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Rheumatic Diseases and Osteoporosis

  • Ombretta Di Munno
  • Nazzarena Malavolta
  • Giovanni Minisola
Chapter

Abstract

Inflammatory joint diseases, such as seronegative spondyloarthropathies, rheumatoid arthritis and systemic lupus erythematosus, are characterized by bone complications including osteoporosis and fragility fractures.

References

  1. 1.
    Maruotti N, Corrado A, Cantatore FP. Osteoporosis and rheumatic diseases. Reumatismo. 2014;66:125–35.PubMedCrossRefGoogle Scholar
  2. 2.
    Schett G, Saag KG, Bijlsma JWJ. From bone to biology to clinical outcome: state of the art and future perspectives. Ann Rheum Dis. 2010;69:1415–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C. Use of oral corticosteroids and risk fractures. J Bone Miner Res. 2000;15:993–1000.PubMedCrossRefGoogle Scholar
  4. 4.
    Briot K, Roux C. Inflammation, bone loss and fracture risk in spondyloarthritis. RMD Open. 2015;1(1):e000052.  https://doi.org/10.1136/rmdopen-2015-000052.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med. 2007;13:156–63.PubMedCrossRefGoogle Scholar
  6. 6.
    Haroon NN, Sriganthan J, Al Ghanim N. Effect of TNF-alpha inhibitor treatment on bone mineral density in patients with ankylosing spondylitis: a systematic review and meta-analysis. Semin Arthritis Rheum. 2014;44:155–61.PubMedCrossRefGoogle Scholar
  7. 7.
    Amarasekara DS, Yu J, Rho J. Bone loss triggered by the cytokine network in inflammatory autoimmune diseases. J Immunol Res. 2015;2015:832127.  https://doi.org/10.1155/2015/832127.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ghozlani I, Ghazi M, Nouijai A, et al. Prevalence and risk factors of osteoporosis and vertebral fractures in patients with ankylosing spondylitis. Bone. 2012;44:772–6.CrossRefGoogle Scholar
  9. 9.
    van der Weijden MA, van Denderen JC, Lems WF, et al. Low bone mineral density is related to male gender and decreased functional capacity in early spondylarthropathies. Clin Rheumatol. 2011;30:497–503.PubMedCrossRefGoogle Scholar
  10. 10.
    van der Weijden MA, Claushuis TA, Nazari T, et al. High prevalence of low bone mineral density in patients within 10 years of onset of ankylosing spondylitis: a systematic review. Clin Rheumatol. 2012;31:1529–35.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Klingberg E, Geijer M, Göthlin J, et al. Vertebral fractures in ankylosing spondylitis are associated with lower bone mineral density in both central and peripheral skeleton. J Rheumatol. 2012;39:1987–95.PubMedCrossRefGoogle Scholar
  12. 12.
    Karberg K, Zochling J, Sieper J, et al. Bone loss is detected more frequently in patients with ankylosing spondylitis with syndesmophytes. J Rheumatol. 2005;32:1290–8.PubMedGoogle Scholar
  13. 13.
    Leone A, Marino M, Dell’Atti C, et al. Spinal fractures in patients with ankylosing spondylitis. Rheumatol Int. 2016;5(1):51–5. [Epub ahead of print].Google Scholar
  14. 14.
    Weiss RJ, Wick MC, Ackermann PW, et al. Increased fracture risk in patients with rheumatic disorders and other inflammatory diseases – a case-control study with 53,108 patients with fracture. J Rheumatol. 2010;37:2247–50.PubMedCrossRefGoogle Scholar
  15. 15.
    van der Weijden MA, van der Horst-Bruinsma IE, van Denderen JC, et al. High frequency of vertebral fractures in early spondylarthropathies. Osteoporos Int. 2012;23:1683–90.PubMedCrossRefGoogle Scholar
  16. 16.
    Muñoz-Ortego J, Vestergaard P, Rubio JB, et al. Ankylosing spondylitis is associated with an increased risk of vertebral and nonvertebral clinical fractures: a population-based cohort study. J Bone Miner Res. 2014;29:1770–6.PubMedCrossRefGoogle Scholar
  17. 17.
    Zhao S, Duffield SJ, Moots RJ, et al. Systematic review of association between vitamin D levels and susceptibility and disease activity of ankylosing spondylitis. Rheumatology. 2014;53:1595–603.PubMedCrossRefGoogle Scholar
  18. 18.
    Goldring SR. Osteoimmunology and bone homeostasis: relevance to spondyloarthritis. Curr Rheumatol Rep. 2013;15:342–7.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Ogdie A, Schwartzman S, Eder L, et al. Comprehensive treatment of psoriatic arthritis: managing comorbidities and extraarticular manifestations. J Rheumatol. 2014;41:2315–22.PubMedCrossRefGoogle Scholar
  20. 20.
    Borman P, Babaoğlu S, Gur G, et al. Bone mineral density and bone turnover in patients with psoriatic arthritis. Clin Rheumatol. 2008;27:443–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Busquets N, Vaquero CG, Moreno JR, et al. Bone mineral density status and frequency of osteoporosis and clinical fractures in 155 patients with psoriatic arthritis followed in a university hospital. Rheumatol Clin. 2014;10:89–93.Google Scholar
  22. 22.
    Riesco M, Manzano F, Font P, et al. Osteoporosis in psoriatic arthritis: an assessment of densitometry and fragility fractures. Clin Rheumatol. 2013;32:1799–804.PubMedCrossRefGoogle Scholar
  23. 23.
    Pedreira PG, Pinheiro MM, Szejnfeld VL. Bone mineral density and body composition in postmenopausal women with psoriasis and psoriatic arthritis. Arthritis Res Ther. 2011;13:R16.  https://doi.org/10.1186/ar3240.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Del Puente A, Esposito A, Costa L, et al. Fragility fractures in patients with psoriatic arthritis. J Rheumatol Suppl. 2015;93:36–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Chandran S, Aldei A, Johnson SR, et al. Prevalence and risk factors of low bone mineral density in psoriatic arthritis: a systematic review. Semin Arthritis Rheum. 2016;46(2):174–82.  https://doi.org/10.1016/j.semarthrit.2016.05.005. [Epub ahead of print].CrossRefPubMedGoogle Scholar
  26. 26.
    Kincse G, Bhattoa PH, Herédi E, et al. Vitamin D3 levels and bone mineral density in patients with psoriasis and/or psoriatic arthritis. J Dermatol. 2015;42:679–84.PubMedCrossRefGoogle Scholar
  27. 27.
    McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2015;365:2205–19.CrossRefGoogle Scholar
  28. 28.
    Deodhar AA, Woolf AD. Bone mass measurement and bone metabolism in rheumatoid arthritis: a review. Br J Rheumatol. 1996;35:309–22.PubMedCrossRefGoogle Scholar
  29. 29.
    Michaud K, Wolfe F. Comorbidities in rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2007;21:885–906.PubMedCrossRefGoogle Scholar
  30. 30.
    Kleyer A, Schett G. Arthritis and bone loss: a hen and egg story. Curr Opin Rheumatol. 2014;26:80–4.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Lee JH, Sung YK, Choi CB, et al. The frequency of and risk factors for osteoporosis in Korean patients with rheumatoid arthritis. BMC Musculoskelet Disord. 2016;17:98.  https://doi.org/10.1186/s12891-016-0952-8.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Haugeberg G, Uhlig T, Falch JA, et al. 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.PubMedCrossRefGoogle Scholar
  33. 33.
    Sinigaglia L, Nervetti A, Mela Q, 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.PubMedGoogle Scholar
  34. 34.
    Ørstavik RE, Haugeberg G, Uhlig T, et al. Vertebral deformities in rheumatoid arthritis: a comparison with population based controls. Arch Intern Med. 2004;164:420–5.PubMedCrossRefGoogle Scholar
  35. 35.
    van Staa T, Geusens P, Bijlsma JW, et al. Clinical assessment of the long-term risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum. 2006;54:3104–12.PubMedCrossRefGoogle Scholar
  36. 36.
    Pell NF, Moore DJ, Barrington NA, et al. Risk of vertebral fracture and relationship to bone mineral density in steroid treated rheumatoid arthritis. Ann Rheum Dis. 1995;54:801–6.CrossRefGoogle Scholar
  37. 37.
    Kanis JA, Johnell O, Oden A, et al. FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int. 2008;19:385–97.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Adami S, Bianchi G, Brandi ML, et al. Validation and further development of the WHO 10-year fracture risk assessment tool in Italia postmenopausal women: project rationale and description. Clin Exp Rheumatol. 2010;28:561–70.PubMedGoogle Scholar
  39. 39.
    Vis M, Guler-Yuksel M, Lems WF. Can bone loss in rheumatoid arthritis be prevented? Osteoporos Int. 2013;24:2541–53.PubMedCrossRefGoogle Scholar
  40. 40.
    Miao CG, Yang YY, He X, et al. Wnt signaling pathway in rheumatoid arthritis, with special emphasis on the different roles in synovial inflammation and bone remodeling. Cell Signal. 2013;25:2069–78.PubMedCrossRefGoogle Scholar
  41. 41.
    Kirwan JR. The effect of glucocorticoids on joint destruction in rheumatoid arthritis. The Arthritis and Rheumatism Council Low-Dose Glucocorticoid Study Group. N Engl J Med. 1995;333:142–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Wassenberg S, Rau R, Steinfeld P, et al. Very low-dose prednisolone in early rheumatoid arthritis retards radiographic progression over two years: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum. 2005;52:3371–80.PubMedCrossRefGoogle Scholar
  43. 43.
    Svensson B, Boonen A, Albertsson K, et al. Low-dose prednisolone in addition to the initial disease-modifying antirheumatic drug in patients with early active rheumatoid arthritis reduces joint destruction and increases the remission rate: a two-year randomized trial. Arthritis Rheum. 2005;52:3360–70.PubMedCrossRefGoogle Scholar
  44. 44.
    Canalis E, Mazziotti G, Giustina A, et al. Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int. 2013;18:1319–28.CrossRefGoogle Scholar
  45. 45.
    Compston J. Management of glucocorticoid-induced osteoporosis. Nat Rev Rheumatol. 2010;6:82–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Pereira RMR, de Carvalho JF, Canalis E. Glucocorticoid-induced osteoporosis in rheumatic diseases. Clinics. 2010;65:1197–205.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Martin JC, Munro R, Campbell MK. Effects of disease and corticosteroids on appendicular bone mass in postmenopausal women with rheumatoid arthritis: comparison with axial measurements. Br J Rheumatol. 1997;36:43–9.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Hall GM, Spector TD, Griffin AJ, et al. The effect of rheumatoid arthritis and steroid therapy on bone density in postmenopausal women. Arthritis Rheum. 1993;36:1510–6.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Sambrook PN, Eisman JA, Champion GD, Yeates MG, et al. Determinants of axial bone loss in rheumatoid arthritis. Arthritis Rheum. 1987;30:721–8.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Kroger H, Honkanen R, Saarikoski S, et al. Decreased axial bone mineral density in perimenopausal women with rheumatoid arthritis—a population based study. Ann Rheum Dis. 1994;53:18–23.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Haugeberg G, Uhlig T, Falch JA, et al. Reduced bone mineral density in male rheumatoid arthritis patients. Arthritis Rheum. 2000;43:2776–84.PubMedCrossRefGoogle Scholar
  52. 52.
    Gough AK, Lilley J, Eyre S, et al. Generalised bone loss in patients with early rheumatoid arthritis. Lancet. 1994;344:23–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Fassio A, Idolazzi L, Jaber MA, 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.PubMedCrossRefGoogle Scholar
  54. 54.
    Peng J, Gong Y, Zhang Y, et al. Bone mineral density in patients with rheumatoid arthritis and 4-year follow-up results. J Clin Rheumatol. 2016;22:71–4.PubMedCrossRefGoogle Scholar
  55. 55.
    van Everdingen AA, Jacobs JW, Siewertsz Van Reesema DR, et al. 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. 2002;136:1–12.PubMedCrossRefGoogle Scholar
  56. 56.
    Bakker MF, Jacobs JW, Welsing PM, et al. Low-dose prednisone inclusion in a methotrexate-based, tight control strategy for early rheumatoid arthritis: a randomized trial. Ann Intern Med. 2012;156:329–39.PubMedCrossRefGoogle Scholar
  57. 57.
    Lodder MC, de Jong Z, Kostense PJ, et al. Bone mineral density in patients with rheumatoid arthritis: relation between disease severity and low bone mineral density. Ann Rheum Dis. 2004;63:1576–80.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Orstavik RE, Haugeberg G, Uhlig T, et al. Self reported non-vertebral fractures in rheumatoid arthritis and population based controls: incidence and relationship with bone mineral density and clinical variables. Ann Rheum Dis. 2004;63:177–82.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Huusko TM, Korpela M, Karppi P, et al. Threefold increased risk of hip fractures with rheumatoid arthritis in Central Finland. Ann Rheum Dis. 2001;60:521–2.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Ghazi M, Kolta S, Briot K, et al. Prevalence of vertebral fractures in patients with rheumatoid arthritis: revisiting the role of glucocorticoids. Osteoporos Int. 2012;23:581–7.PubMedCrossRefGoogle Scholar
  61. 61.
    Orstavik RE, Haugeberg G, Mowinckel P, et al. Vertebral deformities in rheumatoid arthritis. Arch Intern Med. 2004;164:420–5.PubMedCrossRefGoogle Scholar
  62. 62.
    Okano T, Inui K, Tada M, et al. High frequency of vertebral fracture and low bone quality in patients with rheumatoid arthritis—results from TOMORROW study. Mod Rheumatol. 2016;2:1–7. [Epub ahead of print].Google Scholar
  63. 63.
    Ochi K, Inoue E, Furuya T, Ikari K, et al. Ten-year incidences of self-reported non-vertebral fractures in Japanese patients with rheumatoid arthritis: discrepancy between disease activity control and the incidence of non-vertebral fracture. Osteoporos Int. 2015;26:961–8.PubMedCrossRefGoogle Scholar
  64. 64.
    Chopin F, Garnéro P, le Henanff A, et al. Long-term effects of infliximab on bone and cartilage turnover markers in patients with rheumatoid arthritis. Ann Rheum Dis. 2008;67:353–7.PubMedCrossRefGoogle Scholar
  65. 65.
    Haugeberg G, Conaghan PG, Quinn M, et al. 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. 2009;68:1898–901.PubMedCrossRefGoogle Scholar
  66. 66.
    Vis M, Havaardsholm EA, Haugeberg G, et al. Evaluation of bone mineral density, bone metabolism, osteoprotegerin and receptor activator of the NFkB ligand serum levels during treatment with infliximab in patients with rheumatoid arthritis. Ann Rheum Dis. 2006;65:1495–9.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Seriolo B, Paolino S, Sulli A, et al. Bone metabolism changes during anti-TNF-alpha therapy in patients with active rheumatoid arthritis. Ann N Y Acad Sci. 2006;1069:420–7.PubMedCrossRefGoogle Scholar
  68. 68.
    Güler-Yüksel M, Bijsterbosch J, Goekoop-Ruiterman YPM, et al. Bone mineral density in patients with recently diagnosed, active rheumatoid arthritis. Ann Rheum Dis. 2007;66:1508–12.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Wijbrandts CA, Klaasen R, Dijkgraaf MGW, et al. Bone mineral density in rheumatoid arthritis patients 1 year after adalimumab therapy: arrest of bone loss. Ann Rheum Dis. 2009;68:373–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Krieckaert CL, Nurmohamed MT, Wolbink G, et al. Changes in bone mineral density during long-term treatment with adalimumab in patients with rheumatoid arthritis: a cohort study. Rheumatology (Oxford). 2013;52:547–53.CrossRefGoogle Scholar
  71. 71.
    Roussy JP, Bessette L, Bernatsky S, et al. Biologic disease-modifying anti-rheumatic drugs and the risk of nonvertebral osteoporotic fractures in patients with rheumatoid arthritis aged 50 years and over. Osteoporos Int. 2013;24:2483–92.PubMedCrossRefGoogle Scholar
  72. 72.
    Coulson KA, Reed G, Gilliam BE, et al. 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. 2009;15:155–60.PubMedCrossRefGoogle Scholar
  73. 73.
    Kim SY, Schneeweiss S, Liu J, et al. Effects of disease-modifying antirheumatic drugs on nonvertebral fracture risk in rheumatoid arthritis: a population-based cohort study. J Bone Miner Res. 2012;27:789–96.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Lisnevskaia L, Murphy G, Isenberg D. Systemic lupus erythematosus. Lancet. 2014;384:1878–88.PubMedCrossRefGoogle Scholar
  75. 75.
    Bultink IEM, Harvey NC, Lalmohamed A, et al. Elevated risk of clinical fractures and associated risk factors in patients with systemic lupus erythematosus versus matched controls: a population-based study in the United Kingdom. Osteoporos Int. 2014;25:1275–83.PubMedCrossRefGoogle Scholar
  76. 76.
    Cramarossa C, Urowitz MB, Su J, et al. Prevalence and associated factors of low bone mass in adults with systemic lupus erythematosus. Lupus. 2016;26(4):365–72. pii: 0961203316664597. [Epub ahead of print].PubMedCrossRefGoogle Scholar
  77. 77.
    Edens C, Robinson AB. Systemic lupus erythematosus, bone health, and osteoporosis. Curr Opin Endocrinol Diabetes Obes. 2015;22:422–31.PubMedCrossRefGoogle Scholar
  78. 78.
    Schmajuk G, Yelin E, Chakravarty E, et al. Osteoporosis screening, prevention and treatment in systemic lupus erythematosus: application of systemic lupus erythematosus quality indicators. Arthritis Care Res (Hoboken). 2010;62:993–1001.CrossRefGoogle Scholar
  79. 79.
    Wang X, Yan S, Liu C, et al. Fracture risk and bone mineral density levels in patients with systemic lupus erythematosus: a systemic review and meta-analysis. Osteoporos Int. 2016;27:1413–23.PubMedCrossRefGoogle Scholar
  80. 80.
    Bultink IEM, Lems WF. Systemic lupus erythematosus and fractures. RMD Open. 2016;1(Suppl 1):e000069. [Epub ahead of print].CrossRefGoogle Scholar
  81. 81.
    Li EK, Tam LS, Griffith JF, et al. High prevalence of asymptomatic vertebral fractures in Chinese women with systemic lupus erythematosus. J Rheumatol. 2009;36:1646–52.PubMedCrossRefGoogle Scholar
  82. 82.
    Carli L, Tani C, Spera V, et al. Risk factors for osteoporosis and fragility fractures in patients with systemic lupus erythematosus. Lupus Sci Med. 2016;3(1):e000098. [Epub ahead of print].PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    García-Carrasco M, Mendoza-Pint C, Riebeling C, et al. Influence of prevalent vertebral fractures on the quality of life patients with systemic lupus erythematosus. Isr Med Assoc J. 2011;13:333–7.PubMedGoogle Scholar
  84. 84.
    Meacock R, Dale N, Harrison MJ. The humanistic and economic burden of systemic lupus erythematosus: a systematic review. PharmacoEconomics. 2013;31:49–61.PubMedCrossRefGoogle Scholar
  85. 85.
    Di Munno O, Mazzantini M, Delle Sedie A, et al. Risk factors for osteoporosis in female patients with systemic lupus erythematosus. Lupus. 2004;13:724–30.PubMedCrossRefGoogle Scholar
  86. 86.
    Sun YN, Feng XY, He L, et al. Prevalence and possible risk factors of low bone mineral density in untreated female patients with systemic lupus erythematosus. Biomed Res Int. 2015;2015:510514. [Epub ahead of print].PubMedPubMedCentralGoogle Scholar
  87. 87.
    Bultink IEM, Vis M, van der Horst-Bruinsma IE, et al. Inflammatory rheumatic disorders and bone. Curr Rheumatol Rep. 2012;14:224–30.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Bonfá AC, Seguro LPC, Caparbo V, et al. RANKL and OPG gene polymorphisms: associations with vertebral fractures and bone mineral density in premenopausal systemic lupus erythematosus. Osteoporos Int. 2015;26:1563–71.PubMedCrossRefGoogle Scholar
  89. 89.
    Fisher A, Srikusalanukul W, Davis M, et al. Cardiovascular diseases in older patients with osteoporotic hip fracture: prevalence, disturbances in mineral and bone metabolism, and bidirectional links. Clin Interv Aging. 2013;8:239–56.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Farhat GN, Newman AB, Sutton-Tyrrell K. The association of bone mineral density measures with incident cardiovascular disease in older adults. Osteoporos Int. 2007;18:999–1008.PubMedCrossRefGoogle Scholar
  91. 91.
    Schoenfeld SR, Kasturi S, Costenbader KH. The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: a systematic review. Semin Arthritis Rheum. 2013;43:77–95.PubMedCrossRefGoogle Scholar
  92. 92.
    Magder LS, Petri M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am J Epidemiol. 2012;176:708–19.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Ajeganova S, Gustafsson T, Jogestrand T, et al. Bone mineral density and carotid atherosclerosis in systemic lupus erythematosus: a controlled cross-sectional study. Arthritis Res Ther. 2015;17:84–96.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Bultink IEM, Lems WF, Kostense PJ, et al. Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum. 2005;54:2044–50.CrossRefGoogle Scholar
  95. 95.
    Bhattoa HP, Kiss E, Bettembuk P, et al. Bone mineral density, biochemical markers of bone turnover, and hormonal status in men with systemic lupus erythematosus. Rheumatol Int. 2001;21:97–102.PubMedCrossRefGoogle Scholar
  96. 96.
    Zhu TY, Griffith JF, Au SK. Bone mineral density change in systemic lupus erythematosus: a 5-year followup study. J Rheumatol. 2014;41:1990–7.PubMedCrossRefGoogle Scholar
  97. 97.
    Petri M. Musculoskeletal complications of systemic lupus erythematosus in the Hopkins lupus cohort: an update. Arthritis Care Res. 1995;8:137–45.PubMedCrossRefGoogle Scholar
  98. 98.
    Mendoza-Pinto C, García-Carrasco M, Sandoval-Cruz H, et al. Risk factors of vertebral fractures in women with systemic lupus erythematosus. Clin Rheumatol. 2009;28:579–85.PubMedCrossRefGoogle Scholar
  99. 99.
    Almehed K, Forsblad d’Elia H, Kvist G, et al. Prevalence and risk factors of osteoporosis in female SLE patients-extended report. Rheumatology (Oxford). 2007;46:1185–90.CrossRefGoogle Scholar
  100. 100.
    Mok CC. Vitamin D and systemic lupus erythematosus: an update. Expert Rev Clin Immunol. 2013;9:453–63.PubMedCrossRefGoogle Scholar
  101. 101.
    Reynolds JA, Bruce IN. Vitamin D treatment for connective tissue diseases: hope beyond the hype? Rheumatology (Oxford). 2016;56(2):178–86. pii: kew212. [Epub ahead of print].CrossRefGoogle Scholar
  102. 102.
    Salman-Monte TC, Torrente-Segarra V, Almirall M, et al. Prevalence and predictors of vitamin D insufficiency in supplemented and non-supplemented women with systemic lupus erythematosus in the Mediterranean region. Rheumatol Int. 2016;36:975–85.PubMedCrossRefGoogle Scholar
  103. 103.
    Yeap SS, Othman AZ, Zain AA, et al. Vitamin D levels: its relationship to bone mineral density response and disease activity in premenopausal Malaysian systemic lupus erythematosus patients on corticosteroids. Int J Rheum Dis. 2012;15:17–24.PubMedCrossRefGoogle Scholar
  104. 104.
    Guo Q, Fan P, Luo J, et al. Assessment of bone mineral density and bone metabolism in young male adults recently diagnosed with systemic lupus erythematosus in China. Lupus. 2016;26(3):289–93. pii: 0961203316664596. [Epub ahead of print].PubMedCrossRefGoogle Scholar
  105. 105.
    Jacobs J, Korswagen LA, Schilder AM, et al. Six-years follow-up study of bone mineral density in patients with systemic lupus erythematosus. Osteoporos Int. 2013;24:1827–33.PubMedCrossRefGoogle Scholar
  106. 106.
    Cutolo M. Further emergent evidence for the vitamin D endocrine system involvement in autoimmune rheumatic disease risk and prognosis. Ann Rheum Dis. 2013;72:473–5.PubMedCrossRefGoogle Scholar
  107. 107.
    Prietl B, Treiber G, Pieber TR, et al. Vitamin D and immune function. Forum Nutr. 2013;5:2502–21.Google Scholar
  108. 108.
    Watad A, Neumann SG, Soriano A, et al. Vitamin D and systemic lupus erythematosus: myth or reality? Isr Med Assoc J. 2016;18:177–82.PubMedGoogle Scholar
  109. 109.
    Ritterhouse LL, Crow SR, Niewold TB, et al. Vitamin D deficiency is associated with an increased autoimmune response in healthy individuals and in patients with systemic lupus erythematosus. Ann Rheum Dis. 2011;70:1569–74.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Durcan L, Petri M. Immunomodulators in SLE: clinical evidence and immunologic actions. J Autoimmun. 2016;74(16):30088–9.  https://doi.org/10.1016/j.jaut.2016.06.010. [Epub ahead of print].CrossRefGoogle Scholar
  111. 111.
    Mok CC, Mak A, Ma KM. Bone mineral density in postmenopausal Chinese patients with systemic lupus erythematosus. Lupus. 2015;14:106–12.CrossRefGoogle Scholar
  112. 112.
    Lakshminarayanan S, Walsh S, Mohanraj M, et al. Factors associated with low bone mineral density in female patients with systemic lupus erythematosus. J Rheumatol. 2001;28:102–8.PubMedGoogle Scholar
  113. 113.
    Mok CC, Ying SK, To CH, et al. Bone mineral density and body composition in men with systemic lupus erythematosus: a case control study. Bone. 2008;43:327–31.PubMedCrossRefGoogle Scholar
  114. 114.
    Mazzantini M, Di Munno O. Glucocorticoid-induced osteoporosis: 2013 update. Reumatismo. 2014;66:144–52.PubMedCrossRefGoogle Scholar
  115. 115.
    Zhu TY, Griffith JF, Qin L, et al. Cortical thinning and progressive cortical porosity in female patients with systemic lupus erythematosus on long-term glucocorticoids: a 2-year case-control study. Osteoporos Int. 2015;26:1759–71.PubMedCrossRefGoogle Scholar
  116. 116.
    Mak A, Lim JQ, Liu Y, et al. Significantly higher estimated 10-year probability of fracture in lupus patients with bone mineral density comparable to that of healthy individuals. Rheumatol Int. 2013;33:299–307.PubMedCrossRefGoogle Scholar
  117. 117.
    Lee JJ, Aghdassi E, Cheung AM, et al. Ten-year absolute fracture risk and hip bone strength in Canadian women with systemic lupus erythematosus. J Rheumatol. 2012;39:1378–84.PubMedCrossRefGoogle Scholar
  118. 118.
    FRAX® tool. http://www.shef.ac.uk/FRAX. Assessed 9 Sept 2011
  119. 119.
    Grossman JM, Gordon R, Ranganath VK, et al. American College of Rheumatology 2010 recommendations for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Care Res (Hoboken). 2010;62:1515–26.CrossRefGoogle Scholar
  120. 120.
    Rizzoli R, Adachi JD, Cooper C, et al. Management of glucocorticoid-induced osteoporosis. Calcif Tissue Int. 2012;91:225–43.PubMedCrossRefGoogle Scholar
  121. 121.
    Francis RM, Aspray TJ, Boering CE, et al. National Osteoporosis Society practical clinical guideline on vitamin D and bone health. Maturitas. 2015;80:119–21.PubMedCrossRefGoogle Scholar
  122. 122.
    Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96:1911–30.CrossRefPubMedGoogle Scholar
  123. 123.
    Saag KG, Zanchetta JR, Devogelaer JP, et al. Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum. 2009;60:3346–55.PubMedCrossRefGoogle Scholar
  124. 124.
    Baron R, Ferrari S, Graham R, et al. Denosumab and bisphosphonates: different mechanisms of actions and effects. Bone. 2011;48:677–92.PubMedCrossRefGoogle Scholar
  125. 125.
    Mok CC, Ho LY, Ma KM. Switching of oral bisphosphonates to denosumab in chronic glucocorticoid users: a 12-month randomized controlled trial. Bone. 2015;75:222–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ombretta Di Munno
    • 1
  • Nazzarena Malavolta
    • 2
  • Giovanni Minisola
    • 3
  1. 1.University of PisaPisaItaly
  2. 2.“Sant’Orsola-Malpighi” HospitalBolognaItaly
  3. 3.“San Camillo” HospitalRomeItaly

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