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Osteoporosis Pathophysiology, Epidemiology, and Screening in Rheumatoid Arthritis

  • Rheumatoid Arthritis (L Moreland, Section Editor)
  • Published:
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Abstract

Purpose of Review

To review the burden of osteoporosis (OP) in rheumatoid arthritis (RA) and to describe the OP screening strategies applied in RA.

Recent Findings

RA is an inflammatory condition that predisposes patients to development of OP. OP in RA has a multifactorial pathogenesis with systemic inflammation and glucocorticoid use playing major roles. Newer studies have reported an intriguing association between RA autoantibodies and the development of OP. OP screening strategies in RA patients include clinical and vitamin D assessment, biochemical markers of bone remodeling, and bone imaging evaluations, particularly dual-energy X-ray absorptiometry (DXA).

Summary

Fragility fractures are an important comorbidity of RA. OP screening strategies are both feasible and effective in RA patients and recommended by most specialty organizations. Given the considerable exposure to factors related to OP development, such as pro-inflammatory cytokines and glucocorticoid treatment, special attention should be directed to biochemical and DXA results in RA patients.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365:2205–19.

    CAS  PubMed  Google Scholar 

  2. Zhu TY, Griffith JF, Qin L, Hung VW, Fong T-N, Au S-K, et al. Alterations of bone density, microstructure, and strength of the distal radius in male patients with rheumatoid arthritis: a case-control study with HR-pQCT. J Bone Miner Res Off J Am Soc Bone Miner Res. 2014;29:2118–29.

    CAS  Google Scholar 

  3. Stach CM, Bäuerle M, Englbrecht M, Kronke G, Engelke K, Manger B, et al. Periarticular bone structure in rheumatoid arthritis patients and healthy individuals assessed by high-resolution computed tomography. Arthritis Rheum. 2010;62:330–9.

    PubMed  Google Scholar 

  4. Ziegelasch M, Forslind K, Skogh T, Riklund K, Kastbom A, Berglin E. Decrease in bone mineral density during three months after diagnosis of early rheumatoid arthritis measured by digital X-ray radiogrammetry predicts radiographic joint damage after one year. Arthritis Res Ther. 2017;19:195.

    PubMed  PubMed Central  Google Scholar 

  5. Nieuwenhuis WP, van Steenbergen HW, Stomp W, Stijnen T, Huizinga TWJ, Bloem JL, et al. The course of bone marrow edema in early undifferentiated arthritis and rheumatoid arthritis: a longitudinal magnetic resonance imaging study at bone level. Arthritis Rheumatol Hoboken NJ. 2016;68:1080–8.

    Google Scholar 

  6. Black RJ, Spargo L, Schultz C, Chatterton B, Cleland L, Lester S, et al. Decline in hand bone mineral density indicates increased risk of erosive change in early rheumatoid arthritis. Arthritis Care Res. 2014;66:515–22.

    CAS  Google Scholar 

  7. Mangnus L, van Steenbergen HW, Reijnierse M, Kälvesten J, van der Helm-Van Mil A. Bone mineral density loss in clinically suspect arthralgia is associated with subclinical inflammation and progression to clinical arthritis. Scand J Rheumatol. 2017;46:364–8.

    CAS  PubMed  Google Scholar 

  8. Kato G, Shimizu Y, Arai Y, Suzuki N, Sugamori Y, Maeda M, et al. The inhibitory effects of a RANKL-binding peptide on articular and periarticular bone loss in a murine model of collagen-induced arthritis: a bone histomorphometric study. Arthritis Res Ther. 2015;17:251.

    PubMed  PubMed Central  Google Scholar 

  9. Fessler J, Husic R, Schwetz V, Lerchbaum E, Aberer F, Fasching P, et al. Senescent T-cells promote bone loss in rheumatoid arthritis. Front Immunol. 2018;9:95.

    PubMed  PubMed Central  Google Scholar 

  10. Hecht C, Englbrecht M, Rech J, Schmidt S, Araujo E, Engelke K, et al. Additive effect of anti-citrullinated protein antibodies and rheumatoid factor on bone erosions in patients with RA. Ann Rheum Dis. 2015;74:2151–6.

    CAS  PubMed  Google Scholar 

  11. Engdahl C, Bang H, Dietel K, Lang SC, Harre U, Schett G. Periarticular bone loss in arthritis is induced by autoantibodies against citrullinated vimentin. J Bone Miner Res Off J Am Soc Bone Miner Res. 2017;32:1681–91.

    CAS  Google Scholar 

  12. Simon D, Kleyer A, Englbrecht M, Stemmler F, Simon C, Berlin A, et al. A comparative analysis of articular bone in large cohort of patients with chronic inflammatory diseases of the joints, the gut and the skin. Bone. 2018;116:87–93.

    PubMed  Google Scholar 

  13. Behrens F, Koehm M, Thaçi D, Gnann H, Greger G, Maria Wittig B, et al. Anti-citrullinated protein antibodies are linked to erosive disease in an observational study of patients with psoriatic arthritis. Rheumatol Oxf Engl. 2016;55:1791–5.

    CAS  Google Scholar 

  14. Kocijan R, Harre U, Schett G. ACPA and bone loss in rheumatoid arthritis. Curr Rheumatol Rep. 2013;15:366.

    PubMed  Google Scholar 

  15. Krishnamurthy A, Joshua V, Haj Hensvold A, Jin T, Sun M, Vivar N, et al. Identification of a novel chemokine-dependent molecular mechanism underlying rheumatoid arthritis-associated autoantibody-mediated bone loss. Ann Rheum Dis. 2016;75:721–9.

    CAS  PubMed  Google Scholar 

  16. •• Kleyer A, Finzel S, Rech J, Manger B, Krieter M, Faustini F, et al. Bone loss before the clinical onset of rheumatoid arthritis in subjects with anticitrullinated protein antibodies. Ann Rheum Dis. 2014;73:854–60. This article provides evidence on the independent activity of ACPA on bone health. The authors found that bone loss ACPA-positive patients experience bone loss even before the onset of clinical RA.

    PubMed  Google Scholar 

  17. Haugeberg G, Helgetveit KB, Førre Ø, Garen T, Sommerseth H, Prøven A. Generalized bone loss in early rheumatoid arthritis patients followed for ten years in the biologic treatment era. BMC Musculoskelet Disord. 2014;15:289.

    PubMed  PubMed Central  Google Scholar 

  18. Takayanagi H. New developments in osteoimmunology. Nat Rev Rheumatol. 2012;8:684–9.

    CAS  PubMed  Google Scholar 

  19. Hauser B, Riches PL, Gilchrist T, Visconti MR, Wilson JF, Ralston SH. Autoantibodies to osteoprotegerin are associated with increased bone resorption in rheumatoid arthritis. Ann Rheum Dis. 2015;74:1631–2.

    CAS  PubMed  Google Scholar 

  20. •• Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med. 2007;13:156–63. This important pre-clinical paper provides evidence on the crucial role of Dkk-1 in bone loss and bone erosions.

    CAS  PubMed  Google Scholar 

  21. Rossini M, Viapiana O, Adami S, Fracassi E, Idolazzi L, Dartizio C, et al. In patients with rheumatoid arthritis, Dickkopf-1 serum levels are correlated with parathyroid hormone, bone erosions and bone mineral density. Clin Exp Rheumatol. 2015;33:77–83.

    PubMed  Google Scholar 

  22. Ma Y, Zhang X, Wang M, Xia Q, Yang J, Wu M, et al. The serum level of Dickkopf-1 in patients with rheumatoid arthritis: a systematic review and meta-analysis. Int Immunopharmacol. 2018;59:227–32.

    CAS  PubMed  Google Scholar 

  23. Orsolini G, Caimmi C, Viapiana O, Idolazzi L, Fracassi E, Gatti D, et al. Titer-dependent effect of anti-citrullinated protein antibodies on systemic bone mass in rheumatoid arthritis patients. Calcif Tissue Int. 2017;101:17–23.

    CAS  PubMed  Google Scholar 

  24. Amiche MA, Abtahi S, Driessen JHM, Vestergaard P, de Vries F, Cadarette SM, et al. Impact of cumulative exposure to high-dose oral glucocorticoids on fracture risk in Denmark: a population-based case-control study. Arch Osteoporos. 2018;13:30.

    PubMed  PubMed Central  Google Scholar 

  25. Amiche MA, Albaum JM, Tadrous M, Pechlivanoglou P, Lévesque LE, Adachi JD, et al. Fracture risk in oral glucocorticoid users: a Bayesian meta-regression leveraging control arms of osteoporosis clinical trials. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2016;27:1709–18.

    CAS  Google Scholar 

  26. Balasubramanian A, Wade SW, Adler RA, Saag K, Pannacciulli N, Curtis JR. Glucocorticoid exposure and fracture risk in a cohort of US patients with selected conditions. J Bone Miner Res Off J Am Soc Bone Miner Res. 2018;33:1881–8.

    CAS  Google Scholar 

  27. • Balasubramanian A, Wade SW, Adler RA, Lin CJF, Maricic M, O’Malley CD, et al. Glucocorticoid exposure and fracture risk in patients with new-onset rheumatoid arthritis. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2016;27:3239–49. This is a cross-sectional study on fracture risk associated with glucocorticoid use in RA patients. The authors found an increased risk of fracture among young and newly diagnosed RA patients. The fracture risk was directly related to daily and cumulative dose of glucocorticoids.

    CAS  Google Scholar 

  28. Da Silva JAP, Jacobs JWG, Kirwan JR, Boers M, Saag KG, Inês LBS, et al. Safety of low dose glucocorticoid treatment in rheumatoid arthritis: published evidence and prospective trial data. Ann Rheum Dis. 2006;65:285–93.

    PubMed  Google Scholar 

  29. Sambrook PN, Eisman JA, Yeates MG, Pocock NA, Eberl S, Champion GD. Osteoporosis in rheumatoid arthritis: safety of low dose corticosteroids. Ann Rheum Dis. 1986;45:950–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Blavnsfeldt A-BG, de Thurah A, Thomsen MD, Tarp S, Langdahl B, Hauge E-M. The effect of glucocorticoids on bone mineral density in patients with rheumatoid arthritis: a systematic review and meta-analysis of randomized, controlled trials. Bone. 2018;114:172–80.

    CAS  PubMed  Google Scholar 

  31. Siu S, Haraoui B, Bissonnette R, Bessette L, Roubille C, Richer V, et al. Meta-analysis of tumor necrosis factor inhibitors and glucocorticoids on bone density in rheumatoid arthritis and ankylosing spondylitis trials. Arthritis Care Res. 2015;67:754–64.

    CAS  Google Scholar 

  32. van Staa TP, Geusens P, Bijlsma JWJ, Leufkens HGM, Cooper C. Clinical assessment of the long-term risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum. 2006;54:3104–12.

    PubMed  Google Scholar 

  33. Emkey RD, Lindsay R, Lyssy J, Weisberg JS, Dempster DW, Shen V. The systemic effect of intraarticular administration of corticosteroid on markers of bone formation and bone resorption in patients with rheumatoid arthritis. Arthritis Rheum. 1996;39:277–82.

    CAS  PubMed  Google Scholar 

  34. Cooper C, Coupland C, Mitchell M. Rheumatoid arthritis, corticosteroid therapy and hip fracture. Ann Rheum Dis. 1995;54:49–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Simon D, Kleyer A, Stemmler F, Simon C, Berlin A, Hueber AJ, et al. Age- and sex-dependent changes of intra-articular cortical and trabecular bone structure and the effects of rheumatoid arthritis. J Bone Miner Res Off J Am Soc Bone Miner Res. 2017;32:722–30.

    Google Scholar 

  36. Rossini M, Adami G, Viapiana O, Idolazzi L, Orsolini G, Fassio A, et al. Osteoporosis: an independent determinant of bone erosions in rheumatoid arthritis? J Bone Miner Res Off J Am Soc Bone Miner Res. 2017;32:2142–3.

    Google Scholar 

  37. Han MH, Ryu JI, Kim CH, Kim JM, Cheong JH, Bak KH, et al. Influence of systemic bone mineral density on atlantoaxial subluxation in patients with rheumatoid arthritis. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2017;28:1931–8.

    CAS  Google Scholar 

  38. Wilson JC, Sarsour K, Gale S, Pethö-Schramm A, Jick SS, Meier CR. Incidence and risk of glucocorticoid-associated adverse effects in patients with rheumatoid arthritis. Arthritis Care Res. 2019;71:498–511.

    CAS  Google Scholar 

  39. Mori Y, Kuwahara Y, Chiba S, Kogre A, Baba K, Kamimura M, et al. Bone mineral density of postmenopausal women with rheumatoid arthritis depends on disease duration regardless of treatment. J Bone Miner Metab. 2017;35:52–7.

    CAS  PubMed  Google Scholar 

  40. Haugeberg G, Uhlig T, Falch JA, Halse JI, Kvien TK. 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. 2000;43:522–30.

    CAS  PubMed  Google Scholar 

  41. Sinigaglia L, Nervetti A, Mela Q, Bianchi G, Del Puente A, Di Munno O, et al. A multicenter cross sectional study on bone mineral density in rheumatoid arthritis. Italian Study Group on Bone Mass in Rheumatoid Arthritis. J Rheumatol. 2000;27:2582–9.

    CAS  PubMed  Google Scholar 

  42. Hauser B, Riches PL, Wilson JF, Horne AE, Ralston SH. Prevalence and clinical prediction of osteoporosis in a contemporary cohort of patients with rheumatoid arthritis. Rheumatol Oxf Engl. 2014;53:1759–66.

    CAS  Google Scholar 

  43. Lee J-H, Sung Y-K, Choi C-B, Cho S-K, Bang S-Y, Choe J-Y, et al. The frequency of and risk factors for osteoporosis in Korean patients with rheumatoid arthritis. BMC Musculoskelet Disord. 2016;17:98.

    PubMed  PubMed Central  Google Scholar 

  44. Fassio A, Idolazzi L, Jaber MA, Dartizio C, Viapiana O, Rossini M, et al. The negative bone effects of the disease and of chronic corticosteroid treatment in premenopausal women affected by rheumatoid arthritis. Reumatismo. 2016;68:65–71.

    CAS  PubMed  Google Scholar 

  45. Kweon S-M, Sohn DH, Park J-H, Koh JH, Park E-K, Lee H-N, et al. Male patients with rheumatoid arthritis have an increased risk of osteoporosis: frequency and risk factors. Medicine (Baltimore). 2018;97:e11122.

    Google Scholar 

  46. Jin S, Hsieh E, Peng L, Yu C, Wang Y, Wu C, et al. Incidence of fractures among patients with rheumatoid arthritis: a systematic review and meta-analysis. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2018;29:1263–75.

    CAS  Google Scholar 

  47. Mazzucchelli R, Pérez Fernandez E, Crespí-Villarías N, Quirós-Donate J, García Vadillo A, Espinosa M, et al. Trends in hip fracture in patients with rheumatoid arthritis: results from the Spanish National Inpatient Registry over a 17-year period (1999-2015). TREND-AR study. RMD Open. 2018;4:e000671.

    PubMed  PubMed Central  Google Scholar 

  48. Yazdany J, Schmajuk G, Robbins M, Daikh D, Beall A, Yelin E, et al. Choosing wisely: the American College of Rheumatology’s top 5 list of things physicians and patients should question. Arthritis Care Res. 2013;65:329–39.

    Google Scholar 

  49. Dougados M, Soubrier M, Antunez A, Balint P, Balsa A, Buch MH, et al. Prevalence of comorbidities in rheumatoid arthritis and evaluation of their monitoring: results of an international, cross-sectional study (COMORA). Ann Rheum Dis. 2014;73:62–8.

    PubMed  Google Scholar 

  50. Venegas-Pont M, Davis JM, Crowson CS, Gabriel SE, Matteson EL. Frequency of radiologic procedures in patients with rheumatoid arthritis. J Clin Rheumatol Pract Rep Rheum Musculoskelet Dis. 2015;21:15–8.

    Google Scholar 

  51. Ozen G, Kamen DL, Mikuls TR, England BR, Wolfe F, Michaud K. Trends and determinants of osteoporosis treatment and screening in patients with rheumatoid arthritis compared to osteoarthritis. Arthritis Care Res. 2018;70:713–23.

    CAS  Google Scholar 

  52. Amarnath ALD, Franks P, Robbins JA, Xing G, Fenton JJ. Underuse and overuse of osteoporosis screening in a regional health system: a retrospective cohort study. J Gen Intern Med. 2015;30:1733–40.

    PubMed  PubMed Central  Google Scholar 

  53. Schmajuk G, Tonner C, Trupin L, Yazdany J. Variations in radiographic procedure use for Medicare patients with rheumatoid arthritis. Arthritis Care Res. 2017;69:642–8.

    Google Scholar 

  54. Lewiecki EM, Baim S, Siris ES. Osteoporosis care at risk in the United States. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2008;19:1505–9.

    CAS  Google Scholar 

  55. Richards JS, Cannon GW, Hayden CL, Amdur RL, Lazaro D, Mikuls TR, et al. Adherence with bisphosphonate therapy in US veterans with rheumatoid arthritis. Arthritis Care Res. 2012;64:1864–70.

    CAS  Google Scholar 

  56. Udell JA, Fischer MA, Brookhart MA, Solomon DH, Choudhry NK. Effect of the women’s health initiative on osteoporosis therapy and expenditure in Medicaid. J Bone Miner Res. 2006;21:765–71.

    PubMed  Google Scholar 

  57. Wysowski DK, Greene P. Trends in osteoporosis treatment with oral and intravenous bisphosphonates in the United States, 2002-2012. Bone. 2013;57:423–8.

    CAS  PubMed  Google Scholar 

  58. Baillet A, Gossec L, Carmona L, de Wit M, van Eijk-Hustings Y, Bertheussen H, et al. Points to consider for reporting, screening for and preventing selected comorbidities in chronic inflammatory rheumatic diseases in daily practice: a EULAR initiative. Ann Rheum Dis. 2016;75:965–73.

    PubMed  Google Scholar 

  59. 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 Hoboken NJ. 2017;69:1521–37.

    Google Scholar 

  60. Dougados M, Soubrier M, Perrodeau E, Gossec L, Fayet F, Gilson M, et al. Impact of a nurse-led programme on comorbidity management and impact of a patient self-assessment of disease activity on the management of rheumatoid arthritis: results of a prospective, multicentre, randomised, controlled trial (COMEDRA). Ann Rheum Dis. 2015;74:1725–33.

    PubMed  Google Scholar 

  61. Daïen CI, Tubery A, Beurai-Weber M, du Cailar G, Picot M-C, Jaussent A, et al. Relevance and feasibility of a systematic screening of multimorbidities in patients with chronic inflammatory rheumatic diseases. Joint Bone Spine. 2019;86:49–54.

    PubMed  Google Scholar 

  62. Kanis JA, Johnell O. Requirements for DXA for the management of osteoporosis in Europe. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2005;16:229–38.

    CAS  Google Scholar 

  63. Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E. FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2008;19:385–97.

    CAS  Google Scholar 

  64. Martineau P, Leslie WD, Johansson H, Oden A, McCloskey EV, Hans D, et al. Clinical utility of using lumbar spine trabecular bone score to adjust fracture probability: the Manitoba BMD cohort. J Bone Miner Res Off J Am Soc Bone Miner Res. 2017;32:1568–74.

    Google Scholar 

  65. Martineau P, Leslie WD, Johansson H, Harvey NC, McCloskey EV, Hans D, et al. In which patients does lumbar spine trabecular bone score (TBS) have the largest effect? Bone. 2018;113:161–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Kim D, Cho S-K, Kim JY, Choi YY, Sung Y-K. Association between trabecular bone score and risk factors for fractures in Korean female patients with rheumatoid arthritis. Mod Rheumatol. 2016;26:540–5.

    CAS  PubMed  Google Scholar 

  67. Choi YJ, Chung Y-S, Suh C-H, Jung J-Y, Kim H-A. Trabecular bone score as a supplementary tool for the discrimination of osteoporotic fractures in postmenopausal women with rheumatoid arthritis. Medicine (Baltimore). 2017;96:e8661.

    Google Scholar 

  68. Deodhar AA, Brabyn J, Jones PW, Davis MJ, Woolf AD. Measurement of hand bone mineral content by dual energy x-ray absorptiometry: development of the method, and its application in normal volunteers and in patients with rheumatoid arthritis. Ann Rheum Dis. 1994;53:685–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Alenfeld FE, Diessel E, Brezger M, Sieper J, Felsenberg D, Braun J. Detailed analyses of periarticular osteoporosis in rheumatoid arthritis. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA. 2000;11:400–7.

    CAS  Google Scholar 

  70. Ardicoglu O, Ozgocmen S, Kamanli A, Pekkutucu I. Relationship between bone mineral density and radiologic scores of hands in rheumatoid arthritis. J Clin Densitom Off J Int Soc Clin Densitom. 2001;4:263–9.

    CAS  Google Scholar 

  71. Wevers-de Boer KVC, Heimans L, Visser K, Kälvesten J, Goekoop RJ, van Oosterhout M, et al. Four-month metacarpal bone mineral density loss predicts radiological joint damage progression after 1 year in patients with early rheumatoid arthritis: exploratory analyses from the IMPROVED study. Ann Rheum Dis. 2015;74:341–6.

    CAS  PubMed  Google Scholar 

  72. Hoff M, Haugeberg G, Odegård S, Syversen S, Landewé R, van der Heijde D, et al. Cortical hand bone loss after 1 year in early rheumatoid arthritis predicts radiographic hand joint damage at 5-year and 10-year follow-up. Ann Rheum Dis. 2009;68:324–9.

    CAS  PubMed  Google Scholar 

  73. Haugeberg G, Green MJ, Quinn MA, Marzo-Ortega H, Proudman S, Karim Z, et al. Hand bone loss in early undifferentiated arthritis: evaluating bone mineral density loss before the development of rheumatoid arthritis. Ann Rheum Dis. 2006;65:736–40.

    CAS  PubMed  Google Scholar 

  74. Klop C, de Vries F, Bijlsma JWJ, Leufkens HGM, Welsing PMJ. 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. 2016;75:2095–100.

    PubMed  PubMed Central  Google Scholar 

  75. Cheng T-T, Yu S-F, Su F-M, Chen Y-C, Su BY-J, Chiu W-C, et al. Anti-CCP-positive patients with RA have a higher 10-year probability of fracture evaluated by FRAX®: a registry study of RA with osteoporosis/fracture. Arthritis Res Ther. 2018;20:16.

    PubMed  PubMed Central  Google Scholar 

  76. Bugatti S, Bogliolo L, Vitolo B, Manzo A, Montecucco C, Caporali R. 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. 2016;18:226.

    PubMed  PubMed Central  Google Scholar 

  77. Lee YH, Bae S-C. Vitamin D level in rheumatoid arthritis and its correlation with the disease activity: a meta-analysis. Clin Exp Rheumatol. 2016;34:827–33.

    PubMed  Google Scholar 

  78. Weaver CM, Alexander DD, Boushey CJ, Dawson-Hughes B, Lappe JM, LeBoff MS, et al. Calcium plus vitamin D supplementation and risk of fractures: an updated meta-analysis from the National Osteoporosis Foundation. Osteoporos Int. 2016;27:367–76.

    CAS  PubMed  Google Scholar 

  79. Brance ML, Brun LR, Lioi S, Sánchez A, Abdala M, Oliveri B. Vitamin D levels and bone mass in rheumatoid arthritis. Rheumatol Int. 2015;35:499–505.

    CAS  PubMed  Google Scholar 

  80. Hong Q, Xu J, Xu S, Lian L, Zhang M, Ding C. Associations between serum 25-hydroxyvitamin D and disease activity, inflammatory cytokines and bone loss in patients with rheumatoid arthritis. Rheumatol Oxf Engl. 2014;53:1994–2001.

    CAS  Google Scholar 

  81. Lin J, Liu J, Davies ML, Chen W. Serum vitamin D level and rheumatoid arthritis disease activity: review and meta-analysis. PLoS One. 2016;11:e0146351.

    PubMed  PubMed Central  Google Scholar 

  82. Adami G, Rossini M, Bogliolo L, Cantatore FP, Varenna M, Malavolta N, et al. An exploratory study on the role of vitamin D supplementation in improving pain and disease activity in rheumatoid arthritis. Mod Rheumatol. 2018;0:1–8.

    CAS  Google Scholar 

  83. Soubrier M, Lambert C, Combe B, Gaudin P, Thomas T, Sibilia J, et al. A randomised, double-blind, placebo-controlled study assessing the efficacy of high doses of vitamin D on functional disability in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2018;36:1056–60.

    PubMed  Google Scholar 

  84. Coiffier G, Bouvard B, Chopin F, Biver E, Funck-Brentano T, Garnero P, et al. Common bone turnover markers in rheumatoid arthritis and ankylosing spondylitis: a literature review. Joint Bone Spine. 2013;80:250–7.

    PubMed  Google Scholar 

  85. Krabben A, Knevel R, Huizinga TWJ, Cavet G, van der Helm-van Mil AH. Serum pyridinoline levels and prediction of severity of joint destruction in rheumatoid arthritis. J Rheumatol. 2013;40:1303–6.

    CAS  PubMed  Google Scholar 

  86. Garnero P, Landewé R, Boers M, Verhoeven A, Van Der Linden S, Christgau S, et al. Association of baseline levels of markers of bone and cartilage degradation with long-term progression of joint damage in patients with early rheumatoid arthritis: the COBRA study. Arthritis Rheum. 2002;46:2847–56.

    CAS  PubMed  Google Scholar 

  87. Loddenkemper K, Bohl N, Perka C, Burmester G-R, Buttgereit F. Correlation of different bone markers with bone density in patients with rheumatic diseases on glucocorticoid therapy. Rheumatol Int. 2006;26:331–6.

    CAS  PubMed  Google Scholar 

  88. Nonaka T, Nishisaka F, Fukuda K, Sohen S, Hamanishi C. Relationship between bone mineral density and urine level of NTx in rheumatoid arthritis. J Bone Miner Metab. 2005;23:314–7.

    CAS  PubMed  Google Scholar 

  89. Cortet B, Guyot MH, Solau E, Pigny P, Dumoulin F, Flipo RM, et al. Factors influencing bone loss in rheumatoid arthritis: a longitudinal study. Clin Exp Rheumatol. 2000;18:683–90.

    CAS  PubMed  Google Scholar 

  90. Adami G, Orsolini G, Adami S, Viapiana O, Idolazzi L, Gatti D, et al. Effects of TNF inhibitors on parathyroid hormone and Wnt signaling antagonists in rheumatoid arthritis. Calcif Tissue Int. 2016;99:360–4.

    CAS  PubMed  Google Scholar 

  91. Manara M, Sinigaglia L. Bone and TNF in rheumatoid arthritis: clinical implications. RMD Open. 2015;1:e000065.

    PubMed  PubMed Central  Google Scholar 

  92. Fardellone P, Séjourné A, Paccou J, Goëb V. Bone remodelling markers in rheumatoid arthritis. Mediat Inflamm. 2014;2014:484280.

    Google Scholar 

  93. Orsolini G, Adami G, Adami S, Viapiana O, Idolazzi L, Gatti D, et al. Short-term effects of TNF inhibitors on bone turnover markers and bone mineral density in rheumatoid arthritis. Calcif Tissue Int. 2016;98:580–5.

    CAS  PubMed  Google Scholar 

  94. Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, et al. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep. 2013;11:136–46.

    PubMed  PubMed Central  Google Scholar 

  95. Fouque-Aubert A, Boutroy S, Marotte H, Vilayphiou N, Bacchetta J, Miossec P, et al. Assessment of hand bone loss in rheumatoid arthritis by high-resolution peripheral quantitative CT. Ann Rheum Dis. 2010;69:1671–6.

    PubMed  Google Scholar 

  96. Barnabe C, Toepfer D, Marotte H, Hauge E-M, Scharmga A, Kocijan R, et al. Definition for rheumatoid arthritis erosions imaged with high resolution peripheral quantitative computed tomography and interreader reliability for detection and measurement. J Rheumatol. 2016;43:1935–40.

    PubMed  Google Scholar 

  97. Stemmler F, Simon D, Liphardt A-M, Englbrecht M, Rech J, Hueber AJ, et al. Biomechanical properties of bone are impaired in patients with ACPA-positive rheumatoid arthritis and associated with the occurrence of fractures. Ann Rheum Dis. 2018;77:973–80.

    CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Kenneth G. Saag.

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Giovanni Adami declares that he has no conflict of interest. Kenneth G Saag declares research grant from Amgen and Merck and consultant fee from Amgen, Lilly, Merck, Radius, and Roche.

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This article is part of the Topical Collection on Rheumatoid Arthritis

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Adami, G., Saag, K.G. Osteoporosis Pathophysiology, Epidemiology, and Screening in Rheumatoid Arthritis. Curr Rheumatol Rep 21, 34 (2019). https://doi.org/10.1007/s11926-019-0836-7

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