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Osteoporosis International

, Volume 28, Issue 10, pp 2801–2812 | Cite as

Skeletal complications of rheumatoid arthritis

  • L. Heinlen
  • M. B. Humphrey
Review

Abstract

Rheumatoid arthritis (RA) is associated with local and systemic inflammation that induces many changes in the skeletal health. Locally, periarticular bone loss and juxta-articular bone erosions may occur while joint ankylosis, generalized bone loss, osteoporosis, and fractures may develop secondary to inflammation. The aim of this narrative review is to summarize the clinical evidence for abnormal skeletal health in RA, the effects of disease modifying anti-rheumatic drugs (DMARDS) on bone health, and the effects of drugs for the prevention or treatment of osteoporosis in the RA population.

Keywords

Ankylosis Bone erosions Bone fracture Osteoporosis Rheumatoid arthritis 

Abbreviations

ACPA

Anti-citrullinated protein antibodies

BMD

Bone mineral density

BMI

Body mass index

CI

95% confidence intervals

CT

Computerized tomography

DMARDS

Disease modifying anti-rheumatic drugs

DKK-1

Dickkopf-related protein 1

FRAX

Fracture risk assessment tool

GC

Glucocorticoids

MRI

Magnetic resonance imaging

OR

Odds ratio

RA

Rheumatoid arthritis

RANKL

Receptor activator of NF-kB ligand

RF

Rheumatoid factor

RR

Relative risk

TNFα

Tumor necrosis factor alpha

TKR

Total knee replacement

THR

Total hip replacement

Notes

Compliance with ethical standards

Conflict of interest

None.

References

  1. 1.
    Bellucci E, Terenzi R, La Paglia GM, Gentileschi S, Tripoli A, Tani C et al (2016) One year in review 2016: pathogenesis of rheumatoid arthritis. Clin Exp Rheumatol 34(5):793–801PubMedGoogle Scholar
  2. 2.
    Veale DJ, Orr C, Fearon U (2017) Cellular and molecular perspectives in rheumatoid arthritis. Semin Immunopathol 39:343–354PubMedCrossRefGoogle Scholar
  3. 3.
    Schett G, Gravallese E (2012) Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment. Nat Rev Rheumatol 8(11):656–664PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Machold KP, Stamm TA, Nell VP, Pflugbeil S, Aletaha D, Steiner G et al (2007) Very recent onset rheumatoid arthritis: clinical and serological patient characteristics associated with radiographic progression over the first years of disease. Rheumatology (Oxford, England) 46(2):342–349CrossRefGoogle Scholar
  5. 5.
    Koga T, Okada A, Fukuda T, Hidaka T, Ishii T, Ueki Y et al (2017) Anti-citrullinated peptide antibodies are the strongest predictor of clinically relevant radiographic progression in rheumatoid arthritis patients achieving remission or low disease activity: a post hoc analysis of a nationwide cohort in Japan. PLoS One 12(5):e0175281PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kroot EJ, de Jong BA, van Leeuwen MA, Swinkels H, van den Hoogen FH, van't Hof M et al (2000) The prognostic value of anti-cyclic citrullinated peptide antibody in patients with recent-onset rheumatoid arthritis. Arthritis Rheum 43(8):1831–1835PubMedCrossRefGoogle Scholar
  7. 7.
    Carpenter L, Norton S, Nikiphorou E, Jayakumar K, McWilliams DF, Rennie KL et al (2017) Reductions in radiographic progression in early RA over 25-years: changing contribution from RF in 2 multi-centre UK inception cohorts. Arthritis Care Res (Hoboken). doi: 10.1002/acr.23217
  8. 8.
    Kumar S, Pangtey G, Gupta R, Rehan HS, Gupta LK (2017) Assessment of anti-CarP antibodies, disease activity and quality of life in rheumatoid arthritis patients on conventional and biological disease-modifying antirheumatic drugs. Reumatologia 55(1):4–9PubMedPubMedCentralGoogle Scholar
  9. 9.
    Saevarsdottir S, Rezaei H, Geborek P, Petersson I, Ernestam S, Albertsson K et al (2015) Current smoking status is a strong predictor of radiographic progression in early rheumatoid arthritis: results from the SWEFOT trial. Ann Rheum Dis 74(8):1509–1514PubMedCrossRefGoogle Scholar
  10. 10.
    Fisher BA, Bang SY, Chowdhury M, Lee HS, Kim JH, Charles P et al (2014) Smoking, the HLA-DRB1 shared epitope and ACPA fine-specificity in Koreans with rheumatoid arthritis: evidence for more than one pathogenic pathway linking smoking to disease. Ann Rheum Dis 73(4):741–747PubMedCrossRefGoogle Scholar
  11. 11.
    Ciubotariu E, Gabay C, Finckh A (2014) Joint damage progression in patients with rheumatoid arthritis in clinical remission: do biologics perform better than synthetic antirheumatic drugs? J Rheumatol 41(8):1576–1582PubMedCrossRefGoogle Scholar
  12. 12.
    Martel W, Hayes JT, Duff IF (1965) The pattern of bone erosion in the hand and wrist in rheumatoid arthritis. Radiology 84:204–214PubMedCrossRefGoogle Scholar
  13. 13.
    McGonagle D, Tan AL, Moller Dohn U, Ostergaard M, Benjamin M (2009) Microanatomic studies to define predictive factors for the topography of periarticular erosion formation in inflammatory arthritis. Arthritis Rheum 60(4):1042–1051PubMedCrossRefGoogle Scholar
  14. 14.
    Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D et al (2007) Dickkopf-1 is a master regulator of joint remodeling. Nat Med 13(2):156–163PubMedCrossRefGoogle Scholar
  15. 15.
    Seror R, Boudaoud S, Pavy S, Nocturne G, Schaeverbeke T, Saraux A et al (2016) Increased Dickkopf-1 in recent-onset rheumatoid arthritis is a new biomarker of structural severity. Data from the ESPOIR Cohort. Sci Rep 6:18421PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Sen M, Lauterbach K, El-Gabalawy H, Firestein GS, Corr M, Carson DA (2000) Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci U S A 97(6):2791–2796PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Miao CG, Yang YY, He X, Li XF, Huang C, Huang Y et al (2013) Wnt signaling pathway in rheumatoid arthritis, with special emphasis on the different roles in synovial inflammation and bone remodeling. Cell Signal 25(10):2069–2078PubMedCrossRefGoogle Scholar
  18. 18.
    Ideguchi H, Ohno S, Hattori H, Senuma A, Ishigatsubo Y (2006) Bone erosions in rheumatoid arthritis can be repaired through reduction in disease activity with conventional disease-modifying antirheumatic drugs. Arthritis Res Ther 8(3):R76PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Sharp JT, Van Der Heijde D, Boers M, Boonen A, Bruynesteyn K, Emery P et al (2003) Repair of erosions in rheumatoid arthritis does occur. Results from 2 studies by the OMERACT subcommittee on healing of erosions. J Rheumatol 30(5):1102–1107PubMedGoogle Scholar
  20. 20.
    Barbieri F, Zampogna G, Camellino D, Paparo F, Cutolo M, Garlaschi G et al (2016) Ankylosis of the wrist bones in patients with rheumatoid arthritis: a study with extremity-dedicated MRI. Clin Exp Rheumatol 34(1):49–52PubMedGoogle Scholar
  21. 21.
    Leden I, Theander J, Svensson B (2008) Small joint ankylosis in rheumatoid arthritis: a vanishing phenomenon or a pathogenetic clue, or both? Ann Rheum Dis 67(12):1786–1787PubMedCrossRefGoogle Scholar
  22. 22.
    Eulderink F, Meijers KA (1976) Pathology of the cervical spine in rheumatoid arthritis: a controlled study of 44 spines. J Pathol 120(2):91–108PubMedCrossRefGoogle Scholar
  23. 23.
    Gillick JL, Wainwright J, Das K (2015) Rheumatoid arthritis and the cervical spine: a review on the role of surgery. Int J Rheumatol 2015:252456PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Iizuka H, Iizuka Y, Okamura K, Yonemoto Y, Mieda T, Takagishi K (2016) Bony ankylosis of the facet joint of the cervical spine in rheumatoid arthritis: its characteristics and relationship to the clinical findings. Mod Rheumatol:1–5Google Scholar
  25. 25.
    Zhu S, Xu W, Luo Y, Zhao Y, Liu Y (2017) Cervical spine involvement risk factors in rheumatoid arthritis: a meta-analysis. Int J Rheum Dis 20:541–549PubMedCrossRefGoogle Scholar
  26. 26.
    van Staa TP, Geusens P, Bijlsma JW, Leufkens HG, Cooper C (2006) Clinical assessment of the long-term risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum 54(10):3104–3112PubMedCrossRefGoogle Scholar
  27. 27.
    Brennan SL, Toomey L, Kotowicz MA, Henry MJ, Griffiths H, Pasco JA (2014) Rheumatoid arthritis and incident fracture in women: a case-control study. BMC Musculoskelet Disord 15:13PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Chen B, Cheng G, Wang H, Feng Y (2016) Increased risk of vertebral fracture in patients with rheumatoid arthritis: a meta-analysis. Medicine (Baltimore) 95(45):e5262CrossRefGoogle Scholar
  29. 29.
    Ghazi M, Kolta S, Briot K, Fechtenbaum J, Paternotte S, Roux C (2012) Prevalence of vertebral fractures in patients with rheumatoid arthritis: revisiting the role of glucocorticoids. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 23(2):581–587CrossRefGoogle Scholar
  30. 30.
    Amin S, Gabriel SE, Achenbach SJ, Atkinson EJ, Melton LJ 3rd (2013) Are young women and men with rheumatoid arthritis at risk for fragility fractures? A population-based study. J Rheumatol 40(10):1669–1676PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Wright NC, Lisse JR, Walitt BT, Eaton CB, Chen Z (2011) Women’s Health Initiative I. Arthritis increases the risk for fractures—results from the Women’s Health Initiative. J Rheumatol 38(8):1680–1688PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Acurcio FA, Moura CS, Bernatsky S, Bessette L, Rahme E (2016) Opioid use and risk of nonvertebral fractures in adults with rheumatoid arthritis: a nested case-control study using administrative databases. Arthritis Rheumatol 68(1):83–91PubMedCrossRefGoogle Scholar
  33. 33.
    Klop C, de Vries F, Bijlsma JW, Leufkens HG, Welsing PM (2016) Predicting the 10-year risk of hip and major osteoporotic fracture in rheumatoid arthritis and in the general population: an independent validation and update of UK FRAX without bone mineral density. Ann Rheum Dis 75(12):2095–2100PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Van Staa TP, Laan RF, Barton IP, Cohen S, Reid DM, Cooper C (2003) Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 48(11):3224–3229PubMedCrossRefGoogle Scholar
  35. 35.
    Haugeberg G, Uhlig T, Falch 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 County rheumatoid arthritis register. Arthritis Rheum 43(3):522–530PubMedCrossRefGoogle Scholar
  36. 36.
    Sinigaglia L, Nervetti A, Mela Q, Bianchi G, Del Puente A, Di Munno O et al (2000) A multicenter cross sectional study on bone mineral density in rheumatoid arthritis. Italian study group on bone mass in rheumatoid arthritis. J Rheumatol 27(11):2582–2589PubMedGoogle Scholar
  37. 37.
    Hauser B, Riches PL, Wilson JF, Horne AE, Ralston SH (2014) Prevalence and clinical prediction of osteoporosis in a contemporary cohort of patients with rheumatoid arthritis. Rheumatology (Oxford, England) 53(10):1759–1766CrossRefGoogle Scholar
  38. 38.
    Lane NE, Pressman AR, Star VL, Cummings SR, Nevitt MC (1995) Rheumatoid arthritis and bone mineral density in elderly women. The study of osteoporotic fractures research group. J Bone Miner Res 10(2):257–263PubMedCrossRefGoogle Scholar
  39. 39.
    Gough AK, Lilley J, Eyre S, Holder RL, Emery P (1994) Generalised bone loss in patients with early rheumatoid arthritis. Lancet 344(8914):23–27PubMedCrossRefGoogle Scholar
  40. 40.
    Als OS, Gotfredsen A, Riis BJ, Christiansen C (1985) Are disease duration and degree of functional impairment determinants of bone loss in rheumatoid arthritis? Ann Rheum Dis 44(6):406–411PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Sambrook PN, Ansell BM, Foster S, Gumpel JM, Hesp R, Reeve J (1985) Bone turnover in early rheumatoid arthritis 2. Longitudinal bone density studies. Ann Rheum Dis 44(9):580–584PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Sambrook PN, Eisman JA, Champion GD, Yeates MG, Pocock NA, Eberl S (1987) Determinants of axial bone loss in rheumatoid arthritis. Arthritis Rheum 30(7):721–728PubMedCrossRefGoogle Scholar
  43. 43.
    Guler-Yuksel M, Bijsterbosch J, Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Ronday HK, Peeters AJ et al (2007) Bone mineral density in patients with recently diagnosed, active rheumatoid arthritis. Ann Rheum Dis 66(11):1508–1512PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Hwang J, Lee EK, Ahn JK, Cha HS, Koh EM, Lee J (2017) Bone-density testing interval and transition to osteoporosis in patients with rheumatoid arthritis. Osteoporos Int 28(1):231–237Google Scholar
  45. 45.
    McInnes IB, Schett G (2007) Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol 7(6):429–442PubMedCrossRefGoogle Scholar
  46. 46.
    Walsh NC, Reinwald S, Manning CA, Condon KW, Iwata K, Burr DB et al (2009) Osteoblast function is compromised at sites of focal bone erosion in inflammatory arthritis. J Bone Miner Res 24(9):1572–1585PubMedCrossRefGoogle Scholar
  47. 47.
    Zerbini CAF, Clark P, Mendez-Sanchez L, Pereira RMR, Messina OD, Uña CR, Adachi JD, Lems WF, Cooper C, Lane NE (2017) IOF Chronic Inflammation and Bone Structure (CIBS) Working Group. Biologic therapies and bone loss in rheumatoid arthritis. Osteoporos Int 28(2):429-446. doi: 10.1007/s00198-016-3769-2
  48. 48.
    Deodhar AA, Woolf AD (1996) Bone mass measurement and bone metabolism in rheumatoid arthritis: a review. Br J Rheumatol 35(4):309–322PubMedCrossRefGoogle Scholar
  49. 49.
    Di Franco M, Barchetta I, Iannuccelli C, Gerardi MC, Frisenda S, Ceccarelli F et al (2015) Hypovitaminosis D in recent onset rheumatoid arthritis is predictive of reduced response to treatment and increased disease activity: a 12 month follow-up study. BMC Musculoskelet Disord 16:53PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Raczkiewicz A, Kisiel B, Kulig M, Tlustochowicz W (2015) Vitamin D status and its association with quality of life, physical activity, and disease activity in rheumatoid arthritis patients. J Clin Rheumatol Pract Rep Rheum Musculoskeletal Dis 21(3):126–130Google Scholar
  51. 51.
    Bugatti S, Bogliolo L, Vitolo B, Manzo A, Montecucco C, Caporali R (2016) Anti-citrullinated protein antibodies and high levels of rheumatoid factor are associated with systemic bone loss in patients with early untreated rheumatoid arthritis. Arthritis Res Ther 18(1):226PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Kleyer A, Finzel S, Rech J, Manger B, Krieter M, Faustini F et al (2014) Bone loss before the clinical onset of rheumatoid arthritis in subjects with anticitrullinated protein antibodies. Ann Rheum Dis 73(5):854–860PubMedCrossRefGoogle Scholar
  53. 53.
    Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E et al (2012) Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 122(5):1791–1802PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Giles JT, Ling SM, Ferrucci L, Bartlett SJ, Andersen RE, Towns M et al (2008) Abnormal body composition phenotypes in older rheumatoid arthritis patients: association with disease characteristics and pharmacotherapies. Arthritis Rheum 59(6):807–815PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Ngeuleu A, Allali F, Medrare L, Madhi A, Rkain H, Hajjaj-Hassouni N (2017) Sarcopenia in rheumatoid arthritis: prevalence, influence of disease activity and associated factors. Rheumatol Int 37(6):1015–1020PubMedCrossRefGoogle Scholar
  56. 56.
    Okano T, Inui K, Tada M, Sugioka Y, Mamoto K, Wakitani S et al (2017) High frequency of vertebral fracture and low bone quality in patients with rheumatoid arthritis—results from TOMORROW study. Mod Rheumatol 27(3):398–404PubMedCrossRefGoogle Scholar
  57. 57.
    El Maghraoui A, Sadni S, Rezqi A, Bezza A, Achemlal L, Mounach A (2015) Does rheumatoid cachexia predispose patients with rheumatoid arthritis to osteoporosis and vertebral fractures? J Rheumatol 42(9):1556–1562PubMedCrossRefGoogle Scholar
  58. 58.
    Rodriguez JA, Saddler S, Edelman S, Ranawat CS (1996) Long-term results of total knee arthroplasty in class 3 and 4 rheumatoid arthritis. J Arthroplast 11(2):141–145CrossRefGoogle Scholar
  59. 59.
    Ethgen O, Bruyere O, Richy F, Dardennes C, Reginster JY (2004) Health-related quality of life in total hip and total knee arthroplasty. A qualitative and systematic review of the literature. J Bone Joint Surg Am 86-A(5):963–974PubMedCrossRefGoogle Scholar
  60. 60.
    Schrama JC, Espehaug B, Hallan G, Engesaeter LB, Furnes O, Havelin LI et al (2010) Risk of revision for infection in primary total hip and knee arthroplasty in patients with rheumatoid arthritis compared with osteoarthritis: a prospective, population-based study on 108,786 hip and knee joint arthroplasties from the Norwegian arthroplasty register. Arthritis Care Res (Hoboken). 62(4):473–479PubMedCrossRefGoogle Scholar
  61. 61.
    Ravi B, Escott B, Shah PS, Jenkinson R, Chahal J, Bogoch E et al (2012) A systematic review and meta-analysis comparing complications following total joint arthroplasty for rheumatoid arthritis versus for osteoarthritis. Arthritis Rheum 64(12):3839–3849PubMedCrossRefGoogle Scholar
  62. 62.
    Jamsen E, Virta LJ, Hakala M, Kauppi MJ, Malmivaara A, Lehto MU (2013) The decline in joint replacement surgery in rheumatoid arthritis is associated with a concomitant increase in the intensity of anti-rheumatic therapy: a nationwide register-based study from 1995 through 2010. Acta Orthop 84(4):331–337PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Moura CS, Abrahamowicz M, Beauchamp ME, Lacaille D, Wang Y, Boire G et al (2015) Early medication use in new-onset rheumatoid arthritis may delay joint replacement: results of a large population-based study. Arthritis Res Ther 17:197PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Asai S, Kojima T, Oguchi T, Kaneko A, Hirano Y, Yabe Y et al (2015) Effects of concomitant methotrexate on large joint replacement in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitors: a multicenter retrospective cohort study in Japan. Arthritis Care Res (Hoboken) 67(10):1363–1370CrossRefGoogle Scholar
  65. 65.
    Lescaille G, Coudert AE, Baaroun V, Javelot MJ, Cohen-Solal M, Berdal A et al (2013) Osteonecrosis of the jaw and nonmalignant disease: is there an association with rheumatoid arthritis? J Rheumatol 40(6):781–786PubMedCrossRefGoogle Scholar
  66. 66.
    Conte-Neto N, Bastos AS, Spolidorio LC, Marcantonio RA, Marcantonio E Jr (2011) Oral bisphosphonate-related osteonecrosis of the jaws in rheumatoid arthritis patients: a critical discussion and two case reports. Head Face Med 7:7PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Di Fede O, Bedogni A, Giancola F, Saia G, Bettini G, Toia F et al (2016) BRONJ in patients with rheumatoid arthritis: a multicenter case series. Oral Dis 22(6):543–548PubMedCrossRefGoogle Scholar
  68. 68.
    Furuya T, Maeda S, Momohara S, Taniguchi A, Yamanaka H (2017) Dental treatments, tooth extractions, and osteonecrosis of the jaw in Japanese patients with rheumatoid arthritis: results from the IORRA cohort study. J Bone Miner Metab 35(3):344–350PubMedCrossRefGoogle Scholar
  69. 69.
    Barreira SC, Fonseca JE (2016) The impact of conventional and biological disease modifying antirheumatic drugs on bone biology. Rheumatoid arthritis as a case study. Clin Rev Allergy Immunol 51(1):100–109PubMedCrossRefGoogle Scholar
  70. 70.
    Rexhepi S, Rexhepi M, Sahatciu-Meka V, Mahmutaj V, Boshnjaku S (2016) The Impact of Low-Dose Diseasemodifying Anti-rheumatics Drugs (DMARDs) on Bone Mineral Density of Premenopausal Women in Early Rheumatoid Arthritis. Med Arch. 70(2):101–103PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    di Munno O, Mazzantini M, Sinigaglia L, Bianchi G, Minisola G, Muratore M et al (2004) Effect of low dose methotrexate on bone density in women with rheumatoid arthritis: results from a multicenter cross-sectional study. J Rheumatol. 31(7):1305–1309PubMedGoogle Scholar
  72. 72.
    Ornbjerg LM, Ostergaard M, Jensen T, Horslev-Petersen K, Stengaard-Pedersen K, Junker P et al (2017) Hand bone loss in early rheumatoid arthritis during a methotrexate-based treat-to-target strategy with or without adalimumab-a substudy of the optimized treatment algorithm in early RA (OPERA) trial. Clin Rheumatol. 36(4):781–789PubMedCrossRefGoogle Scholar
  73. 73.
    Pfeil A, Lippold J, Eidner T, Lehmann G, Oelzner P, Renz DM et al (2009) Effects of leflunomide and methotrexate in rheumatoid arthritis detected by digital X-ray radiogrammetry and computer-aided joint space analysis. Rheumatol Int. 29(3):287–295PubMedCrossRefGoogle Scholar
  74. 74.
    Vis M, Havaardsholm EA, Haugeberg G, Uhlig T, Voskuyl AE, van de Stadt RJ 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(11):1495–1499PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Guler-Yuksel M, Allaart CF, Goekoop-Ruiterman YP, de Vries-Bouwstra JK, van Groenendael JH, Mallee C et al (2009) Changes in hand and generalised bone mineral density in patients with recent-onset rheumatoid arthritis. Ann Rheum Dis. 68(3):330–336PubMedCrossRefGoogle Scholar
  76. 76.
    Siu S, Haraoui B, Bissonnette R, Bessette L, Roubille C, Richer V et al (2015) Meta-analysis of tumor necrosis factor inhibitors and glucocorticoids on bone density in rheumatoid arthritis and ankylosing spondylitis trials. Arthritis Care Res (Hoboken). 67(6):754–764PubMedCrossRefGoogle Scholar
  77. 77.
    Eekman DA, Vis M, Bultink IE, Kuik DJ, Voskuyl AE, Dijkmans BA et al (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):389–390PubMedCrossRefGoogle Scholar
  78. 78.
    Marotte H, Miossec P (2008) Prevention of bone mineral density loss in patients with rheumatoid arthritis treated with anti-TNFalpha therapy. Biologics : targets & therapy. 2(4):663–669Google Scholar
  79. 79.
    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. 1069:420–427PubMedCrossRefGoogle Scholar
  80. 80.
    Briot K, Rouanet S, Schaeverbeke T, Etchepare F, Gaudin P, Perdriger A et al (2015) The effect of tocilizumab on bone mineral density, serum levels of Dickkopf-1 and bone remodeling markers in patients with rheumatoid arthritis. Joint Bone Spine. 82(2):109–115PubMedCrossRefGoogle Scholar
  81. 81.
    Kume K, Amano K, Yamada S, Kanazawa T, Ohta H, Hatta K et al (2014) The effect of tocilizumab on bone mineral density in patients with methotrexate-resistant active rheumatoid arthritis. Rheumatology (Oxford, England) 53(5):900–903CrossRefGoogle Scholar
  82. 82.
    Hein G, Eidner T, Oelzner P, Rose M, Wilke A, Wolf G et al (2011) Influence of Rituximab on markers of bone remodeling in patients with rheumatoid arthritis: a prospective open-label pilot study. Rheumatol Int. 31(2):269–272PubMedCrossRefGoogle Scholar
  83. 83.
    Boumans MJ, Thurlings RM, Yeo L, Scheel-Toellner D, Vos K, Gerlag DM et al (2012) Rituximab abrogates joint destruction in rheumatoid arthritis by inhibiting osteoclastogenesis. Ann Rheum Dis. 71(1):108–113PubMedCrossRefGoogle Scholar
  84. 84.
    Coulson KA, Reed G, Gilliam BE, Kremer JM, Pepmueller PH (2009) Factors influencing fracture risk, T score, and management of osteoporosis in patients with rheumatoid arthritis in the Consortium of Rheumatology Researchers of North America (CORRONA) registry. J Clin Rheumatol. 15(4):155–160PubMedCrossRefGoogle Scholar
  85. 85.
    Roussy JP, Bessette L, Bernatsky S, Rahme E, Lachaine J (2013) Biologic disease-modifying antirheumatic drugs and the risk of non-vertebral osteoporotic fractures in patients with rheumatoid arthritis aged 50 years and over. Osteoporos Int. 24(9):2483–2492PubMedCrossRefGoogle Scholar
  86. 86.
    Moller Dohn U, Boonen A, Hetland ML, Hansen MS, Knudsen LS, Hansen A et al (2009) Erosive progression is minimal, but erosion healing rare, in patients with rheumatoid arthritis treated with adalimumab. A 1 year investigator-initiated follow-up study using high-resolution computed tomography as the primary outcome measure. Ann Rheum Dis 68(10):1585–1590PubMedCrossRefGoogle Scholar
  87. 87.
    Gravallese EM, Walsh NC (2011) Rheumatoid arthritis: repair of erosion in RA—shifting the balance to formation. Nat Rev Rheumatol 7(11):626–628PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Ramirez J, Narvaez JA, Ruiz-Esquide V, Hernandez-Ganan J, Cuervo A, Inciarte-Mundo J et al (2017) Clinical and sonographic biomarkers of structural damage progression in RA patients in clinical remission: a prospective study with 12 months follow-up. Semin Arthritis Rheum. doi: 10.1016/j.semarthrit.2017.04.007
  89. 89.
    Lisbona MP, Pamies A, Ares J, Almirall M, Navallas M, Solano A et al (2014) Association of bone edema with the progression of bone erosions quantified by hand magnetic resonance imaging in patients with rheumatoid arthritis in remission. J Rheumatol 41(8):1623–1629PubMedCrossRefGoogle Scholar
  90. 90.
    Kirwan JR, Bijlsma JW, Boers M, Shea BJ (2007) Effects of glucocorticoids on radiological progression in rheumatoid arthritis. Cochrane Database Syst Rev 24(1):Cd006356Google Scholar
  91. 91.
    van Staa TP, Leufkens HG, Cooper C (2002) The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporosis Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 13(10):777–787CrossRefGoogle Scholar
  92. 92.
    Guler-Yuksel M, Bijsterbosch J, Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Hulsmans HM, de Beus WM et al (2008) Changes in bone mineral density in patients with recent onset, active rheumatoid arthritis. Ann Rheum Dis 67(6):823–828PubMedCrossRefGoogle Scholar
  93. 93.
    van der Goes MC, Jacobs JW, Jurgens MS, Bakker MF, van der Veen MJ, van der Werf JH et al (2013) Are changes in bone mineral density different between groups of early rheumatoid arthritis patients treated according to a tight control strategy with or without prednisone if osteoporosis prophylaxis is applied? Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 24(4):1429–1436CrossRefGoogle Scholar
  94. 94.
    Buckley L, Guyatt G, Fink HA, Cannon M, Grossman J, Hansen KE et al (2017) American College of Rheumatology Guideline for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Rheumatol. doi: 10.1002/acr.23279
  95. 95.
    Panday K, Gona A, Humphrey MB (2014) Medication-induced osteoporosis: screening and treatment strategies. Ther Adv Musculoskelet Dis 6(5):185–202PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Watt J, Thompson A, Le Riche N, Pope J (2014) There is still a care gap in osteoporosis management for patients with rheumatoid arthritis. Joint Bone Spine 81(4):347–351PubMedCrossRefGoogle Scholar
  97. 97.
    Ebina K, Noguchi T, Hirao M, Hashimoto J, Kaneshiro S, Yukioka M et al (2016) Effects of switching weekly alendronate or risedronate to monthly minodronate in patients with rheumatoid arthritis: a 12-month prospective study. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 27(1):351–359CrossRefGoogle Scholar
  98. 98.
    Shin K, Park SH, Park W, Baek HJ, Lee YJ, Kang SW et al (2017) Monthly oral ibandronate reduces bone loss in Korean women with rheumatoid arthritis and osteopenia receiving long-term glucocorticoids: a 48-week double-blinded randomized placebo-controlled investigator-initiated trial. Clin Ther 39(2):268–278 e2PubMedCrossRefGoogle Scholar
  99. 99.
    Lems WF, Lodder MC, Lips P, Bijlsma JW, Geusens P, Schrameijer N et al (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 J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 17(5):716–723CrossRefGoogle Scholar
  100. 100.
    Tada M, Inui K, Sugioka Y, Mamoto K, Okano T, Anno S et al (2017) Use of bisphosphonate might be important to improve bone mineral density in patients with rheumatoid arthritis even under tight control: the TOMORROW study. Rheumatol Int 37(6):999–1005PubMedCrossRefGoogle Scholar
  101. 101.
    Wen L, Kang JH, Yim YR, Lee JW, Lee KE, Park DJ et al (2016) Risk factors for treatment failure in osteoporotic patients with rheumatoid arthritis. Mod Rheumatol 26(2):194–199PubMedGoogle Scholar
  102. 102.
    Takayanagi H (2007) Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 7(4):292–304PubMedCrossRefGoogle Scholar
  103. 103.
    Nakamura Y, Suzuki T, Yoshida T, Yamazaki H, Kato H. (2017) Vitamin D and Calcium are required during denosumab treatment in osteoporosis with rheumatoid arthritis. Nutrients 9(5)Google Scholar
  104. 104.
    Takeuchi T, Tanaka Y, Ishiguro N, Yamanaka H, Yoneda T, Ohira T et al (2016) Effect of denosumab on Japanese patients with rheumatoid arthritis: a dose-response study of AMG 162 (denosumab) in patients with rheumatoid arthritis on methotrexate to validate inhibitory effect on bone erosion (DRIVE)-a 12-month, multicentre, randomised, double-blind, placebo-controlled, phase II clinical trial. Ann Rheum Dis 75(6):983–990PubMedCrossRefGoogle Scholar
  105. 105.
    Kinoshita H, Miyakoshi N, Kashiwagura T, Kasukawa Y, Sugimura Y, Shimada Y (2016) Comparison of the efficacy of denosumab and bisphosphonates for treating secondary osteoporosis in patients with rheumatoid arthritis. Mod Rheumatol 23:1–5Google Scholar
  106. 106.
    Yue J, Griffith JF, Xiao F, Shi L, Wang D, Shen J et al (2016) Repair of bone erosion in rheumatoid arthritis by denosumab: a high-resolution peripheral quantitative computed tomography study. Arthritis Care Res (Hoboken). doi: 10.1002/acr.23133
  107. 107.
    Curtis JR, Xie F, Yun H, Saag KG, Chen L, Delzell E (2015) Risk of hospitalized infection among rheumatoid arthritis patients concurrently treated with a biologic agent and denosumab. Arthritis Rheumatol 67(6):1456–1464PubMedCrossRefGoogle Scholar
  108. 108.
    Ebina K, Hashimoto J, Shi K, Kashii M, Hirao M, Yoshikawa H (2014) Comparison of the effect of 18-month daily teriparatide administration on patients with rheumatoid arthritis and postmenopausal osteoporosis patients. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 25(12):2755–2765CrossRefGoogle Scholar
  109. 109.
    Solomon DH, Kay J, Duryea J, Lu B, Bolster MB, Yood RA et al (2017) Effects of teriparatide on joint erosions in rheumatoid arthritis: a randomized controlled trial. Arthritis RheumatolGoogle Scholar
  110. 110.
    Kanis JA, Johansson H, Oden A, McCloskey EV (2011) Guidance for the adjustment of FRAX according to the dose of glucocorticoids. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 22(3):809–816CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2017

Authors and Affiliations

  1. 1.University of Oklahoma Health Sciences CenterOklahoma CityUSA
  2. 2.Veterans Affairs Medical CenterOklahoma CityUSA

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