Skip to main content

Advertisement

Log in

Association of sarcopenia and vitamin D deficiency with glucocorticoid-induced osteoporosis in Chinese patients with rheumatoid arthritis

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Objectives

The study aimed to explore the association of sarcopenia and vitamin D deficiency with glucocorticoid-induced osteoporosis (GIOP) in Chinese patients with rheumatoid arthritis (RA).

Method

Skeletal muscle mass, serum 25(OH)D levels, and bone mineral density (BMD) were assessed.

Results

The prevalence of OP, sarcopenia, and vitamin D deficiency in RA patients was significantly higher than in controls (all P < 0.001). The percentage of GC use was 56.9%, and the prevalence of GIOP was 38.1% in 480 RA patients. The prevalence of OP in RA patients without sarcopenia was lower than that in RA patients with sarcopenia (P < 0.05). In RA patients with and without GC, the prevalence of OP in patients without sarcopenia was significantly lower than that in patients with sarcopenia (P < 0.001 and P < 0.05). Female sex (OR = 54.737; 95% CI: 7.103–421.809; P < 0.0001), age (OR = 1.078; 95% CI: 1.048–1.110; P < 0.0001), sarcopenia, and vitamin D deficiency (OR = 2.250; 95% CI: 1.246–64.065; P = 0.007) were risk factors for GIOP in RA patients.

Conclusions

GIOP is associated with sarcopenia and vitamin D deficiency and is widespread among Chinese patients with RA.

Key points

·Percentage of using GC and the prevalence of OP were all high in Chinese patients with RA.

·GIOP was widely existed in Chinese RA patients, which was associated with sarcoprnia and vitamin D deficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Raterman HG, Bultink IE, Lems WF (2020) Osteoporosis in patients with rheumatoid arthritis: an update in epidemiology, pathogenesis, and fracture prevention. Expert Opin Pharmacother 21:1725–1737. https://doi.org/10.1080/14656566.2020.1787381

    Article  PubMed  Google Scholar 

  2. Korb-Pap A, Stratis A, Mühlenberg K, Niederreiter B, Hayer S, Echtermeyer F, Stange R, Zwerina J, Pap T, Pavenstädt H, Schett G, Smolen JS, Redlich K (2012) Early structural changes in cartilage and bone are required for the attachment and invasion of inflamed synovial tissue during destructive inflammatory arthritis. Ann Rheum Dis 71:1004–1011. https://doi.org/10.1136/annrheumdis-2011-200386

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  4. Kareem R, Botleroo RA, Bhandari R, Ogeyingbo OD, Ahmed R, Gyawali M, Venkatesan N, Elshaikh AO (2021) The impact of rheumatoid arthritis on bone loss: links to osteoporosis and osteopenia. Cureus 13:e17519. https://doi.org/10.7759/cureus.17519

    Article  PubMed  PubMed Central  Google Scholar 

  5. Buttgereit F (2020) Views on glucocorticoid therapy in rheumatology: the age of convergence. Nat Rev Rheumatol 16:239–246. https://doi.org/10.1038/s41584-020-0370-z

    Article  CAS  PubMed  Google Scholar 

  6. Saag KG (2012) Short-term and long-term safety of glucocorticoids in rheumatoid arthritis. Bull NYU Hosp Jt Dis 70(Suppl 1):21–25

    PubMed  Google Scholar 

  7. Chinese Association of Rheumatology and Immunology Physicians; Chinese Rheumatology Association; Chinese Society of Bone and Mineral Research; National Clinical Research Center for Dermatologic and Immunologic Diseases (2021) Chinese consensus on the prevention and treatment of glucocorticoid induced osteoporosis (2020). Zhonghua Nei Ke Za Zhi 60:13–21. https://doi.org/10.3760/cma.j.cn112138-20201102-00914

    Article  Google Scholar 

  8. Wang Y, Zhao R, Gu Z, Dong C, Guo G, Li L (2020) Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: a systematic review and meta-analysis. Osteoporos Int 31:1401–1409. https://doi.org/10.1007/s00198-020-05360-w

    Article  CAS  PubMed  Google Scholar 

  9. Chiodini I, Falchetti A, Merlotti D, Eller Vainicher C, Gennari L (2020) Updates in epidemiology, pathophysiology and management strategies of glucocorticoid-induced osteoporosis. Expert Rev Endocrinol Metab 15:283–298. https://doi.org/10.1080/17446651.2020.1772051

    Article  CAS  PubMed  Google Scholar 

  10. Sato AY, Richardson D, Cregor M, Davis HM, Au ED, McAndrews K, Zimmers TA, Organ JM, Peacock M, Plotkin LI, Bellido T (2017) Glucocorticoids induce bone and muscle atrophy by tissue-specific mechanisms upstream of E3 ubiquitin ligases. Endocrinology 158:664–677. https://doi.org/10.1210/en.2016-1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gennari C (1993) Differential effect of glucocorticoids on calcium absorption and bone mass. Br J Rheumatol 32:11–14. https://doi.org/10.1093/rheumatology/32.suppl_2.11

    Article  PubMed  Google Scholar 

  12. Troy KL, Mancuso ME, Butler TA, Johnson JE (2018) Exercise early and often: effects of physical activity and exercise on women's bone health. Int J Environ Res Public Health15:878. https://doi.org/10.3390/ijerph15050878

  13. Sobh MM, Abdalbary M, Elnagar S, Nagy E, Elshabrawy N, Abdelsalam M, Asadipooya K, El-Husseini A (2022) Secondary osteoporosis and metabolic bone diseases. J Clin Med 11:2382. https://doi.org/10.3390/jcm11092382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Scott DL, Symmons DP, Coulton BL, Popert AJ (1987) Long-term outcome of treating rheumatoid arthritis: results after 20 years. Lancet 1:1108–1111. https://doi.org/10.1016/s0140-6736(87)91672-2

    Article  CAS  PubMed  Google Scholar 

  15. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd et al (2010) 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581. https://doi.org/10.1002/art.27584

    Article  PubMed  Google Scholar 

  16. 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 12:33. https://doi.org/10.1007/s11657-017-0329-0

    Article  PubMed  Google Scholar 

  17. Richards AM, Coleman NW, Knight TA, Belkoff SM, Mears SC (2010) Bone density and cortical thickness in normal, osteopenic, and osteoporotic sacra. J Osteoporos 2010:504078. https://doi.org/10.4061/2010/504078

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, Jang HC et al (2020) Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 21:300–307. https://doi.org/10.1016/j.jamda.2019.12.012

    Article  PubMed  Google Scholar 

  19. Holick MF (2011) Vitamin D deficiency in 2010: health benefits of vitamin D and sunlight: a D-bate. Nat Rev Endocrinol 7:73–75. https://doi.org/10.1038/nrendo.2010.234

    Article  CAS  PubMed  Google Scholar 

  20. Hardy RS, Zhou H, Seibel MJ, Cooper MS (2018) Glucocorticoids and bone: consequences of endogenous and exogenous excess and replacement therapy. Endocr Rev 39:519–548. https://doi.org/10.1210/er.2018-00097

    Article  PubMed  Google Scholar 

  21. Park JH, Park EK, Koo DW, Lee S, Lee SH, Kim GT, Lee SG (2017) Compliance and persistence with oral bisphosphonates for the treatment of osteoporosis in female patients with rheumatoid arthritis. BMC Musculoskelet Disord 18:152. https://doi.org/10.1186/s12891-017-1514-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lindner L, Callhoff J, Alten R, Krause A, Ochs W, Zink A, Albrecht K (2020) Osteoporosis in patients with rheumatoid arthritis: trends in the German National Database 2007-2017. Rheumatol Int 40:2005–2012. https://doi.org/10.1007/s00296-020-04593-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Steinbuch M, Youket TE, Cohen S (2004) Oral glucocorticoid use is associated with an increased risk of fracture. Osteoporos Int 15:323–328. https://doi.org/10.1007/s00198-003-1548-3

    Article  CAS  PubMed  Google Scholar 

  24. Wang D, Song J, Ma H (2018) An in vitro experimental insight into the osteoblast responses to vitamin D3 and its metabolites. Pharmacology 101:225–235. https://doi.org/10.1159/000486446

    Article  CAS  PubMed  Google Scholar 

  25. Meena N, Singh Chawla SP, Garg R, Batta A, Kaur S (2018) Assessment of vitamin D in rheumatoid arthritis and its correlation with disease activity. J Nat Sci Biol Med 9:54–58. https://doi.org/10.4103/jnsbm.JNSBM_128_17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hong Q, Xu J, Xu S, Lian L, Zhang M, Ding C (2014) Associations between serum 25-hydroxyvitamin D and disease activity, inflammatory cytokines and bone loss in patients with rheumatoid arthritis. Rheumatology (Oxford) 53:1994–2001. https://doi.org/10.1093/rheumatology/keu173

    Article  CAS  PubMed  Google Scholar 

  27. Zhang Y, Leung DYM, Goleva E (2013) Vitamin D enhances glucocorticoid action in human monocytes: involvement of granulocyte-macrophage colony-stimulating factor and mediator complex subunit 14. J Biol Chem 288:14544–14553. https://doi.org/10.1074/jbc.M112.427054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mazziotti G, Formenti AM, Adler RA, Bilezikian JP, Grossman A, Sbardella E, Minisola S, Giustina A (2016) Glucocorticoid-induced osteoporosis: pathophysiological role of GH/IGF-I and PTH/vitamin D axes, treatment options and guidelines. Endocrine 54:603–611. https://doi.org/10.1007/s12020-016-1146-8

    Article  CAS  PubMed  Google Scholar 

  29. Huybers S, Naber TH, Bindels RJ, Hoenderop JG (2007) Prednisolone-induced Ca2+ malabsorption is caused by diminished expression of the epithelial Ca2+ channel TRPV6. Am J Physiol Gastrointest Liver Physiol 292:G92–G97. https://doi.org/10.1152/ajpgi.00317.2006

    Article  CAS  PubMed  Google Scholar 

  30. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:601. https://doi.org/10.1093/ageing/afz046

    Article  PubMed  PubMed Central  Google Scholar 

  31. Torii M, Hashimoto M, Hanai A, Fujii T, Furu M, Ito H et al (2019) Prevalence and factors associated with sarcopenia in patients with rheumatoid arthritis. Mod Rheumatol 29:589–595. https://doi.org/10.1080/14397595.2018.1510565

    Article  PubMed  Google Scholar 

  32. Tournadre A, Pereira B, Dutheil F, Giraud C, Courteix D, Sapin V, Frayssac T, Mathieu S, Malochet-Guinamand S, Soubrier M (2017) Changes in body composition and metabolic profile during interleukin 6 inhibition in rheumatoid arthritis. J Cachexia Sarcopenia Muscle 8:639–646. https://doi.org/10.1002/jcsm.12189

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ngeuleu A, Allali F, Medrare L, Madhi A, Rkain H, Hajjaj-Hassouni N (2017) Sarcopenia in rheumatoid arthritis: prevalence, influence of disease activity and associated factors. Rheumatol Int 37:1015–1020. https://doi.org/10.1007/s00296-017-3665-x

    Article  CAS  PubMed  Google Scholar 

  34. Doğan SC, Hizmetli S, Hayta E, Kaptanoğlu E, Erselcan T, Güler E (2015) Sarcopenia in women with rheumatoid arthritis. Eur J Rheumatol 2:57–61. https://doi.org/10.5152/eurjrheum.2015.0038

    Article  PubMed  PubMed Central  Google Scholar 

  35. Giles JT, Ling SM, Ferrucci L, Bartlett SJ, Andersen RE, Towns M, Muller D, Fontaine KR, Bathon JM (2008) Abnormal body composition phenotypes in older rheumatoid arthritis patients: association with disease characteristics and pharmacotherapies. Arthritis Rheum 59:807–815. https://doi.org/10.1002/art.23719

    Article  PubMed  PubMed Central  Google Scholar 

  36. Reina D, Gómez-Vaquero C, Díaz-Torné C, JMN S, Rheumatology Service. Hospital Moisès Broggi (2019) Assessment of nutritional status by dual X-Ray absorptiometry in women with rheumatoid arthritis: A case-control study. Medicine (Baltimore) 98:e14361. https://doi.org/10.1097/MD.0000000000014361

    Article  CAS  PubMed  Google Scholar 

  37. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R (2004) Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol 159:413–421. https://doi.org/10.1093/aje/kwh058

    Article  PubMed  Google Scholar 

  38. Di Monaco M, Vallero F, Di Monaco R, Tappero R (2011) Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr 52:71–74. https://doi.org/10.1016/j.archger.2010.02.002

    Article  PubMed  Google Scholar 

  39. Beaudart C, Buckinx F, Rabenda V, Gillain S, Cavalier E, Slomian J, Petermans J, Reginster JY, Bruyère O (2014) The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: a systematic review and meta-analysis of randomized controlled trials. J Clin Endocrinol Metab 99:4336–4345. https://doi.org/10.1210/jc.2014-1742

    Article  CAS  PubMed  Google Scholar 

  40. Uchitomi R, Oyabu M, Kamei Y (2020) Vitamin D and sarcopenia: potential of vitamin D supplementation in sarcopenia prevention and treatment. Nutrients 12:3189. https://doi.org/10.3390/nu12103189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hirose Y, Onishi T, Miura S, Hatazawa Y, Kamei Y (2018) Vitamin D attenuates FOXO1-target atrophy gene expression in C2C12 muscle cells. J Nutr Sci Vitaminol (Tokyo) 64:229–232. https://doi.org/10.3177/jnsv.64.229

    Article  CAS  PubMed  Google Scholar 

  42. Gogulothu R, Nagar D, Gopalakrishnan S, Garlapati VR, Kallamadi PR, Ismail A (2020) Disrupted expression of genes essential for skeletal muscle fibre integrity and energy metabolism in Vitamin D deficient rats. J Steroid Biochem Mol Biol 197:105525. https://doi.org/10.1016/j.jsbmb.2019.105525

    Article  CAS  PubMed  Google Scholar 

  43. Minamino H, Katsushima M, Torii M, Yamamoto W, Fujita Y, Ikeda K et al (2021) Serum vitamin D status inversely associates with a prevalence of severe sarcopenia among female patients with rheumatoid arthritis. Sci Rep 11:20485. https://doi.org/10.1038/s41598-021-99894-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the individuals who have helped us in our study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheng-qian Xu.

Ethics declarations

Disclosures

None

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Wj., Wang, Xl., Chu, Yr. et al. Association of sarcopenia and vitamin D deficiency with glucocorticoid-induced osteoporosis in Chinese patients with rheumatoid arthritis. Clin Rheumatol 43, 15–22 (2024). https://doi.org/10.1007/s10067-023-06784-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-023-06784-5

Keywords

Navigation