Corticosteroids and Vertebral Trabecular Bone Quality in Women with Rheumatoid Arthritis
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design: Cross-Sectional Study
2.1.1. Study Population
2.1.2. Inclusion and Exclusion Criteria
2.1.3. Ethics
2.1.4. Study Protocol
2.1.5. Epidemiological Variables
2.1.6. Clinical Assessment
2.1.7. Bone Mineral Density Measurements
2.1.8. Vertebral Bone Quality Assessment
2.2. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Peláez-Ballestas, I.; Sanín, L.H.; Moreno-Montoya, J.; Álvarez-Nemegyei, J.; Burgos-Vargas, R.; Garza-Elizondo, M.; Rodriguez-Amado, J.; Goycochea-Robles, M.-V.; Madariaga, M.; Zamudio, J.; et al. Epidemiology of the rheumatic diseases in Mexico: A study of 5 regions based on the COPCORD methodology. J. Rheumatol. Suppl. 2011, 86, 3–8. [Google Scholar] [CrossRef] [PubMed]
- Cardiel, M.H.; Carrillo, S.; Pérez, M.; Andrade, L.; Pacheco Tena, C.; Silveira, L.H.; Limón, L.; Cerpa, S.; Ureña, S.G.; Durán, S.; et al. Update of the Mexican College of Rheumatology Guidelines for the Pharmacological Treatment of Rheumatoid Arthritis, 2018. Reumatol. Clin. 2021, 17, 215–228. [Google Scholar] [CrossRef] [PubMed]
- Smolen, J.S.; Aletaha, D.; McInnes, I.B. Rheumatoid arthritis. Lancet. 2016, 388, 2023–2038. [Google Scholar] [CrossRef] [PubMed]
- Hauser, B.; Riches, P.L.; Wilson, J.F.; Horne, A.E.; Ralston, S.H. Prevalence and clinical prediction of osteoporosis in a contemporary cohort of patients with rheumatoid arthritis. Rheumatology 2014, 53, 1759–1766. [Google Scholar] [CrossRef] [PubMed]
- Richards, C.; Leslie, W.D. Trabecular bone score in rheumatic disease. Curr. Rheumatol. Rep. 2022, 24, 81–87. [Google Scholar] [CrossRef] [PubMed]
- Tong, J.J.; Xu, S.Q.; Zong, H.X.; Pan, M.J.; Teng, Y.Z.; Xu, J.H. Prevalence and risk factors associated with vertebral osteoporotic fractures in patients with rheumatoid arthritis. Clin. Rheumatol. 2020, 39, 357–364. [Google Scholar] [CrossRef] [PubMed]
- Warzecha, M.; Czerwiński, E.; Amarowicz, J.; Berwecka, M. Trabecular bone score (TBS) in clinical practice—Review. Ortop. Traumatol. Rehabil. 2018, 20, 347–359. [Google Scholar] [CrossRef] [PubMed]
- Bousson, V.; Bergot, C.; Sutter, B.; Levitz, P.; Cortet, B. Trabecular bone score (TBS): Available knowledge, clinical relevance, and future prospects. Osteoporos. Int. 2012, 23, 1489–1501. [Google Scholar] [CrossRef] [PubMed]
- Compston, J.E.; McClung, M.R.; Leslie, W.D. Osteoporosis. Lancet. 2019, 393, 364–376. [Google Scholar] [CrossRef] [PubMed]
- Sparks, J.A. In the Clinic® rheumatoid arthritis. In Annals of Internal Medicine; American College of Physicians: Philadelphia, PA, USA, 2019; Volume 170, p. ITC1–15. [Google Scholar]
- Wang, Y.; Zhao, R.; Gu, Z.; Dong, C.; Guo, G.; Li, L. Effects of glucocorticoids on osteoporosis in rheumatoid arthritis: A systematic review and meta-analysis. Osteoporos. Int. 2020, 31, 1401–1409. [Google Scholar] [CrossRef] [PubMed]
- Sandru, F.; Carsote, M.; Dumitrascu, M.C.; Albu, S.E.; Valea, A. Glucocorticoids and Trabecular Bone Score. J. Med. Life. 2020, 13, 449–453. [Google Scholar] [CrossRef] [PubMed]
- Paggiosi, M.A.; Peel, N.F.A.; Eastell, R. The impact of glucocorticoid therapy on trabecular bone score in older women. Osteoporos. Int. 2015, 26, 1773–1780. [Google Scholar] [CrossRef] [PubMed]
- Ruangnopparut, R.; Charoensri, S.; Sribenjalak, D.; Theerakulpisut, D.; Pongchaiyakul, C. Trabecular Bone Score Improves Fracture Risk Discrimination in Postmenopausal Rheumatoid Arthritis Patients Receiving Glucocorticoids. Int. J. Gen. Med. 2024, 17, 287–295. [Google Scholar] [CrossRef] [PubMed]
- Nowakowska-Płaza, A.; Wroński, J.; Sudoł-Szopińska, I.; Głuszko, P. Clinical Utility of Trabecular Bone Score (TBS) in Fracture Risk Assessment of Patients with Rheumatic Diseases Treated with Glucocorticoids. Horm. Metab. Res. 2021, 53, 499–503. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.A.; Kim, J.; Kim, H.J.; Kim, H.S. Discriminative ability of trabecular bone score over bone mineral density for vertebral and fragility fracture in patients treated with long-term and low-dose glucocorticoid. Int. J. Rheum. Dis. 2021, 24, 1053–1060. [Google Scholar] [CrossRef] [PubMed]
- Corrado, A.; Rotondo, C.; Mele, A.; Cici, D.; Maruotti, N.; Sanpaolo, E.; Colia, R.; Cantatore, F.P. Influence of glucocorticoid treatment on trabecular bone score and bone remodeling regulators in early rheumatoid arthritis. Arthritis Res. Ther. 2021, 23, 180. [Google Scholar] [CrossRef] [PubMed]
- Arnett, F.C.; Edworthy, S.M.; Bloch, D.A.; Mcshane, D.J.; Fries, J.F.; Cooper, N.S.; Healey, L.A.; Kaplan, S.R.; Liang, M.H.; Luthra, H.S.; et al. The american rheumatism association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988, 31, 315–324. [Google Scholar] [CrossRef] [PubMed]
- Fransen, J.; van Riel, P.L.C.M. The Disease Activity Score and the EULAR response criteria. In Clin. Exp. Rheumatol.; 2005; 23, (Suppl. S39), pp. S93–S99. Available online: http://www.ncbi.nlm.nih.gov/pubmed/16273792 (accessed on 7 June 2025). [CrossRef] [PubMed]
- Cardiel, M.H.; Abello-Banfi, M.; Ruiz-Mercado, R.; Alarcon-Segovia, D. How to measure health status in rheumatoid arthritis in non-English speaking patients: Validation of a Spanish version of the Health Assessment Questionnaire Disability Index (Spanish HAQ-DI). In Clin. Exp. Rheumatol.; 1993; 11, pp. 117–121. Available online: http://www.ncbi.nlm.nih.gov/pubmed/8508553 (accessed on 7 June 2025). [PubMed]
- The International Society for Clinical Densitometry (ISCD) (2019) Official Positions-Adult [Internet]. 2019. Available online: https://iscd.org/learn/official-positions/adult-positions/ (accessed on 7 June 2025).
- Hans, D.; Barthe, N.; Boutroy, S.; Pothuaud, L.; Winzenrieth, R.; Krieg, M.-A. Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: An experimental study on human cadaver vertebrae. J. Clin. Densitom. 2011, 14, 302–312. [Google Scholar] [CrossRef] [PubMed]
- Sepriano, A.; Kerschbaumer, A.; Bergstra, S.A.; Smolen, J.S.; van der Heijde, D.; Caporali, R.; Edwards, C.J.; Verschueren, P.; de Souza, S.; Pope, J.; et al. Safety of synthetic and biological DMARDs: A systematic review informing the 2022 EULAR recommendations. Ann. Rheum. Dis. 2023, 82, 107–118. [Google Scholar] [CrossRef] [PubMed]
- Fraenkel, L.; Bathon, J.M.; England, B.R.; St Clair, E.W.; Arayssi, T.; Carandang, K.; Deane, K.D.; Genovese, M.; Huston, K.K.; Kerr, G.; et al. 2021 American College of Rheumatology Guideline for the Treatment of Rheumatoid Arthritis. Arthritis Care Res. 2021, 73, 924–939. [Google Scholar] [CrossRef] [PubMed]
- Murdaca, G.; Negrini, S.; Magnani, O.; Penza, E.; Pellecchio, M.; Puppo, F. Impact of pharmacogenomics upon the therapeutic response to etanercept in psoriasis and psoriatic arthritis. Expert Opin. Drug Saf. 2017, 16, 1173–1179. [Google Scholar] [CrossRef] [PubMed]
- Wallace, B.I.; Lin, P.; Kamdar, N.; Noureldin, M.; Hayward, R.; Fox, D.A.; Curtis, J.R.; Saag, K.G.; Waljee, A.K. Patterns of glucocorticoid prescribing in RA: A retrospective cohort study. Semin. Arthritis Rheum. 2020, 50, 228–236. [Google Scholar] [CrossRef] [PubMed]
- Cutolo, M.; Shoenfeld, Y.; Bogdanos, D.P.; Gotelli, E.; Salvato, M.; Gunkl-Tóth, L.; Nagy, G. To treat or not to treat RA with glucocorticoids? A reheated debate. Autoimmun. Rev. 2024, 23, 103437. [Google Scholar] [CrossRef] [PubMed]
- Tavassoli, S.; Rajaei, A.; Emam, M.M.; Farsad, F. Evaluating the value-added of the trabecular bone score in patients with rheumatoid arthritis. Arch. Iran. Med. 2021, 24, 193–198. [Google Scholar] [CrossRef] [PubMed]
- Buehring, B.; Thomas, J.; Wittkämper, T.; Baraliakos, X.; Braun, J. Evaluation of the trabecular bone score (TBS) in routine clinical care of patients with inflammatory rheumatic and non-inflammatory diseases: Correlation with conventional bone mineral density measurement and prevalence of vertebral fractures. Z. Rheumatol. 2020, 79, 1067–1074. [Google Scholar] [CrossRef] [PubMed]
- Koumakis, E.; Avouac, J.; Winzenrieth, R.; Toth, E.; Payet, J.; Kahan, A.; Allanore, Y.; Cormier, C. Trabecular bone score in female patients with systemic sclerosis: Comparison with rheumatoid arthritis and influence of glucocorticoid exposure. J. Rheumatol. 2015, 42, 228–235. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.; Cho, S.K.; Kim, J.Y.; Choi, Y.Y.; Sung, Y.K. Association between trabecular bone score and risk factors for fractures in Korean female patients with rheumatoid arthritis. Mod. Rheumatol. 2016, 26, 540–545. [Google Scholar] [CrossRef] [PubMed]
- Omichi, Y.; Shinomiya, F.; Mima, N.; Hirose, J.; Enomoto, T.; Goto, T.; Nakano, S.; Enishi, T.; Morimoto, M.; Sairyo, K. Impact of Bone Mineral Density and Bone Structural Properties on Postmenopausal Women With Rheumatoid Arthritis in Japan: A Cross-Sectional Study. Cureus 2024, 16, e65056. [Google Scholar] [CrossRef] [PubMed]
- Bréban, S.; Briot, K.; Kolta, S.; Paternotte, S.; Ghazi, M.; Fechtenbaum, J.; Roux, C. Identification of Rheumatoid Arthritis Patients With Vertebral Fractures Using Bone Mineral Density and Trabecular Bone Score. J. Clin. Densitom. 2012, 15, 260–266. [Google Scholar] [CrossRef] [PubMed]
- Senosi, M.R.; Fathi, H.M.; Baki, N.M.A.; Zaki, O.; Magdy, A.M.; Gheita, T.A. Bone mineral density, vitamin D receptor (VDR) gene polymorphisms, fracture risk assessment (FRAX), and trabecular bone score (TBS) in rheumatoid arthritis patients: Connecting pieces of the puzzle. Clin. Rheumatol. 2022, 41, 1333–1342. [Google Scholar] [CrossRef] [PubMed]
- Ioniță-Radu, F.; Nicolau, I.N.; Petrache, O.G.; Groșeanu, M.L.; Bojincă, V.C.; Negru, M.M.; Bucurică, S.; Anghel, D. Correlation between TBS and homocysteine in RA patients on anti-TNF inhibitors. Life 2024, 14, 463. [Google Scholar] [CrossRef] [PubMed]
- Ruaro, B.; Casabella, A.; Molfetta, L.; Salton, F.; Confalonieri, P.; Confalonieri, M.; Bratella, E.; De Tanti, A.; Bruni, C. What Role Does Trabecular Bone Score Play in Chronic Inflammatory Rheumatic Diseases. Front. Med. 2020, 7, 600697. [Google Scholar] [CrossRef] [PubMed]
- Wiebe, E.; Huscher, D.; Schaumburg, D.; Palmowski, A.; Hermann, S.; Buttgereit, T.; Biesen, R.; Burmester, G.-R.; Palmowski, Y.; Boers, M.; et al. Optimising both disease control and glucocorticoid dosing is essential for bone protection in patients with rheumatic disease. Ann. Rheum. Dis. 2022, 81, 1313–1322. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Chen, F.; Liu, L.; Zhang, Q. Prevalence of osteoporosis in patients with diabetes mellitus: A systematic review and meta-analysis of observational studies. BMC Endocr. Disord. 2023, 23, 1. [Google Scholar] [CrossRef] [PubMed]
- Corrado, A.; Cici, D.; Rotondo, C.; Maruotti, N.; Cantatore, F.P. Molecular basis of bone aging. Int. J. Mol. Sci. 2020, 21, 3679. [Google Scholar] [CrossRef] [PubMed]
Variable | n = 203 |
---|---|
Age in years: mean ± SD | 58.9 ± 11.4 |
Menopause, n (%) | 169 (83) |
Sedentary lifestyle, n (%) | 136 (67) |
Smoking, n (%) | 21 (10) |
History of fragility fractures, n (%) | 17 (5.8) |
Diabetes Mellitus type 2, n (%) | 18 (9) |
Hypertension, n (%) | 86 (42) |
Overweight/obesity, n (%) | 145 (71) |
RA characteristics | |
Years of duration of RA: mean ± SD | 13.6 ± 9.7 |
Functional disability (HAQ-DI > 0.6), n (%) | 86 (42) |
Disease activity (DAS28-ESR ≥ 2.6), n (%) | 144 (71) |
Densitometry variables | |
Bone mineral density (BMD), gr/cm2: mean ± SD | 1.8 ± 0.3 |
Central DXA results | |
Normal BMD, n (%) | 52 (26) |
Osteopenia, n (%) | 74 (36) |
Osteoporosis, n (%) | 77 (38) |
Trabecular Bone quality | |
TBS L1–L4, index: mean ± SD | 1.301 ± 0.108 |
Normal bone quality, n (%) | 97 (48) |
Low bone quality, n (%) | 106 (52) |
Laboratory variables | |
Positive CRP (≥10 mg/L), n (%) | 88 (43) |
Elevated ESR (>20 mm/Hr), n (%) | 117 (57) |
Positive RF (≥12 Ul/mL), n (%) | 121 (60) |
Pharmacological treatment | |
Synthetic DMARDs, n (%) | 197 (97) |
Monotherapy, n (%) | 108 (53) |
Combination therapy, n (%) | 95 (47) |
Corticosteroid use, n (%) | 147 (72) |
Corticosteroid dose, mg/day: mean ± SD | 4.3 ± 3.2 |
Time of corticosteroid use, years: mean ± SD | 5.8 ± 7 |
Corticosteroid cumulative dose, g: mean ± SD | 35.6 ± 49.9 |
Variables | RA + Normal Bone Quality n = 97 | RA + Low Bone Quality n = 106 | p |
---|---|---|---|
Age, years: mean ± SD | 55.5 ± 10.5 | 61.9 ± 11.4 | <0.001 |
Menopause, n (%) | 73 (75) | 96 (90) | 0.004 |
Sedentary life style, n (%) | 65 (67) | 71 (67) | 0.99 |
Hypertension, n (%) | 33 (34) | 53 (50) | 0.02 |
Diabetes Mellitus, n (%) | 4 (4) | 14 (13) | 0.02 |
Smoking, n (%) | 5 (5) | 16 (15) | 0.02 |
Body mass index, kg/m2: mean ± SD | 27.6 ± 4.7 | 27.5 ± 3.7 | 0.09 |
Bone mineral density (BMD), gr/cm2 | 1.86 ± 0.29 | 1.77 ± 0.31 | 0.03 |
Normal BMD, n (%) | 34 (65) | 18 (35) | <0.001 |
Osteopenia, n (%) | 41 (55) | 33 (45) | |
Osteoporosis, n (%) | 22 (22) | 55 (52) | |
Disease duration, years | 12.1 ± 8 | 15.1 ± 11 | 0.02 |
Functional disability (HAQDI > 0.6) | 45 (47) | 41 (40) | 0.31 |
Disease activity (DAS28-ESR ≥ 2.6) | 72 (50) | 73 (50) | 0.52 |
Positive RF (≥12 Ul/mL), n (%) | 55 (56) | 66 (62) | 0.42 |
Synthetic DMARDs, n (%) | 96 (99) | 101 (95) | 0.21 |
Corticosteroid use, n (%) | 73 (75) | 74 (70) | 0.38 |
Corticosteroid dose, mg/day: mean ± SD | 4.6 ± 3.3 | 4.0 ± 3.1 | 0.15 |
Time of corticosteroid use, years: mean ± SD | 6.4 ± 7.5 | 5.4 ± 6.4 | 0.30 |
Corticosteroid cumulative dose, g: mean ± SD | 40.4 ± 57.9 | 31.2 ± 41 | 0.19 |
Variables (n = 203) | Enter Method | Forward Method (Stepwise) | ||||
---|---|---|---|---|---|---|
OR | 95% CI | p | OR | 95% CI | p | |
Age (years) | 1.05 | (1.01–1.09) | 0.02 | 1.05 | (1.02–1.08) | <0.001 |
Smoking | 3.380 | (1.08–10.54) | 0.035 | Not in the model | - | - |
Menopause | 1.11 | (0.37–3.37) | 0.85 | Not in the model | - | - |
Diabetes mellitus | 3.20 | (0.94–10.85) | 0.06 | 3.30 | (1.03–10.60) | 0.045 |
Hypertension | 1.38 | (0.72–2.66) | 0.33 | Not in the model | - | - |
Body mass index | 0.99 | (0.92–1.06) | 0.78 | Not in the model | - | - |
Duration of RA | 1.02 | (0.99–1.06) | 0.21 | Not in the model | - | - |
Functional disability | 1.35 | (0.69–2.66) | 0.38 | Not in the model | - | - |
Disease activity | 1.54 | (0.26–1.15) | 0.11 | Not in the model | - | - |
Corticosteroid use | 1.24 | (0.62–2.52) | 0.54 | Not in the model | - | - |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gomez-Camarena, J.J.; Ramirez-Villafaña, M.; Gomez-Ramirez, E.E.; Gonzalez-Ponce, F.; Alcaraz-Lopez, M.F.; Ponce-Guarneros, J.M.; Vazquez-Villegas, M.L.; Rodriguez-Santillan, L.R.; Rodriguez-Jimenez, N.A.; Saldaña-Cruz, A.M.; et al. Corticosteroids and Vertebral Trabecular Bone Quality in Women with Rheumatoid Arthritis. J. Clin. Med. 2025, 14, 5223. https://doi.org/10.3390/jcm14155223
Gomez-Camarena JJ, Ramirez-Villafaña M, Gomez-Ramirez EE, Gonzalez-Ponce F, Alcaraz-Lopez MF, Ponce-Guarneros JM, Vazquez-Villegas ML, Rodriguez-Santillan LR, Rodriguez-Jimenez NA, Saldaña-Cruz AM, et al. Corticosteroids and Vertebral Trabecular Bone Quality in Women with Rheumatoid Arthritis. Journal of Clinical Medicine. 2025; 14(15):5223. https://doi.org/10.3390/jcm14155223
Chicago/Turabian StyleGomez-Camarena, Jose Jorge, Melissa Ramirez-Villafaña, Eli Efrain Gomez-Ramirez, Fabiola Gonzalez-Ponce, Miriam Fabiola Alcaraz-Lopez, Juan Manuel Ponce-Guarneros, Maria Luisa Vazquez-Villegas, Larissa Renne Rodriguez-Santillan, Norma Alejandra Rodriguez-Jimenez, Ana Miriam Saldaña-Cruz, and et al. 2025. "Corticosteroids and Vertebral Trabecular Bone Quality in Women with Rheumatoid Arthritis" Journal of Clinical Medicine 14, no. 15: 5223. https://doi.org/10.3390/jcm14155223
APA StyleGomez-Camarena, J. J., Ramirez-Villafaña, M., Gomez-Ramirez, E. E., Gonzalez-Ponce, F., Alcaraz-Lopez, M. F., Ponce-Guarneros, J. M., Vazquez-Villegas, M. L., Rodriguez-Santillan, L. R., Rodriguez-Jimenez, N. A., Saldaña-Cruz, A. M., Cardona-Muñoz, E. G., Totsuka-Sutto, S. E., Gamez-Nava, J. I., & Gonzalez-Lopez, L. (2025). Corticosteroids and Vertebral Trabecular Bone Quality in Women with Rheumatoid Arthritis. Journal of Clinical Medicine, 14(15), 5223. https://doi.org/10.3390/jcm14155223