Top

Published in:

01-08-2020 | Glucocorticoid | Review

Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: a systematic review and meta-analysis

Authors: Y. Wang, R. Zhao, Z. Gu, C. Dong, G. Guo, L. Li

Published in: Osteoporosis International | Issue 8/2020

Abstract

We evaluated the effects of glucocorticoids on bone mineral density (BMD), and prevalence of osteoporosis and fracture in rheumatoid arthritis (RA) by meta-analysis. Until June 26, 2019, we conducted a systematic literature search in EMBASE, Web of science, PubMed, and Cochrane Library to obtain BMD and the prevalence of osteoporosis and fracture in glucocorticoid-treated subjects with RA. The BMD of the treatment and control groups were analyzed by meta-analysis (Stata. version 15), and the 95% confidence interval (CI) was calculated. We identified 15 observational studies, including 46,711 RA subjects and 857 healthy controls. The BMD of the lumbar spine (− 0.038 g/cm²; CI, − 0.052, − 0.024) and femoral neck (− 0.017 g/cm²; − 0.030, − 0.003) in RA treated with glucocorticoids were significantly lower than those in RA controls. Compared with healthy control group, the BMD of the lumbar spine (− 0.094 g/cm²; − 0.126, − 0.061) and femoral neck (− 0.097 g/cm², − 0.109, − 0.085) of RA treated with glucocorticoids decreased more significantly. The prevalence of osteoporosis in whole body, spine, and femur was 38.6% (0.305, 0.466), 32.9% (0.277, 0.381), and 21.7% (0.106, 0.328), respectively. And the prevalence of vertebral fracture was 13.0% (0.058, 0.203). Glucocorticoids may lead to a decline in skeletal health in subjects with RA, especially in vertebral and femoral BMD, compared with normal people or RA without glucocorticoid therapy. Meanwhile, osteoporosis and fractures were also common. Therapeutic measures should be targeted at individuals, which needs further study. Through meta-analysis, we found that glucocorticoids have some negative effects on the bone health of subjects with rheumatoid arthritis. Therefore, when using glucocorticoids to treat rheumatoid arthritis, we should take strategic measures to prevent the decline of bone quality.

Available only for authorised users

Adami G, Saag KG (2019) Glucocorticoid-induced osteoporosis update. Curr Opin Rheumatol 31(4):388–393. https://doi.org/10.1097/bor.0000000000000608 CrossRefPubMed

Grossman JM, Gordon R, Ranganath VK, Deal C, Caplan L, Chen W, Curtis JR, Furst DE, McMahon M, Patkar NM, Volkmann E, Saag KG (2010) American College of Rheumatology 2010 recommendations for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Care Res 62(11):1515–1526. https://doi.org/10.1002/acr.20295 CrossRef

Palmowski Y, Buttgereit T, Buttgereit F (2019) The 70th anniversary of glucocorticoids in rheumatic diseases: the second youth of an old friend. Rheumatology (Oxford, England) 58(4):580–587. https://doi.org/10.1093/rheumatology/key169 CrossRef

Kavanaugh A, Wells AF (2014) Benefits and risks of low-dose glucocorticoid treatment in the patient with rheumatoid arthritis. Rheumatology (Oxford, England) 53(10):1742–1751. https://doi.org/10.1093/rheumatology/keu135 CrossRef

Wells GA, Shea BJ, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2010) The Newcastle–Ottawa scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. Appl Eng Agric 18(6):727–734

Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Bmj 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557 CrossRefPubMedPubMedCentral

Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(4):264–269, w264. https://doi.org/10.7326/0003-4819-151-4-200908180-00135 CrossRef

Sambrook PN, Eisman JA, Champion GD, Pocock NA (1988) Sex hormone status and osteoporosis in postmenopausal women with rheumatoid arthritis. Arthritis Rheum 31(8):973–978. https://doi.org/10.1002/art.1780310805 CrossRefPubMed

Peel NFA, Moore DJ, Barrington NA, Bax DE, Eastell R (1995) Risk of vertebral fracture and relationship to bone mineral density in steroid treated rheumatoid arthritis. Ann Rheum Dis 54(10):801–806CrossRef

10.

Shibuya K, Hagino H, Morio Y, Teshima R (2002) Cross-sectional and longitudinal study of osteoporosis in patients with rheumatoid arthritis. Clin Rheumatol 21(2):150–158. https://doi.org/10.1007/s10067-002-8274-7 CrossRefPubMed

11.

Ma CC, Xu SQ, Gong X, Wu Y, Qi S, Liu W, Xu JH (2017) Prevalence and risk factors associated with glucocorticoid-induced osteoporosis in Chinese patients with rheumatoid arthritis. Arch Osteoporos 12(1):33. https://doi.org/10.1007/s11657-017-0329-0 CrossRefPubMed

12.

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 23(2):581–587. https://doi.org/10.1007/s00198-011-1584-3 CrossRefPubMed

13.

de Nijs RN, Jacobs JW, Bijlsma JW, Lems WF, Laan RF, Houben HH, ter Borg EJ, Huisman AM, Bruyn GA, van Oijen PL, Westgeest AA, Algra A, Hofman DM (2001) Prevalence of vertebral deformities and symptomatic vertebral fractures in corticosteroid treated patients with rheumatoid arthritis. Rheumatology (Oxford, England) 40(12):1375–1383. https://doi.org/10.1093/rheumatology/40.12.1375 CrossRef

14.

Arai K, Hanyu T, Sugitani H, Murai T, Fujisawa J, Nakazono K, Kondo N, Endo N (2006) Risk factors for vertebral fracture in menopausal or postmenopausal Japanese women with rheumatoid arthritis: a cross-sectional and longitudinal study. J Bone Miner Metab 24(2):118–124. https://doi.org/10.1007/s00774-005-0657-9 CrossRefPubMed

15.

Dao HH, Do QT, Sakamoto J (2011) Bone mineral density and frequency of osteoporosis among Vietnamese women with early rheumatoid arthritis. Clin Rheumatol 30(10):1353–1361. https://doi.org/10.1007/s10067-011-1762-x CrossRefPubMed

16.

Caplan L, Hines AE, Williams E, Prochazka AV, Saag KG, Cunningham F, Hutt E (2011) An observational study of glucocorticoid-induced osteoporosis prophylaxis in a national cohort of male veterans with rheumatoid arthritis. Osteoporos Int 22(1):305–315. https://doi.org/10.1007/s00198-010-1201-x CrossRefPubMed

17.

Lee JH, Cho SK, Han M, Kim D, Bae SC, Sung YK (2014) Are glucocorticoid-induced osteoporosis recommendations sufficient to determine antiosteoporotic treatment for patients with rheumatoid arthritis? Korean J Intern Med 29(4):509–515. https://doi.org/10.3904/kjim.2014.29.4.509 CrossRefPubMedPubMedCentral

18.

Rentero ML, Amigo E, Chozas N, Fernandez Prada M, Silva-Fernandez L, Abad Hernandez MA, Rodriguez Barrera JM, del Pino-Montes J (2015) Prevalence of fractures in women with rheumatoid arthritis and/or systemic lupus erythematosus on chronic glucocorticoid therapy. BMC Musculoskelet Disord 16:300. https://doi.org/10.1186/s12891-015-0733-9 CrossRefPubMedPubMedCentral

19.

Balasubramanian A, Wade SW, Adler RA, Lin CJF, Maricic M, O'Malley CD, Saag K, Curtis JR (2016) Glucocorticoid exposure and fracture risk in patients with new-onset rheumatoid arthritis. Osteoporos Int 27(11):3239–3249. https://doi.org/10.1007/s00198-016-3646-z CrossRefPubMed

20.

Conn DL, Tiliakos A, Bao G, Liu S, Li S, Easley KA (2018) Effect of daily low dose prednisone, divided or single daily dose, in the treatment of African Americans with early rheumatoid arthritis. Clin Rheumatol 37(2):355–365. https://doi.org/10.1007/s10067-017-3943-8 CrossRefPubMed

21.

Rossini M, Viapiana O, Vitiello M, Malavolta N, La Montagna G, Maddali Bongi S, Di Munno O, Nuti R, Manzini CU, Ferri C, Bogliolo L, Mathieu A, Cantatore F, Del Puente A, Muratore M, Grassi W, Frediani B, Saviola G, Delvino P, Mirone L, Ferraccioli G, Tripi G, Piazza I, Gatti D (2017) Prevalence and incidence of osteoporotic fractures in patients on long-term glucocorticoid treatment for rheumatic diseases: the glucocorticoid induced OsTeoporosis TOol (GIOTTO) study. Reumatismo 69(1):30–39. https://doi.org/10.4081/reumatismo.2017.922 CrossRefPubMed

22.

Malochet-Guinamand S, Lambert C, Gossec L, Soubrier M, Dougados M (2019) Evaluation of the implementation of guidelines on the treatment of osteoporosis in patients with rheumatoid arthritis. J Rheumatol. https://doi.org/10.3899/jrheum.180889

23.

Adami G, Saag KG (2019) Osteoporosis pathophysiology, epidemiology, and screening in rheumatoid arthritis. Curr Rheumatol Rep 21(7):34. https://doi.org/10.1007/s11926-019-0836-7 CrossRefPubMed

24.

Shen G, Ren H, Qiu T, Liang WQ, Tang J, Zhang Z, Yao Z, Zhao W, Jiang X (2016) Effect of glucocorticoid withdrawal on glucocorticoid inducing bone impairment. Biochem Biophys Res Commun 477(4):1059–1064. https://doi.org/10.1016/j.bbrc.2016.07.036 CrossRefPubMed

25.

Aeberli D, Fankhauser N, Zebaze R, Bonel H, Moller B, Villiger PM (2019) Effect of rheumatoid arthritis and age on metacarpal bone shaft geometry and density: a longitudinal pQCT study in postmenopausal women. Semin Arthritis Rheum. https://doi.org/10.1016/j.semarthrit.2019.08.003

26.

Monadi M, Javadian Y, Cheraghi M, Heidari B, Amiri M (2015) Impact of treatment with inhaled corticosteroids on bone mineral density of patients with asthma: related with age. Osteoporos Int 26(7):2013–2018. https://doi.org/10.1007/s00198-015-3089-y CrossRefPubMed

27.

Lo JC, Burnett-Bowie SA, Finkelstein JS (2011) Bone and the perimenopause. Obstet Gynecol Clin N Am 38(3):503–517. https://doi.org/10.1016/j.ogc.2011.07.001 CrossRef

28.

Masud T, Miller PD (2000) Bone densitometry in the elderly. Springer, LondonCrossRef

29.

Lewiecki EM, Binkley N, Bilezikian JP, Kendler DL, Leib ES, Petak SM (2006) Official positions of the International Society for Clinical Densitometry. Osteoporos Int 17(11):1700–1701. https://doi.org/10.1007/s00198-006-0202-2 CrossRefPubMed

30.

Lai EL, Huang WN, Chen HH, Hsu CY, Chen DY, Hsieh TY, Hung WT, Lin CT, Lai KL, Tang KT, Chen YM, Chen YH (2019) Ten-year fracture risk by FRAX and osteoporotic fractures in patients with systemic autoimmune diseases. Lupus 28(8):945–953. https://doi.org/10.1177/0961203319855122 CrossRefPubMed

31.

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):2095–2100. https://doi.org/10.1136/annrheumdis-2015-208958 CrossRefPubMedPubMedCentral

32.

Elde KD, Madsen OR (2019) FRAX 10-yr fracture risk in rheumatoid arthritis-assessments with and without bone mineral density may lead to very different results in the individual patient. J Clin Densitom 22(1):31–38. https://doi.org/10.1016/j.jocd.2018.10.007 CrossRefPubMed

33.

Ruyssen-Witrand A, Fautrel B, Saraux A, Le-Loet X, Pham T (2010) Infections induced by low-dose corticosteroids in rheumatoid arthritis: a systematic literature review. Joint Bone Spine 77(3):246–251. https://doi.org/10.1016/j.jbspin.2010.02.009 CrossRefPubMed

34.

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):3104–3112. https://doi.org/10.1002/art.22117 CrossRefPubMed

35.

Balasubramanian A, Wade SW, Adler RA, Saag K, Pannacciulli N, Curtis JR (2018) Glucocorticoid exposure and fracture risk in a cohort of US patients with selected conditions. J Bone Miner Res 33(10):1881–1888. https://doi.org/10.1002/jbmr.3523 CrossRefPubMed

36.

Van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C (2000) Use of oral corticosteroids and risk of fractures. J Bone Miner Res 15(6):993–1000. https://doi.org/10.1359/jbmr.2000.15.6.993 CrossRefPubMed

37.

Krasselt M, Baerwald C (2016) An update on glucocorticoid-induced osteoporosis. Dtsch Med Wochenschr (1946) 141(5):352–357. https://doi.org/10.1055/s-0042-101896 CrossRef

38.

Saag KG, Wagman RB, Geusens P, Adachi JD, Messina OD, Emkey R, Chapurlat R, Wang A, Pannacciulli N, Lems WF (2018) Denosumab versus risedronate in glucocorticoid-induced osteoporosis: a multicentre, randomised, double-blind, active-controlled, double-dummy, non-inferiority study. Lancet Diabetes Endocrinol 6(6):445–454. https://doi.org/10.1016/s2213-8587(18)30075-5 CrossRefPubMed

39.

Buckley L, Guyatt G, Fink HA, Cannon M, Grossman J, Hansen KE, Humphrey MB, Lane NE, Magrey M, Miller M, Morrison L, Rao M, Byun Robinson A, Saha S, Wolver S, Bannuru RR, Vaysbrot E, Osani M, Turgunbaev M, Miller AS, McAlindon T (2017) 2017 American College of Rheumatology Guideline for the prevention and treatment of glucocorticoid-induced osteoporosis. Arthritis Care Res 69(8):1095–1110. https://doi.org/10.1002/acr.23279 CrossRef

40.

Lekamwasam S, Adachi JD, Agnusdei D, Bilezikian J, Boonen S, Borgstrom F, Cooper C, Diez Perez A, Eastell R, Hofbauer LC, Kanis JA, Langdahl BL, Lesnyak O, Lorenc R, McCloskey E, Messina OD, Napoli N, Obermayer-Pietsch B, Ralston SH, Sambrook PN, Silverman S, Sosa M, Stepan J, Suppan G, Wahl DA, Compston JE (2012) A framework for the development of guidelines for the management of glucocorticoid-induced osteoporosis. Osteoporos Int 23(9):2257–2276. https://doi.org/10.1007/s00198-012-1958-1 CrossRefPubMed

41.

Raterman HG, Lems WF (2019) Pharmacological management of osteoporosis in rheumatoid arthritis patients: a review of the literature and practical guide. Drugs Aging 36(12):1061–1072. https://doi.org/10.1007/s40266-019-00714-4 CrossRefPubMedPubMedCentral

42.

Lips P (2007) Relative value of 25(OH)D and 1,25(OH)2D measurements. J Bone Miner Res 22(11):1668–1671. https://doi.org/10.1359/jbmr.070716 CrossRefPubMed

43.

Tang BM, Eslick GD, Nowson C, Smith C, Bensoussan A (2007) Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older: a meta-analysis. Lancet 370(9588):657–666. https://doi.org/10.1016/s0140-6736(07)61342-7 CrossRefPubMed

44.

Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R (2014) Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int 25(10):2359–2381. https://doi.org/10.1007/s00198-014-2794-2 CrossRefPubMedPubMedCentral

45.

Iwamoto N, Okamoto M, Tsuji S, Endo Y, Takatani A, Shimizu T, Umeda M, Fukui S, Sumiyoshi R, Igawa T, Koga T, Kawashiri SY, Aramaki T, Ichinose K, Tamai M, Nakamura H, Origuchi T, Eguchi K, Ueki Y, Kawakami A (2019) Denosumab is effective toward glucocorticoid-induced osteoporosis patients complicated with rheumatic diseases regardless of prior anti-osteoporotic drugs. J Bone Miner Metab 37(3):554–562. https://doi.org/10.1007/s00774-018-0955-7 CrossRefPubMed

46.

Kendler DL, Marin F, Zerbini CAF, Russo LA, Greenspan SL, Zikan V, Bagur A, Malouf-Sierra J, Lakatos P, Fahrleitner-Pammer A, Lespessailles E, Minisola S, Body JJ, Geusens P, Moricke R, Lopez-Romero P (2018) Effects of teriparatide and risedronate on new fractures in post-menopausal women with severe osteoporosis (VERO): a multicentre, double-blind, double-dummy, randomised controlled trial. Lancet 391(10117):230–240. https://doi.org/10.1016/s0140-6736(17)32137-2 CrossRefPubMed

Title: Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: a systematic review and meta-analysis
Authors: Y. Wang
R. Zhao
Z. Gu
C. Dong
G. Guo
L. Li
Publication date: 01-08-2020
Publisher: Springer London
Keywords: Glucocorticoid
Osteoporosis
Osteoporosis
Rheumatoid Arthritis
Published in: Osteoporosis International / Issue 8/2020
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI: https://doi.org/10.1007/s00198-020-05360-w

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: a systematic review and meta-analysis

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2020

Effects of dynamic resistance exercise on bone mineral density in postmenopausal women: a systematic review and meta-analysis with special emphasis on exercise parameters

Impact of denosumab on cardiovascular calcification in patients with secondary hyperparathyroidism undergoing dialysis: a pilot study

Osteoporosis care after distal radius fracture reduces subsequent hip or spine fractures: a 4-year longitudinal study

Existing severe osteoporotic vertebral fractures in elderly Chinese males were only weakly associated with higher further vertebral fracture risk at year-4 follow-up

Correction to: Abaloparatide effect on forearm bone mineral density and wrist fracture risk in postmenopausal women with osteoporosis

Correspondence to “Denosumab-induced hypocalcemia in patients with osteoporosis: can you know who will get low?”