Calcified Tissue International

, Volume 102, Issue 5, pp 592–606 | Cite as

Glucocorticoids, Inflammation and Bone

  • Melek Güler-Yüksel
  • Jos N. Hoes
  • Irene E.M. Bultink
  • Willem F. Lems
Review

Abstract

The current review on glucocorticoids (GCs), inflammation and bone is focused on three aspects: (1) the mutual effects between GCs, inflammation and bone in inflammatory rheumatic diseases, (2) current views on fracture risk assessment in patients using GCs and (3) non-pharmacological and pharmacological treatment to prevent fractures in GC-using patients with inflammatory rheumatic diseases. The use of GCs results in increased risk for fractures due to both direct and indirect negative effects of GCs on bone mass, and on bone and muscle strength. However, also the underlying inflammatory rheumatic disease is associated with the increased bone loss and fracture risk due to the chronic inflammation itself, and due to disability/immobility caused by active disease or joint destruction. The rapid and strong anti-inflammatory effect of GCs in patients with rheumatoid arthritis seems to balance the negative effects of GCs on bone in the early, active phase of the disease. Recently, an update of the American College of Rheumatology guidelines for prevention and treatment of GC-induced osteoporosis was published with renewed recommendations. To prevent fractures, general measures, including treatment of the underlying inflammatory disease adequately (even with GCs when indicated), a healthy lifestyle, including adequate calcium and vitamin D supplementation, and regular weight bearing exercises are important. In rheumatic patients with high fracture risk using GCs, especially when the cumulative dose is high and/or the underlying inflammatory disease is active, treatment with anti-osteoporotic drugs, usually an oral bisphosphonate, is indicated.

Keywords

Glucocorticoids Inflammation Rheumatic diseases Rheumatoid arthritis Osteoporosis Fracture prevention 

Notes

Funding

No funding to declare.

Compliance with Ethical Standard

Conflict of interest

MGY received consultant and/or speaker fees from Eli Lilly and Company Netherlands and Abbvie. IEMB received consultant and/or speaker fees from Eli Lilly and Company Netherlands, Merck Sharpe and Dohme, Amgen, UCB Pharma, Roche Netherlands and Sanofi Genzyme. WFL received consultant and/or speaker fees from Amgen, Merck Sharpe, Eli Lilly, Pfizer, Roche, Abbvie and Sanofi Genzyme. JNH declares no conflict of interest.

References

  1. 1.
    Fardet L, Petersen I, Nazareth I (2011) Prevalence of long-term oral glucocorticoid prescriptions in the UK over the past 20 years. Oxford, England 50:1982–1990Google Scholar
  2. 2.
    Braun T, Schett G (2012) Pathways for bone loss in inflammatory disease. Current osteoporosis reports 10:101–108PubMedGoogle Scholar
  3. 3.
    Van Staa TP, Leufkens HG, Cooper C (2002) The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporosis Int 13:777–7787Google Scholar
  4. 4.
    Van Staa TP, Laan RF, Barton IP et al (2003) Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 48:3224–3229PubMedGoogle Scholar
  5. 5.
    Kuchuk NO, Hoes JN, Bijlsma JW, Jacobs JW (2014) Glucocorticoid-induced osteoporosis: an overview. Int J Clin Rheum 9:311–326Google Scholar
  6. 6.
    O’Brien CA, Jia D, Plotkin LI et al (2004) Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 145:1835–1841PubMedGoogle Scholar
  7. 7.
    Ohnaka K, Tanabe M, Kawate H et al (2005) Glucocorticoid suppresses the canonical Wnt signal in cultured human osteoblasts. Biochem Biophys Res Commun 329:177–181PubMedGoogle Scholar
  8. 8.
    Butler JS, Queally JM, Devitt BM et al (2010) Silencing Dkk1 expression rescues dexamethasone-induced suppression of primary human osteoblast differentiation. BMC musculoskeletal disorders 11:210PubMedPubMedCentralGoogle Scholar
  9. 9.
    Komori T (2016) Glucocorticoid Signaling and Bone Biology. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme 48: 755-763Google Scholar
  10. 10.
    Shi C, Huang P, Kang H et al (2015) Glucocorticoid inhibits cell proliferation in differentiating osteoblasts by microRNA-199a targeting of WNT signaling. J Mol Endocrinol 54(3):325–337PubMedGoogle Scholar
  11. 11.
    Pereira RC, Delany AM, Canalis E (2002) Effects of cortisol and bone morphogenetic protein-2 on stromal cell differentiation: correlation with CCAAT-enhancer binding protein expression. Bone 30:685–691PubMedGoogle Scholar
  12. 12.
    Shi XM, Blair HC, Yang X et al (2000) Tandem repeat of C/EBP binding sites mediates PPARgamma2 gene transcription in glucocorticoid-induced adipocyte differentiation. J Cell Biochem 76:518–527PubMedGoogle Scholar
  13. 13.
    Carcamo-Orive I, Gaztelumendi A, Delgado J et al (2010) Regulation of human bone marrow stromal cell proliferation and differentiation capacity by glucocorticoid receptor and AP-1 crosstalk. J bone miner res 25:2115–2125PubMedPubMedCentralGoogle Scholar
  14. 14.
    Bultink IE, Baden M, Lems WF (2013) Glucocorticoid-induced osteoporosis: an update on current pharmacotherapy and future directions. Expert Opin Pharmacother 14:185–197PubMedGoogle Scholar
  15. 15.
    Teitelbaum SL (2012) Bone: the conundrum of glucocorticoid-induced osteoporosis. Nat reviews Endocrinol 8:451–452Google Scholar
  16. 16.
    Hofbauer LC, Gori F, Riggs BL et al (1999) Stimulation of osteoprotegerin ligand and inhibition of osteoprotegerin production by glucocorticoids in human osteoblastic lineage cells: potential paracrine mechanisms of glucocorticoid-induced osteoporosis. Endocrinology 140:4382–4389PubMedGoogle Scholar
  17. 17.
    Kondo T, Kitazawa R, Yamaguchi A et al (2008) Dexamethasone promotes osteoclastogenesis by inhibiting osteoprotegerin through multiple levels. J Cell Biochem 103:335–345PubMedGoogle Scholar
  18. 18.
    Kim HJ, Zhao H, Kitaura H et al (2006) Glucocorticoids suppress bone formation via the osteoclast. J Clin Investig 116:2152–2160PubMedPubMedCentralGoogle Scholar
  19. 19.
    Teitelbaum SL, Seton MP, Saag KG (2011) Should bisphosphonates be used for long-term treatment of glucocorticoid-induced osteoporosis? Arthritis Rheum 63:325–328PubMedPubMedCentralGoogle Scholar
  20. 20.
    Brabnikova Maresova K, Pavelka K et al (2013) Acute effects of glucocorticoids on serum markers of osteoclasts, osteoblasts, and osteocytes. Calcif Tissue Int 92:354–361PubMedGoogle Scholar
  21. 21.
    Bonadonna S, Burattin A, Nuzzo M et al (2005) Chronic glucocorticoid treatment alters spontaneous pulsatile parathyroid hormone secretory dynamics in human subjects. Eur J Endocrinol 152:199–205PubMedGoogle Scholar
  22. 22.
    Whirledge S, Cidlowski JA (2010) Glucocorticoids, stress, and fertility. Minerva Endocrinol 35:109–125PubMedPubMedCentralGoogle Scholar
  23. 23.
    Schakman O, Kalista S, Barbe C et al (2013) Glucocorticoid-induced skeletal muscle atrophy. The international journal of biochemistry & cell biology 45:2163–2172Google Scholar
  24. 24.
    Szulc P, Beck TJ, Marchand F et al (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men–the MINOS study. J bone miner res 20:721–729PubMedGoogle Scholar
  25. 25.
    Buttgereit F, Straub RH, Wehling M et al (2004) Glucocorticoids in the treatment of rheumatic diseases: an update on the mechanisms of action. Arthritis Rheum 50:3408–3417PubMedGoogle Scholar
  26. 26.
    Then T, Ja Cidlowski (2005) Antiinflammatory action of glucocorticoids–new mechanisms for old drugs. N Engl J Med 353:1711–1723Google Scholar
  27. 27.
    Stahn C, Buttgereit F (2008) Genomic and nongenomic effects of glucocorticoids. Nat Clin Pract Rheumatol 4:525–533PubMedGoogle Scholar
  28. 28.
    Coutinho AE, Chapman KE (2011) The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol Cell Endocrinol 335:2–13PubMedPubMedCentralGoogle Scholar
  29. 29.
    Cain DW, Cidlowski JA (2017) Immune regulation by glucocorticoids. Nat Rev Immunol 17:233–247PubMedGoogle Scholar
  30. 30.
    Barnes PJ (1998) Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin Sci (Lond) 94:557–572Google Scholar
  31. 31.
    Smolen JS, Landewe R, Bijlsma J et al (2017) EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis 76:960–977PubMedGoogle Scholar
  32. 32.
    Singh JA, Saag KG, Bridges SL Jr et al (2016) 2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol 68:1–26PubMedGoogle Scholar
  33. 33.
    Sokka T, Kautiainen H, Toloza S et al (2007) QUEST-RA: quantitative clinical assessment of patients with rheumatoid arthritis seen in standard rheumatology care in 15 countries. Ann Rheum Dis 66:1491–1496PubMedPubMedCentralGoogle Scholar
  34. 34.
    Criswell LA, Saag KG, Sems KM et al (2004) Moderate-term, low-dose corticosteroids for rheumatoid arthritis. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD001158 Google Scholar
  35. 35.
    Safy M, Jacobs J, Ijff ND et al (2017) Long-term outcome is better when a methotrexate-based treatment is combined with 10 mg prednisone daily: follow-up after the second Computer-Assisted Management in Early Rheumatoid Arthritis trial. Ann Rheum Dis 76:1432–1435PubMedGoogle Scholar
  36. 36.
    Goekoop-Ruiterman YPM, de Vries-Bouwstra JK, Allaart CF et al (2005) Clinical and radiographic outcomes of four different treatment strategies in patients with early rheumatoid arthritis (the BeSt study): a randomized, controlled trial. Arthritis Rheum 52:3381–3390PubMedGoogle Scholar
  37. 37.
    Van Everdingen AA, Jacobs JWG, Siewertsz van Reesema DR et al (2002) Low-dose prednisone therapy for patients with early active rheumatoid arthritis: clinical efficacy, disease-modifying properties, and side effects: a randomized, double-blind, placebo-controlled clinical trial. Ann Intern Med 136:1–12PubMedGoogle Scholar
  38. 38.
    Boers M, Verhoeven AC, Markusse HM et al (1997) Randomised comparison of combined step-down prednisolone, methotrexate and sulphasalazine with sulphasalazine alone in early rheumatoid arthritis. Lancet 350:309–318PubMedGoogle Scholar
  39. 39.
    Kavanaugh A, Wells AF (2014) Benefits and risks of low-dose glucocorticoid treatment in the patient with rheumatoid arthritis. Rheumatol 53:1742–1751Google Scholar
  40. 40.
    Kirwan JR, Bijlsma JW, Boers M et al (2007) Effects of glucocorticoids on radiological progression in rheumatoid arthritis. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD006356 Google Scholar
  41. 41.
    Jacobs JW, van Everdingen AA, Verstappen SM et al (2006) Followup radiographic data on patients with rheumatoid arthritis who participated in a two-year trial of prednisone therapy or placebo. Arthritis Rheum 54:1422–1428PubMedGoogle Scholar
  42. 42.
    Hafstrom I, Albertsson K, Bonnen A et al (2009) Remission achieved after 2 years treatment with low-dose prednisolone in addition to disease-modifying anti-rheumatic drugs in early rheumatoid arthritis is associated with reduced joint destruction still present after 4 years: an open 2-year continuation study. Ann Rheum Dis 68:508–513PubMedGoogle Scholar
  43. 43.
    Van Tuyl LH, Boers M, Lems WF et al (2010) Survival, comorbidities and joint damage 11 years after the COBRA combination therapy trial in early rheumatoid arthritis. Ann Rheum Dis 69:807–812PubMedGoogle Scholar
  44. 44.
    Westhovens R, Dequeker J (2000) Rheumatoid arthritis and osteoporosis. Z Rheumatol 59(suppl 1):33–38PubMedGoogle Scholar
  45. 45.
    Green MJ, Deodhar AA (2001) Bone changes in early rheumatoid arthritis. Best Pract Res Clin Rheumatol 15:105–123PubMedGoogle Scholar
  46. 46.
    Haugeberg G, Uhlig T, Falch JA et al (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 43:522–530PubMedGoogle Scholar
  47. 47.
    Haugeberg G, Uhlig T, Falch JA et al (2000) Reduced bone mineral density in male rheumatoid arthritis patients: frequencies and associations with demographic and disease variables in ninety-four patients in the Oslo County Rheumatoid Arthritis Register. Arthritis Rheum 43:2776–2784PubMedGoogle Scholar
  48. 48.
    Forslind K, Keller C, Svensson B et al (2003) Reduced bone mineral density in early rheumatoid arthritis is associated with radiological joint damage at baseline and after 2 years in women. J Rheumatol 30:2590–2596PubMedGoogle Scholar
  49. 49.
    Book C, Karlsson M, Akesson K et al (2008) Disease activity and disability but probably not glucocorticoid treatment predicts loss in bone mineral density in women with early rheumatoid arthritis. Scand J Rheumatol 37:248–254PubMedGoogle Scholar
  50. 50.
    Van der Goes MC, Jacobs JW, Jurgens MS et al (2013) Are changes in bone mineral density different between groups of early rheumatoid arthritis patients treated according a tight control strategy with or without prednisone if osteoporosis prophylaxis is applied? Osteoporosis Int 24:1429–1436Google Scholar
  51. 51.
    Guler-Yuksel M, Bijsterbosch J, Goekoop-Ruiterman YP et al (2008) Changes in bone mineral density in patients with recent onset, active rheumatoid arthritis. Ann Rheum Dis 67:823–828PubMedGoogle Scholar
  52. 52.
    Schett G, Stach C, Zwerina J et al (2008) How antirheumatic drugs protect joints from damage in rheumatoid arthritis. Artthritis Rheum 58:2936–2948Google Scholar
  53. 53.
    Schett G, Kaag KG, Bijlsma JW (2010) From bone biology to clinical outcome: state of the art and future perspectives. Ann Rheum Dis 69:1415–1419PubMedGoogle Scholar
  54. 54.
    Vis M, Guler-Yuksel M, Lems WF (2013) Can bone loss in rheumatoid arthritis be prevented? Osteoporosis Int 24:2541–2553Google Scholar
  55. 55.
    Van Staa TP, Geusens P, Bijlsma JW et al (2006) Clinical assessment of the longterm risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum 54:3104–3112PubMedGoogle Scholar
  56. 56.
    Van Staa TP, Leufkens HG, Cooper C (2002) The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int 13:777–787PubMedGoogle Scholar
  57. 57.
    Sambrook PN, Cohen ML, Eisman JA et al (1989) Effects of low dose corticosteroids on bone mass in rheumatoid arthritis: a longitudinal study. Ann Rheum Dis 48:535–538PubMedPubMedCentralGoogle Scholar
  58. 58.
    Verhoeven AC, Boers M, te Koppele JM et al (2001) Bone turnover, joint damage and bone mineral density in early rheumatoid arthritis treated with combination therapy including high-dose prednisone. Rheumatol 40:1231–1237Google Scholar
  59. 59.
    Verhoeven AC, Boers M (1997) Limited bone loss due to corticosteroids; a systematic review of prospective studies in rheumatoid arthritis and other diseases. J Rheumatol 24:1495–1503PubMedGoogle Scholar
  60. 60.
    Habib GS, Haj S (2005) Bone mineral density in patients with early arthritis treated with corticosteroids. Clin Rheumatol 24:129–133PubMedGoogle Scholar
  61. 61.
    Haugeberg G, Strand A, Kvien TK et al (2005) Reduced loss of hand bone density with prednisolone in early rheumatoid arthritis: results from a randomized placebo-controlled trial. Arch Intern Med 165:1293–1297PubMedGoogle Scholar
  62. 62.
    Guler-Yuksel M, Allaart CF, Goekoop-Ruiterman YP et al (2009) Changes in hand and generalised bone mineral density in patients with recent-onset rheumatoid arthritis. Ann Rheum Dis 68:330–336PubMedGoogle Scholar
  63. 63.
    Linda Hartman, Linda A. Rasch, Thomas Klausch, et al (submitted) Harm and benefit associated with low-dose glucocorticoids added to the treatment strategies for rheumatoid arthritis in elderly patients (GLORIA trial): Design of a 2-year multicentre, double-blind, randomised controlled trialGoogle Scholar
  64. 64.
    Gudbjornsson B, Juliusson UI, Gudjonsson FV (2002) Prevalence of long term steroid treatment and the frequency of decision making to prevent steroid induced osteoporosis in daily clinical practice. Ann Rheum Dis 61:32–36PubMedPubMedCentralGoogle Scholar
  65. 65.
    Weinstein RS (2011) Clinical practice. glucocorticoid-induced bone disease. N Engl J Med 365:62–70PubMedGoogle Scholar
  66. 66.
    Canalis E, Mazziotti G, Giustina A et al (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18:1319–1328PubMedGoogle Scholar
  67. 67.
    Schett G, Kiechl S, Weger S et al (2006) High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch Intern Med 166:2495–2501PubMedGoogle Scholar
  68. 68.
    Eriksson AL, Moverare-Skrtic S, Ljunggren Ö et al (2014) High-sensitivity CRP is an independent risk factor for all fractures and vertebral fractures in elderly men: the MrOS Sweden study. J Bone Miner Res 29:418–423PubMedPubMedCentralGoogle Scholar
  69. 69.
    Konijn NPC, van Tuyl LHD, Bultink IEM et al (2014) Making the invisible visible: bioelectrical impedance analysis demonstrates unfavourable body composition in rheumatoid arthritis patients in clinical practice. Scand J Rheumatol 43:273–278PubMedGoogle Scholar
  70. 70.
    Katz PP, Andrews J, Yazdany J et al (2017) Is frailty a relevant concept in SLE? Lupus Sci Med 4:e000186PubMedPubMedCentralGoogle Scholar
  71. 71.
    Van Staa TP, Leufkens HG, Abenhaim L et al (2000) Use of oral corticosteroids and risk of fractures. J Bone Miner Res 15:993–1000PubMedGoogle Scholar
  72. 72.
    Steinbuch M, Youket TE, Cohen S (2004) Oral glucocorticoid use is associated with an increased risk of fracture. Osteoporos Int 15:323–328PubMedGoogle Scholar
  73. 73.
    de Vries F, Bracke M, Leufkens HG et al (2007) Fracture risk with intermittent high-dose oral glucocorticoid therapy. Arthritis Rheum 56:208–214PubMedGoogle Scholar
  74. 74.
    Van Staa TP, Leufkens HG, Abenhaim L et al (2000) Use of oral corticosteroids in the United Kingdom. QJM 93:105–111PubMedGoogle Scholar
  75. 75.
    Van Staa TP, Geusens P, Pols HA et al (2005) A simple score for estimating the long-term risk of fracture in patients using oral glucocorticoids. QJM 98:191–198PubMedGoogle Scholar
  76. 76.
  77. 77.
    Kanis JA, Johansson H, Oden H et al (2011) Guidance for the adjustment of FRAX according to the dose of glucocorticoids. Osteoporosis Int 22:809–816Google Scholar
  78. 78.
    Orstavik RE, Haugeberg G, Mowinckel P et al (2004) Vertebral deformities in rheumatoid arthritis: a comparison with population-based controls. Arch Intern Med 164:420–425PubMedGoogle Scholar
  79. 79.
    Grossmann JM, Gordon R, Ranganath VK et al (2010) American college of rheumatology 2010 recommendations for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Care Res (Hoboken) 62:1515–1526Google Scholar
  80. 80.
    Cosman F, de Beur SJ, LeBoff MS (2009) Clinician’s guide to the prevention and treatment of osteoporosis. National Osteoporosis Foundation, Washington DCGoogle Scholar
  81. 81.
    Bone and tooh society of Great Britain (2003) Guidelines on the prevention and treatment of glucocorticoid-induced osteoporosis. Royal College of Physicians, LondonGoogle Scholar
  82. 82.
    Devogelaer JP, Goemaere S, Boonen S et al (2006) Evidence-based guidelines for the prevention and treatment of glucocorticoid-induced osteoporosis: a consensus document of the Belgian Bone Club. Osteoporos Int 17:8–19PubMedGoogle Scholar
  83. 83.
    Dutch CBO guideline osteoporosis and fracture prevention. 2011. www.cbo.nl/en/Guidelines
  84. 84.
    Finnish national guidelines for treatment of osteoporosis. 2006. www.kaypahoim.fi/web/english/guidelines
  85. 85.
    DVO Guideline 2009 for prevention, diagnosis and therapy of osteoporosis in adults. www.dv-osteologie.org/dvo_leitlinien/dvo-leitlinie-2009
  86. 86.
    Lekamwasam S, Adachi JD, Agnusdei D, Bilezikian J, Joint IOF-ECTS GIO Guidelines Working Group (2012) A framework for the development of guidelines for the management of glucocorticoid-induced osteoporosis. Osteoporos Int 23:2257–2276Google Scholar
  87. 87.
    Buckley L, Gyuatt G, Fink HA et al (2017) 2017 American College of Rheumatology Guideline for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Care Res 69(8):1521–1537Google Scholar
  88. 88.
    Hoes JN, Jacobs JW, Boers M et al (2007) EULAR-evidence based recommendations on the management of systemic glucocorticoid-therapy in rheumatic diseases. Ann Rheum Dis 66:1500–1507Google Scholar
  89. 89.
    Caporali R, Cimmino MA, Ferraccioli G et al (2004) Prednisone plus methotrexate for polymyalgia rheumatica: a randomized, double-blind, placebo-controlled trial. Ann Int Med 141:493–500PubMedGoogle Scholar
  90. 90.
    Lekenwasam S, Adachi JD, Agnusdei D et al (2012) A framework for the development of guidelines for the management of GIOP. Osteoporosis Int 23:2257–2276Google Scholar
  91. 91.
    Body JJ, Bergmann P, Boonen S et al (2011) Non-pharmacological management of osteoporosis: a consensus of the belgian bone club. Osteoporos Int 22:2769–2788PubMedPubMedCentralGoogle Scholar
  92. 92.
    Hoes JN, Jacobs JW, Boers M et al (2007) EULAR evidence-based recommendations on the management of systemic glucocorticoid therapy in rheumatic diseases. Ann Rheum Dis 66:1560–1567PubMedPubMedCentralGoogle Scholar
  93. 93.
    Den Uyl D, Bultink IEM, Lems WF (2011) Advances in glucocorticoid induced osteoporosis. Curr Rheumatol Rep 13:233–240Google Scholar
  94. 94.
    Briot K, Roux C (2015) Glucocorticoid induced osteoporosis. RMD open 1:e00014Google Scholar
  95. 95.
    Buckley LM, Leib ES, Cartularo KS et al (1996) Calcium and vitamin D3 supplementation prevents bone loss in the spine secondary to low dose GC in RA. Ann Int Med 125:961–968PubMedGoogle Scholar
  96. 96.
    Rasch LA, de van der Schueren MA, van Tuyl LH et al (2017) Content validity of a short calcium intake list to estimate daily dietary calcium intake of patients with osteoporosis. Calcif Tissue Int 100:271–277PubMedPubMedCentralGoogle Scholar
  97. 97.
    Reid IR, Bristow SM, Bolland MJ (2015) Calcium supplements: benefits and risks. J Intern Med 278:354–368PubMedGoogle Scholar
  98. 98.
    den Uyl D, Geusens PP, van Berkum FN et al (2010) Patient preference and acceptability of calcium plus vitamin D3 supplementation: a randomised, open, cross-over trial. Clin Rheumatol 29:465–472Google Scholar
  99. 99.
    Van Schoor NM, Lips P (2011) Worldwide vitamin D status. Best Pract Res Clin Endocrinol Metab 25:671–680PubMedGoogle Scholar
  100. 100.
    Lin J, Liu J, Davies ML et al (2016) Serum vitamin D level and rheumatoid arthritis disease activity: review and meta-analysis. PLoS ONE 11:e0146351PubMedPubMedCentralGoogle Scholar
  101. 101.
    Bischoff-Ferrari HA, Willett WC, Orav EJ et al (2012) A pooled analysis of vitamin D dose requirements for fracture prevention. N Engl J Med 367:40–49PubMedGoogle Scholar
  102. 102.
    Bischoff-Ferrari HA, Dawson-Hughes B, Staehelin HB et al (2009) Fall prevention with supplemental and active forms of vitamin D: a meta-analysis of randomised controlled trials. BMJ 339:b3692PubMedPubMedCentralGoogle Scholar
  103. 103.
    Sanders KM, Stuart AL, Williamson EJ et al (2010) Annual high-dose oral vitamin D and falls and fractures in older women: a randomized controlled trial. JAMA 303:1815–1822PubMedGoogle Scholar
  104. 104.
    Bischoff-Ferrari HA, Dawson-Hughes B, Orav EJ et al (2016) Monthly High-Dose Vitamin D Treatment for the Prevention of Functional Decline: a Randomized Clinical Trial. JAMA Intern Med 176:175–183PubMedGoogle Scholar
  105. 105.
    Sambrook P, Birmingham J, Kelly P et al (1993) Prevention of Glucocorticoid Osteoporosis: a comparison of calcium, calcitriol and calcitonin. New Engl J Med 328:1747–1752PubMedGoogle Scholar
  106. 106.
    de Nijs RN, Jacobs JW, Lems WF et al (2006) Alendronate or alfacalcidol in glucocorticoid-induced osteoporosis. N Engl J Med 355:675–684PubMedGoogle Scholar
  107. 107.
    Brotto M, Bonewald L (2015) Bone and muscle: interactions beyond mechanical. Bone 109:14Google Scholar
  108. 108.
    Cianferotti L, Brandi ML (2014) Muscle bone interactions: basic and clinical aspects. Endocrine 45:165–177PubMedGoogle Scholar
  109. 109.
    Yoon V, Maalouf NM, Sakhaee K (2012) The effects of smoking on bone metabolism. Osteoporos Int 23:2081–2092PubMedGoogle Scholar
  110. 110.
    Kanis JA, Johnell O, Oden A et al (2005) Smoking and fracture risk: a meta-analysis. Osteoporos Int 16:155–162PubMedGoogle Scholar
  111. 111.
    Maurel DB, Boisseau N, Benhamou CL et al (2012) Alcohol and bone: review of dose effects and mechanisms. Osteoporos Int 23:1–16PubMedGoogle Scholar
  112. 112.
    Kanis JA, Johansson H, Johnell O et al (2005) Alcohol intake as a risk factor for fracture. Osteoporos Int 16:737–742PubMedGoogle Scholar
  113. 113.
    Berg KM, Kunins HV, Jackson JL et al (2008) Association between alcohol consumption and both osteoporotic fracture and bone density. Am J Med 121:406–418PubMedPubMedCentralGoogle Scholar
  114. 114.
    Black DM, Cummings SR, Karpf DB et al (1996) Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Lancet 348:1535–1541PubMedGoogle Scholar
  115. 115.
    Harris ST, Watts NB, Genant HK et al (1999) Effects of risedronate treatment on vertebral and nonvertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial. JAMA 282:1344–1352PubMedGoogle Scholar
  116. 116.
    Black DM, Delmas PD, Eastell IR (2007) Once-yearly zoledronic acid for treatment of postmenopausal osteoporosis. N Engl J Med 356:1809–1822PubMedGoogle Scholar
  117. 117.
    Cummings SR, San Martin J, McClung MR et al (2009) Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med 361:756–765PubMedGoogle Scholar
  118. 118.
    Saag K, Emkey R, Schnitzer TJ et al (1998) Alendronate for the prevention and treatment of glucocorticoid-induced osteoporosis. New Engl J Med 339:292–299PubMedGoogle Scholar
  119. 119.
    Wallach S, Cohen S, Reid DM et al (2000) Effects of risedronate treatment on bone density and vertebral fracture in patients on corticosteroid therapy. Calcif Tissue Int 67:277–285PubMedGoogle Scholar
  120. 120.
    Reid DM, Devogelaer JP, Saag K et al (2009) Zoledronic acid and risedronate in the prevention and treatment of GIOP (HORIZON): a multicentre, double-blind, double-dummy, randomized controlled trail. Lancet 373:1253–1263PubMedGoogle Scholar
  121. 121.
    Kanis JA, Stevenson M, Mc Closkey EV et al (2007) Glucocorticoid-induced osteoporosis: a systematic review and cost-utility analysis. Health Technol Assessment 11(7):1–231Google Scholar
  122. 122.
    Makhzoum A, Petriw L, Sattin M et al (2017) OP0049 Systematic review of randomized controlled trials evaluating bisphosphonates for the prevention and treatment of glucocorticoid-induced osteoporosis. Ann Rheum Dis 76:71–72Google Scholar
  123. 123.
    Mok CC, Ying KY, To CH et al (2011) Raloxifene for prevention of glucocorticoid-induced bone loss: a 12 month randomized double-blinded placebo-controlled trial. Ann Rheum Dis 70:778–784PubMedGoogle Scholar
  124. 124.
    Dore RK, Cohen SB, Lane NE et al (2010) Effects of denosumab on bone mineral density and bone turnover in patients with rheumatoid arthritis receiving concurrent glucocorticoids or bisphosphonates. Ann Rheum Dis 69:872–875PubMedGoogle Scholar
  125. 125.
    Curtis JR, Westfall AO, Allison JJ et al (2005) Longitudinal patterns in the prevention of glucocorticoid-treated patients. Arthritis Rheum 52:2485–2494PubMedGoogle Scholar
  126. 126.
    Duyvendak M, Naunton M, Atthobari J et al (2007) Corticosteroid-induced osteoporosis prevention: longitudinal practice patterns in the Netherlands 2001–2005. Ost Int 18:1429–1433Google Scholar
  127. 127.
    Klop C, de Vries F, Vinks T et al (2014) Increase in prophylaxis of glucocorticoid-induced osteoporosis by pharmacist feedback. Osteoporosis Int 25:385–392Google Scholar
  128. 128.
    Saag KG, Zanchetta JR, Devogelaer JP et al (2009) Effects of teriparatide versus alendronate for testing glucocorticoid-induced osteoporosis: 36 months results of a randomized, double-blind, controlled trial. Arthritis Rheum 60:3346–3355PubMedGoogle Scholar
  129. 129.
    Gluer CC, Marin F, Ringe JD et al (2013) Comparative effects of teriparatide and risedronate in glucocorticoid-induced osteoporosis in men: 18 month results of the EuroGIOPs trial. J Bone Min Res 28:1355–1368Google Scholar
  130. 130.
    Van de Hoven JM, van Tomme SR, Metselaar JM et al (2011) Liposomal drug formulations in the treatment of rheumatoid arthritis. Mol Pharm 8:1002–1015PubMedGoogle Scholar
  131. 131.
    Barrera P MS, Smetsers AI, et al. (2008) Long-circulating liposomal prednisolone versus pulse intramuscular methylprednisolone in patients with active rheumatoid arthritis. ACRGoogle Scholar
  132. 132.
    Conrado DJ, Krishnaswami S, Shoji S et al (2016) Predicting the probability of successful efficacy of a dissociated agonist of the glucocorticoid receptor from dose-response analysis. J Pharmacokinet Pharmacodyn 43:325–341PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2018

Authors and Affiliations

  • Melek Güler-Yüksel
    • 1
  • Jos N. Hoes
    • 2
  • Irene E.M. Bultink
    • 3
  • Willem F. Lems
    • 3
  1. 1.Department of Rheumatology and Clinical ImmunologyMaasstad hospitalRotterdamThe Netherlands
  2. 2.Bravis hospitalRoosendaalThe Netherlands
  3. 3.Department of Rheumatology, Amsterdam Rheumatology and immunology CenterVU University Medical CenterAmsterdamThe Netherlands

Personalised recommendations