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

Osteoporosis International

Volumn 24, Issue 2, 2013, Pages 423-432

  Ricciardi, B F ^a   Paul, J ^b   Kim, A ^c   Russell, L A ^a   Lane, J M ^a  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

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

Indexed keywords

ADALIMUMAB; ALENDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; DENOSUMAB; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; INFLIXIMAB; METHOTREXATE; PAMIDRONIC ACID; PARATHYROID HORMONE[1-34]; PLACEBO; PREDNISONE; SALAZOSULFAPYRIDINE; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; ZOLEDRONIC ACID;

ADD ON THERAPY; AUTOIMMUNE DISEASE; BONE DENSITY; BONE METABOLISM; BONE MINERAL; BONE PAIN; BONE TURNOVER; CLINICAL EVALUATION; COHORT ANALYSIS; COMPRESSION FRACTURE; CORTICOSTEROID THERAPY; CROHN DISEASE; DRUG EFFICACY; DRUG POTENTIATION; DRUG TREATMENT FAILURE; FRAGILITY FRACTURE; HUMAN; INFLAMMATORY DISEASE; JUVENILE RHEUMATOID ARTHRITIS; LOW DRUG DOSE; NONHUMAN; OSTEOLYSIS; OSTEOPOROSIS; OSTEOSARCOMA; PRIORITY JOURNAL; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SPINE FRACTURE; SPONDYLOARTHROPATHY; SYSTEMATIC REVIEW; TREATMENT DURATION;

AUTOIMMUNE DISEASES; BONE DENSITY; BONE DENSITY CONSERVATION AGENTS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; METHOTREXATE; OSTEOPOROSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84873743101     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-012-2113-8     Document Type: Review

References (92)

1. Feely MG, Erickson A, O'Dell JR (2009) Therapeutic options for rheumatoid arthritis. Expert Opin Pharmacother 10(13):2095-2106
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) 41:714-749
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 44:61-70
4. Chan ES, Cronstein BN (2010) Methotrexate - how does it really work? Nat Rev Rheumatol 6(3):175-178
5. Smolen JS, Aletaha D, Keystone E (2005) Superior efficacy of combination therapy for rheumatoid arthritis: fact or fiction? Arthritis Rheum 52(10):2975-2983
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):115-123
7. Maricic M (2011) Update on glucocorticoid-induced osteoporosis. Rheum Dis Clin North Am 37(3):415-431
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, Hoboken
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 14:429-433
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 43:522-530
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 53:18-23
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 18:683-690
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 340:706-70914
14. Deodhar AA, Woolf AD (1996) Bone mass measurement and bone metabolism in rheumatoid arthritis: a review. Br J Rheumatol 35:309-322
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 22:1055-1059
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 28:363-367
17. Davies JH, Evans BA, Jenney ME, Gregory JW (2002) In vitro effects of chemotherapeutic agents on human osteoblast cells. Calcif Tissue Int 70:408-415
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 4:17
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):342-349
20. May KP, Mercill D, McDermott MT, West SG (1996) The effect of methotrexate mouse bone cells in culture. Arthritis Rheum 39(3):489-494
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 66:602-607
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 16:215-221
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 24:936-944
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 14:227-231
25. Wijnands M, Burgers A (2001) Stress fracture in long term methotrexate treatment for psoriatic arthritis. Ann Rheum Dis 60:736-738
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):184-187
27. Mäenpää HM, Soini I, Lehto MU, Belt EA (2002) Insufficiency fractures in patients with chronic inflammatory joint diseases. Clin Exp Rheumatol 20(1):77-79
28. Preston SJ, Diamond T, Scott A, Laurent MR (1993) Methotrexate osteopathy in rheumatic disease. Ann Rheum Dis 52(8):582-585
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):1971-1975
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 64:100-101
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 28:2395-2399
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 31:1305-1309
33. Vestergaard P, Rejnmark L, Mosekilde L (2006) Methotrexate, azathioprine, cyclosporine, and risk of fracture. Calcif Tissue Int 79:69-75
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):231-235
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):327-331
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):1489-1494
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 10:20-25
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):1772-1777
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):156-163
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):823-828
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):389-390
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):R61
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):1898-1901
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):1546-1548
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 68:373-376
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 65:1495-1499
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):353-357
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 1069:420-427
49. Unnanuntana A, Gladnick BP, Donnelly E, Lane JM (2010) The assessment of fracture risk. J Bone Joint Surg Am 92(3):743-753
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. 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):777-780
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):1550-1558
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 68:175-182
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):1137-1140
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 35:855-861
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):1020-1021
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-S186
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):347-349
59. Mauro M, Radovic V, Armstrong D (2007) Improvement of lumbar bone mass after infliximab therapy in Crohn's disease patients. Can J Gastroenterol 21:637-642
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):2031-2035
61. Weinstein RS, Roberson PK, Manolagas SC (2009) Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360(1):53-62
62. Lane N, Morris S (2005) New perspectives on parathyroid hormone therapy. Curr Opin Rheumatol 17(4):467-474
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):756-765
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):716-723
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):3340-3349
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):407-413
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):1253-1263
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):200-204
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):13-20
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):65-69
71. Goldring SR, Gravallese EM (2004) Bisphosphonates: environmental protection for the joint? Arthritis Rheum 50(7):2044-2047
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 1068:543-556
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):732-738
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):1410-1414
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):623-633
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):2327-2337
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):1299-1309
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):537-544
79. Ferrari-Lacraz S, Ferrari S (2011) Do RANKL inhibitors (denosumab) affect inflammation and immunity? Osteoporos Int 22(2):435-446
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):2028-2039
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):3346-3355
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):543-555
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):404-414
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):120-127
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):1583-1587
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):997-1002
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):2556-2561
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):1353-1362
89. Geyer M, Müller-Ladner U (2010) Actual status of antiinterleukin-1 therapies in rheumatic diseases. Curr Opin Rheumatol 22(3):246-251
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):1580-1584
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):2572-2581
92. Schiff M, Bessette L (2010) Evaluation of abatacept in biologic-naïve patients with active rheumatoid arthritis. Clin Rheumatol 29(6):583-591