementary treatment. Bone 44:61–70CrossRefPubMedGoogle Scholar
  4. 4.
    Chan ES, Cronstein BN (2010) Methotrexate—how does it really work? Nat Rev Rheumatol 6(3):175–178CrossRefPubMedGoogle Scholar
  5. 5.
    Smolen JS, Aletaha D, Keystone E (2005) Superior efficacy of combination therapy for rheumatoid arthritis: fact or fiction? Arthritis Rheum 52(10):2975–2983CrossRefPubMedGoogle Scholar
  6. 6.
    Saag KG, Koehnke R, Caldwell JR et al (1994) Low dose long-term corticosteroid therapy in rheumatoid arthritis: an analysis of serious adverse events. Am J Med 96(2):115–123CrossRefPubMedGoogle Scholar
  7. 7.
    Maricic M (2011) Update on glucocorticoid-induced osteoporosis. Rheum Dis Clin North Am 37(3):415–431CrossRefPubMedGoogle Scholar
  8. 8.
    Goldring SR (2009) Chapter 59: inflammation-induced bone loss in the rheumatic diseases. In Primer on metabolic bone disease and disorders of mineral metabolism. Chapter 59. John Wiley and Sons, Inc, HobokenGoogle Scholar
  9. 9.
    Celiker R, Gokce-Kutsal Y, Cindas A, Ariyurek M, Renda N, Koray Z, Basgoze O (1995) Osteoporosis in rheumatoid arthritis: effect of disease activity. Clin Rheumatol 14:429–433CrossRefPubMedGoogle Scholar
  10. 10.
    Haugeberg G, Uhlig T, Flach JA, Halse JI, Kvien TK (2000) Bone mineral density and frequency of osteoporosis in female patients with rheumatoid arthritis. Results from 394 patients in the Oslo country rheumatoid arthritis register. Arthritis Rheum 43:522–530CrossRefPubMedGoogle Scholar
  11. 11.
    Kroger H, Honkanen R, Saarikoski S, Alhave E (1994) Decreased axial BMD in perimenopausal women with rheumatoid arthritis—a population-based study. Ann Rheum Dis 53:18–23CrossRefPubMedGoogle Scholar
  12. 12.
    Cortet B, Guyot MH, Solau E, Pigny P, Dumoulin F, Flipo RM (2000) Factors influencing bone loss in rheumatoid arthritis: a longitudinal study. Clin Exp Rheumatol 18:683–690PubMedGoogle Scholar
  13. 13.
    Eastgate JA, Wood NC, Di Giovine FS, Symons JA, Grinlinton FM, Duff GW (1988) Correlation of plasma interleukin-1 levels with disease activity in rheumatoid arthritis. Lancet 340:706–70914CrossRefGoogle Scholar
  14. 14.
    Deodhar AA, Woolf AD (1996) Bone mass measurement and bone metabolism in rheumatoid arthritis: a review. Br J Rheumatol 35:309–322CrossRefPubMedGoogle Scholar
  15. 15.
    Buckley LM, Leib ES, Cartularo KS, Vacek PM, Cooper SM (1995) Effects of low dose corticosteroids on the bone mineral density of patients with rheumatoid arthritis. J Rheumatol 22:1055–1059PubMedGoogle Scholar
  16. 16.
    Saario R, Sonninen P, Mottonen T, Viikari J, Toivanen A (1999) Bone mineral density of the lumbar spine in patients with advanced rheumatoid arthritis: influence of functional capacity and corticosteroid use. Scand J Rheumatol 28:363–367CrossRefPubMedGoogle Scholar
  17. 17.
    Davies JH, Evans BA, Jenney ME, Gregory JW (2002) In vitro effects of chemotherapeutic agents on human osteoblast cells. Calcif Tissue Int 70:408–415CrossRefPubMedGoogle Scholar
  18. 18.
    Malviya A, Kuiper JH, Makwana N, Laing P, Ashton B (2009) The effect of newer anti-rheumatic drugs on osteogenic cell proliferation: an in vitro study. J Orthop Surg Res 4:17CrossRefPubMedGoogle Scholar
  19. 19.
    van der Veen MJ, Scheven BA, van Roy JL, Damen CA, Lafeber FP, Bijlsma JW (1996) In vitro effects of methotrexate on human articular cartilage and bone-derived osteoblasts. Br J Rheumatol 35(4):342–349CrossRefPubMedGoogle Scholar
  20. 20.
    May KP, Mercill D, McDermott MT, West SG (1996) The effect of methotrexate mouse bone cells in culture. Arthritis Rheum 39(3):489–494CrossRefPubMedGoogle Scholar
  21. 21.
    Friedlaender GE, Tross RB, Doganis AC, Kirkwood JM, Baron R (1984) Effects of chemotherapeutic agents on bone. I. Short-term methotrexate and doxorubicin (adriamycin) treatment in a rat model. J Bone Joint Surg Am 66:602–607PubMedGoogle Scholar
  22. 22.
    Wheeler DL, Vander Griend RA, Wronski TJ, Miller GJ, Keith EE, Graves JE (1995) Effects of long-term administration of methotrexate on bone mineral density in rheumatoid arthritis. Bone 16:215–221CrossRefPubMedGoogle Scholar
  23. 23.
    Spadaro JA, Damron TA, Horton JA, Margulies BS, Murray GM, Clemente DA, Strauss JA (2006) Density and structural changes in the bone of growing rats after weekly alendronate administration with and without a methotrexate challenge. J Orthop Res 24:936–944CrossRefPubMedGoogle Scholar
  24. 24.
    Gnudi S, Butturini L, Ripamonti C, Avella M, Bacci G (1988) The effect of methotrexate on bone. A densitometric study conducted on 59 patients with methotrexate administered at different doses. Ital J Orthop Traumatol 14:227–231PubMedGoogle Scholar
  25. 25.
    Wijnands M, Burgers A (2001) Stress fracture in long term methotrexate treatment for psoriatic arthritis. Ann Rheum Dis 60:736–738CrossRefPubMedGoogle Scholar
  26. 26.
    Zonneveld IM, Bakker WK, Dijkstra PF, Bos JD, van Soesbergen RM, Dinant HJ (1996) Methotrexate osteopathy in long-term, low-dose methotrexate treatment for psoriasis and rheumatoid arthritis. Arch Dermatol 132(2):184–187CrossRefPubMedGoogle Scholar
  27. 27.
    Mäenpää HM, Soini I, Lehto MU, Belt EA (2002) Insufficiency fractures in patients with chronic inflammatory joint diseases. Clin Exp Rheumatol 20(1):77–79PubMedGoogle Scholar
  28. 28.
    Preston SJ, Diamond T, Scott A, Laurent MR (1993) Methotrexate osteopathy in rheumatic disease. Ann Rheum Dis 52(8):582–585CrossRefPubMedGoogle Scholar
  29. 29.
    Kinjo M, Setoguchi S, Solomon DH (2007) Bone mineral density in older adult patients with rheumatoid arthritis: an analysis of NHANES III. J Rheumatol 34(10):1971–1975PubMedGoogle Scholar
  30. 30.
    Carbone LD, Kaely G, McKown KM, Cremer M, Palmieri G, Kaplan S (1999) Effects of long-term administration of methotrexate on bone mineral density in rheumatoid arthritis. Calcif Tissue Int 64:100–101CrossRefPubMedGoogle Scholar
  31. 31.
    Cranney AB, McKendry RJ, Wells GA, Ooi DS, Kanigsberg ND, Kraag GR, Smith CD (2001) The effect of low dose methotrexate on bone density. J Rheumatol 28:2395–2399PubMedGoogle Scholar
  32. 32.
    Di Munno O, Mazzantini M, Sinigaglia L, Bianchi G, Minisola G, Muratore M, La Corte R, Di Matteo L, Canesi B, Caminiti M, Broggini M, Adami S (2004) Effect of low dose methotrexate on bone density in women with rheumatoid arthritis: results from a multicenter cross-sectional study. J Rheumatol 31:1305–1309PubMedGoogle Scholar
  33. 33.
    Vestergaard P, Rejnmark L, Mosekilde L (2006) Methotrexate, azathioprine, cyclosporine, and risk of fracture. Calcif Tissue Int 79:69–75CrossRefPubMedGoogle Scholar
  34. 34.
    Tascioglu F, Oner C, Armagan O (2003) The effect of low-dose methotrexate on bone mineral density in patients with early rheumatoid arthritis. Rheumatol Int 23(5):231–235CrossRefPubMedGoogle Scholar
  35. 35.
    Mazzantini M, Di Munno O, Incerti-Vecchi L, Pasero G (2000) Vertebral bone mineral density changes in female rheumatoid arthritis patients treated with low-dose methotrexate. Clin Exp Rheumatol 18(3):327–331PubMedGoogle Scholar
  36. 36.
    Buckley LM, Leib ES, Cartularo KS, Vacek PM, Cooper SM (1997) Effects of low dose methotrexate on the bone mineral density of patients with rheumatoid arthritis. J Rheumatol 24(8):1489–1494PubMedGoogle Scholar
  37. 37.
    Bianchi ML, Cimaz R, Galbiati E, Corona F, Cherubini R, Bardare M (1999) Bone mass change during methotrexate treatment in patients with juvenile rheumatoid arthritis. Osteoporosis Int 10:20–25CrossRefGoogle Scholar
  38. 38.
    Geusens PP, Landewé RB, Garnero P, Chen D, Dunstan CR, Lems WF, Stinissen P, van der Heijde DM, van der Linden S, Boers M (2006) The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis Rheum 54(6):1772–1777CrossRefPubMedGoogle Scholar
  39. 39.
    Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D, Korb A, Smolen J, Hoffmann M, Scheinecker C, van der Heide D, Landewe R, Lacey D, Richards WG, Schett G (2007) Dickkopf-1 is a master regulator of joint remodeling. Nat Med 13(2):156–163CrossRefPubMedGoogle Scholar
  40. 40.
    Güler-Yüksel M, Bijsterbosch J, Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Hulsmans HM, de Beus WM, Han KH, Breedveld FC, Dijkmans BA, Allaart CF, Lems WF (2008) Changes in bone mineral density in patients with recent onset, active rheumatoid arthritis. Ann Rheum Dis 67(6):823–828CrossRefPubMedGoogle Scholar
  41. 41.
    Eekman DA, Vis M, Bultink IE, Kuik DJ, Voskuyl AE, Dijkmans BA, Lems WF (2011) 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. Ann Rheum Dis 70(2):389–390CrossRefPubMedGoogle Scholar
  42. 42.
    Marotte H, Pallot-Prades B, Grange L, Gaudin P, Alexandre C, Miossec P (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(3):R61CrossRefPubMedGoogle Scholar
  43. 43.
    Haugeberg G, Conaghan PG, Quinn M, Emery P (2009) 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. Ann Rheum Dis 68(12):1898–1901CrossRefPubMedGoogle Scholar
  44. 44.
    Lange U, Teichmann J, Müller-Ladner U, Strunk J (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(12):1546–1548CrossRefGoogle Scholar
  45. 45.
    Wijbrandts CA, Klaasen R, Dijkgraaf MGW, Gerlag DM, van Eck-Smit BLF, Tak PP (2009) Bone mineral density in rheumatoid arthritis patients 1 year after adalimumab therapy: arrest of bone loss. Ann Rheum Dis 68:373–376CrossRefPubMedGoogle Scholar
  46. 46.
    Vis M, Havaardsholm EA, Haugeberg G, Uhlig T, Voskuyl AE, van de Stadt RJ, Dijkmans BA, Woolf AD, Kvien TK, Lems WF (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 65:1495–1499CrossRefPubMedGoogle Scholar
  47. 47.
    Chopin F, Garnero P, le Henanff A, Debiais F, Daragon A, Roux C, Sany J, Wendling D, Zarnitsky C, Ravaud P, Thomas T (2008) Long-term effects of infliximab on bone and cartilage turnover markers in patients with rheumatoid arthritis. Ann Rheum Dis 67(3):353–357CrossRefPubMedGoogle Scholar
  48. 48.
    Seriolo B, Paolino S, Sulli A, Ferretti V, Cutolo M (2006) Bone metabolism changes during anti-TNF-alpha therapy in patients with active rheumatoid arthritis. Ann N Y Acad Sci 1069:420–427CrossRefPubMedGoogle Scholar
  49. 49.
    Unnanuntana A, Gladnick BP, Donnelly E, Lane JM (2010) The assessment of fracture risk. J Bone Joint Surg Am 92(3):743–753CrossRefPubMedGoogle Scholar
  50. 50.
    Kim SY, Schneeweiss S, Liu J, Solomon DH (2011) Effects of disease-modifying antirheumatic drugs on non-vertebral fracture risk in rheumatoid arthritis: a population-based cohort study. J Bone Miner Res. doi:10.1002/jbmr.1489
  51. 51.
    Simonini G, Giani T, Stagi S, de Martino M, Falcini F (2005) Bone status over 1 yr of etanercept treatment in juvenile idiopathic arthritis. Rheumatology (Oxford) 44(6):777–780CrossRefGoogle Scholar
  52. 52.
    Billiau AD, Loop M, Le PQ, Berthet F, Philippet P, Kasran A, Wouters CH (2010) Etanercept improves linear growth and bone mass acquisition in MTX-resistant polyarticular-course juvenile idiopathic arthritis. Rheumatology (Oxford) 49(8):1550–1558CrossRefGoogle Scholar
  53. 53.
    Visvanathan S, van der Heijde D, Deodhar A, Wagner C, Baker DG, Han J, Braun J (2009) Effects of infliximab on markers of inflammation and bone turnover and associations with bone mineral density in patients with ankylosing spondylitis. Ann Rheum Dis 68:175–182CrossRefPubMedGoogle Scholar
  54. 54.
    Briot K, Garnero P, Le Henanff A, Dougados M, Roux C (2005) Body weight, body composition, and bone turnover changes in patients with spondyloarthropathy receiving anti-tumour necrosis factor alpha treatment. Ann Rheum Dis 64(8):1137–1140CrossRefPubMedGoogle Scholar
  55. 55.
    Briot K, Gossec L, Kolta S, Dougados M, Roux C (2008) Prospective assessment of body weight, body composition, and bone density changes in patients with spondyloarthropathy receiving anti-tumor necrosis factor-alpha treatment. J Rhematol 35:855–861Google Scholar
  56. 56.
    Marzo-Ortega H, McGonagle D, Haugeberg G, Green MJ, Stewart SP, Emery P (2003) Bone mineral density improvement in spondyloarthropathy after treatment with etanercept. Ann Rheum Dis 62(10):1020–1021CrossRefPubMedGoogle Scholar
  57. 57.
    Demis E, Roux C, Breban M, Dougados M (2002) Infliximab in spondylarthropathy—influence on bone density. Clin Exp Rheumatol 20(6 Suppl 28):S185–S186PubMedGoogle Scholar
  58. 58.
    Allali F, Breban M, Porcher R, Maillefert JF, Dougados M, Roux C (2003) Increase in bone mineral density of patients with spondyloarthropathy treated with anti-tumour necrosis factor alpha. Ann Rheum Dis 62(4):347–349CrossRefPubMedGoogle Scholar
  59. 59.
    Mauro M, Radovic V, Armstrong D (2007) Improvement of lumbar bone mass after infliximab therapy in Crohn's disease patients. Can J Gastroenterol 21:637–642PubMedGoogle Scholar
  60. 60.
    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(9):2031–2035CrossRefPubMedGoogle Scholar
  61. 61.
    Weinstein RS, Roberson PK, Manolagas SC (2009) Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360(1):53–62CrossRefPubMedGoogle Scholar
  62. 62.
    Lane N, Morris S (2005) New perspectives on parathyroid hormone therapy. Curr Opin Rheumatol 17(4):467–474CrossRefPubMedGoogle Scholar
  63. 63.
    Cummings SR, San Martin J, McClung MR, Siris ES, Eastell R, Reid IR, Delmas P, Zoog HB, Austin M, Wang A, Kutilek S, Adami S, Zanchetta J, Libanati C, Siddhanti S, Christiansen C, FREEDOM Trial (2009) Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med 361(8):756–765CrossRefPubMedGoogle Scholar
  64. 64.
    Lems WF, Lodder MC, Lips P, Bijlsma JW, Geusens P, Schrameijer N, van de Ven CM, Dijkmans BA (2006) Positive effect of alendronate on bone mineral density and markers of bone turnover in patients with rheumatoid arthritis on chronic treatment with low-dose prednisone: a randomized, double-blind, placebo-controlled trial. Osteoporos Int 17(5):716–723CrossRefPubMedGoogle Scholar
  65. 65.
    Mawatari T, Miura H, Hamai S, Shuto T, Nakashima Y, Okazaki K, Kinukawa N, Sakai S, Hoffmann PF, Iwamoto Y, Keaveny TM (2008) Vertebral strength changes in rheumatoid arthritis patients treated with alendronate, as assessed by finite element analysis of clinical computed tomography scans: a prospective randomized clinical trial. Arthritis Rheum 58(11):3340–3349CrossRefPubMedGoogle Scholar
  66. 66.
    Morishita M, Nagashima M, Wauke K, Takahashi H, Takenouchi K (2008) Osteoclast inhibitory effects of vitamin K2 alone or in combination with etidronate or risedronate in patients with rheumatoid arthritis: 2-year results. J Rheumatol 35(3):407–413PubMedGoogle Scholar
  67. 67.
    Reid DM, Devogelaer JP, Saag K, Roux C, Lau CS, Reginster JY, Papanastasiou P, Ferreira A, Hartl F, Fashola T, Mesenbrink P, Sambrook PN, HORIZON investigators (2009) Zoledronic acid and risedronate in the prevention and treatment of glucocorticoid-induced osteoporosis (HORIZON): a multicentre, double-blind, double-dummy, randomised controlled trial. Lancet 373(9671):1253–1263CrossRefPubMedGoogle Scholar
  68. 68.
    Stokkers PC, Deley M, Van Der Spek M, Verberne HJ, Van Deventer SJ, Hommes DW (2006) Intravenous pamidronate in combination with calcium and vitamin D: highly effective in the treatment of low bone mineral density in inflammatory bowel disease. Scand J Gastroenterol 41(2):200–204CrossRefPubMedGoogle Scholar
  69. 69.
    Van Offel JF, Schuerwegh AJ, Bridts CH, Bracke PG, Stevens WJ, De Clerck LS (2001) Influence of cyclic intravenous pamidronate on proinflammatory monocytic cytokine profiles and bone density in rheumatoid arthritis treated with low dose prednisolone and methotrexate. Clin Exp Rheumatol 19(1):13–20PubMedGoogle Scholar
  70. 70.
    Yilmaz L, Ozoran K, Gündüz OH, Uçan H, Yücel M (2001) Alendronate in rheumatoid arthritis patients treated with methotrexate and glucocorticoids. Rheumatol Int 20(2):65–69CrossRefPubMedGoogle Scholar
  71. 71.
    Goldring SR, Gravallese EM (2004) Bisphosphonates: environmental protection for the joint? Arthritis Rheum 50(7):2044–2047CrossRefPubMedGoogle Scholar
  72. 72.
    Pazianas M, Rhim AD, Weinberg AM, Su C, Lichtenstein GR (2006) The effect of anti-TNF-alpha therapy on spinal bone mineral density in patients with Crohn's disease. Ann N Y Acad Sci 1068:543–556CrossRefPubMedGoogle Scholar
  73. 73.
    Bringmann A, Schmidt SM, Weck MM, Brauer KM, von Schwarzenberg K, Werth D, Grünebach F, Brossart P (2007) Zoledronic acid inhibits the function of Toll-like receptor 4 ligand activated monocyte-derived dendritic cells. Leukemia 21(4):732–738PubMedGoogle Scholar
  74. 74.
    Jarrett SJ, Conaghan PG, Sloan VS, Papanastasiou P, Ortmann CE, O'Connor PJ, Grainger AJ, Emery P (2006) Preliminary evidence for a structural benefit of the new bisphosphonate zoledronic acid in early rheumatoid arthritis. Arthritis Rheum 54(5):1410–1414CrossRefPubMedGoogle Scholar
  75. 75.
    Giraudo E, Inoue M, Hanahan D (2004) An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 114(5):623–633PubMedGoogle Scholar
  76. 76.
    Herrak P, Görtz B, Hayer S, Redlich K, Reiter E, Gasser J, Bergmeister H, Kollias G, Smolen JS, Schett G (2004) Zoledronic acid protects against local and systemic bone loss in tumor necrosis factor-mediated arthritis. Arthritis Rheum 50(7):2327–2337CrossRefPubMedGoogle Scholar
  77. 77.
    Cohen SB, Dore RK, Lane NE, Ory PA, Peterfy CG, Sharp JT, van der Heijde D, Zhou L, Tsuji W, Newmark R, Denosumab Rheumatoid Arthritis Study Group (2008) Denosumab treatment effects on structural damage, bone mineral density, and bone turnover in rheumatoid arthritis: a twelve-month, multicenter, randomized, double-blind, placebo-controlled, phase II clinical trial. Arthritis Rheum 58(5):1299–1309CrossRefPubMedGoogle Scholar
  78. 78.
    Sharp JT, Tsuji W, Ory P, Harper-Barek C, Wang H, Newmark R (2010) Denosumab prevents metacarpal shaft cortical bone loss in patients with erosive rheumatoid arthritis. Arthritis Care Res (Hoboken) 62(4):537–544CrossRefGoogle Scholar
  79. 79.
    Ferrari-Lacraz S, Ferrari S (2011) Do RANKL inhibitors (denosumab) affect inflammation and immunity? Osteoporos Int 22(2):435–446CrossRefPubMedGoogle Scholar
  80. 80.
    Saag KG, Shane E, Boonen S, Marín F, Donley DW, Taylor KA, Dalsky GP, Marcus R (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med 357(20):2028–2039CrossRefPubMedGoogle Scholar
  81. 81.
    Saag KG, Zanchetta JR, Devogelaer JP, Adler RA, Eastell R, See K, Krege JH, Krohn K, Warner MR (2009) Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum 60(11):3346–3355CrossRefPubMedGoogle Scholar
  82. 82.
    Redlich K, Görtz B, Hayer S, Zwerina J, Doerr N, Kostenuik P, Bergmeister H, Kollias G, Steiner G, Smolen JS, Schett G (2004) Repair of local bone erosions and reversal of systemic bone loss upon therapy with anti-tumor necrosis factor in combination with osteoprotegerin or parathyroid hormone in tumor necrosis factor-mediated arthritis. Am J Pathol 164(2):543–555CrossRefPubMedGoogle Scholar
  83. 83.
    Aspenberg P, Genant HK, Johansson T, Nino AJ, See K, Krohn K, García-Hernández PA, Recknor CP, Einhorn TA, Dalsky GP, Mitlak BH, Fierlinger A, Lakshmanan MC (2010) Teriparatide for acceleration of fracture repair in humans: a prospective, randomized, double-blind study of 102 postmenopausal women with distal radial fractures. J Bone Miner Res 25(2):404–414CrossRefPubMedGoogle Scholar
  84. 84.
    Barnes GL, Kakar S, Vora S, Morgan EF, Gerstenfeld LC, Einhorn TA (2008) Stimulation of fracture-healing with systemic intermittent parathyroid hormone treatment. J Bone Joint Surg Am 90(Suppl 1):120–127CrossRefPubMedGoogle Scholar
  85. 85.
    Piechl P, Holzer LA, Maier R, Holzer G (2011) Parathyroid hormone 1-84 accelerates fracture healing in pubic bones of elderly osteoporotic women. J Bone Joint Surg 93(17):1583–1587CrossRefGoogle Scholar
  86. 86.
    Rossini M, Bagnato G, Frediani B, Iagnocco A, LA Montagna G, Minisola G, Caminiti M, Varenna M, Adami S (2011) Relationship of focal erosions, bone mineral density, and parathyroid hormone in rheumatoid arthritis. J Rheumatol 38(6):997–1002CrossRefPubMedGoogle Scholar
  87. 87.
    Capeci CM, Tejwani NC (2009) Bilateral low-energy simultaneous or sequential femoral fractures in patients on long-term alendronate therapy. J Bone Joint Surg Am 91(11):2556–2561CrossRefPubMedGoogle Scholar
  88. 88.
    Lenart BA, Neviaser AS, Lyman S, Chang CC, Edobor-Osula F, Steele B, van der Meulen MC, Lorich DG, Lane JM (2009) Association of low-energy femoral fractures with prolonged bisphosphonate use: a case control study. Osteoporos Int 20(8):1353–1362CrossRefPubMedGoogle Scholar
  89. 89.
    Geyer M, Müller-Ladner U (2010) Actual status of antiinterleukin-1 therapies in rheumatic diseases. Curr Opin Rheumatol 22(3):246–251CrossRefPubMedGoogle Scholar
  90. 90.
    Nishimoto N, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, Azuma J (2009) Long-term safety and efficacy of tocilizumab, an anti-IL-6 receptor monoclonal antibody, in monotherapy, in patients with rheumatoid arthritis (the STREAM study): evidence of safety and efficacy in a 5-year extension study. Ann Rheum Dis 68(10):1580–1584CrossRefPubMedGoogle Scholar
  91. 91.
    Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T (2004) Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 350(25):2572–2581CrossRefPubMedGoogle Scholar
  92. 92.
    Schiff M, Bessette L (2010) Evaluation of abatacept in biologic-naïve patients with active rheumatoid arthritis. Clin Rheumatol 29(6):583–591CrossRefPubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2012

Authors and Affiliations

  • B. F. Ricciardi
    • 1
  • J. Paul
    • 2
  • A. Kim
    • 3
  • L. A. Russell
    • 4
  • J. M. Lane
    • 1
  1. 1.Metabolic Bone Disease ServiceHospital for Special SurgeryNew YorkUSA
  2. 2.Weill Cornell Medical CollegeNew YorkUSA
  3. 3.College of Physicians and SurgeonsNew YorkUSA
  4. 4.Department of RheumatologyHospital for Special SurgeryNew YorkUSA

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