The High Prevalence of Sarcopenia in Rheumatoid Arthritis in the Korean Population: A Nationwide Cross-Sectional Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Setting
2.2. Participants
2.3. Main Variables and Covariates
2.4. Subgroup Analysis
2.5. Statistical Analysis
3. Results
3.1. Baseline Characteristics
3.2. Association between RA and Sarcopenia
3.3. Association between RA and Sarcopenia in Subgroup Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rosenberg, I.H. Summary Comments. Am. J. Clin. Nutr. 1989, 50, 1231–1233. [Google Scholar] [CrossRef]
- Liguori, I.; Russo, G.; Aran, L.; Bulli, G.; Curcio, F.; Della-Morte, D.; Gargiulo, G.; Testa, G.; Cacciatore, F.; Bonaduce, D.; et al. Sarcopenia: Assessment of disease burden and strategies to improve outcomes. Clin. Interv. Aging 2018, 13, 913–927. [Google Scholar] [CrossRef] [PubMed]
- Noack, M.; Miossec, P. Selected cytokine pathways in rheumatoid arthritis. Semin. Immunopathol. 2017, 39, 365–383. [Google Scholar] [CrossRef] [PubMed]
- Harris, E.D., Jr. Rheumatoid arthritis. Pathophysiology and implications for therapy. N. Engl. J. Med. 1990, 322, 1277–1289. [Google Scholar] [PubMed]
- Rudrappa, S.S.; Wilkinson, D.J.; Greenhaff, P.L.; Smith, K.; Idris, I.; Atherton, P.J. Human skeletal muscle disuse atrophy: Effects on muscle protein synthesis, breakdown, and insulin resistance-a qualitative review. Front. Physiol. 2016, 7, 361. [Google Scholar] [CrossRef]
- Helliwell, P.; Jackson, S. Relationship between weakness and muscle wasting in rheumatoid arthritis. Ann. Rheum. Dis. 1994, 53, 726–728. [Google Scholar] [CrossRef]
- Roubenoff, R.; Roubenoff, R.A.; Cannon, J.G.; Kehayias, J.J.; Zhuang, H.; Dawson-Hughes, B.; Dinarello, C.A.; Rosenberg, I.H. Rheumatoid cachexia: Cytokine-driven hypermetabolism accompanying reduced body cell mass in chronic inflammation. J. Clin. Investig. 1994, 93, 2379–2386. [Google Scholar] [CrossRef]
- Torii, M.; Hashimoto, M.; Hanai, A.; Fujii, T.; Furu, M.; Ito, H.; Uozumi, R.; Hamaguchi, M.; Terao, C.; Yamamoto, W.; et al. Prevalence and factors associated with sarcopenia in patients with rheumatoid arthritis. Mod. Rheumatol. 2019, 29, 589–595. [Google Scholar] [CrossRef]
- Vlietstra, L.; Stebbings, S.; Meredith-Jones, K.; Abbott, J.H.; Treharne, G.J.; Waters, D.L. Sarcopenia in osteoarthritis and rheumatoid arthritis: The association with self-reported fatigue, physical function and obesity. PLoS ONE 2019, 14, e0217462. [Google Scholar] [CrossRef]
- Doğan, S.C.; Hizmetli, S.; Hayta, E.; Kaptanoğlu, E.; Erselcan, T.; Güler, E. Sarcopenia in women with rheumatoid arthritis. Eur. J. Rheumatol. 2015, 2, 57–61. [Google Scholar] [CrossRef]
- Ngeuleu, A.; Allali, F.; Medrare, L.; Madhi, A.; Rkain, K.; Hajjaj-Hassouni, N. Sarcopenia in rheumatoid arthritis: Prevalence, influence of disease activity and associated factors. Rheumatol. Int. 2017, 37, 1015–1020. [Google Scholar] [CrossRef]
- Targowski, T. Sarcopaenia and rheumatoid arthritis. Reumatologia 2017, 55, 84–87. [Google Scholar] [CrossRef]
- Tsekoura, M.; Kastrinis, A.; Katsoulaki, M.; Billis, E.; Gliatis, J. Sarcopenia and its impact on quality of life. Adv. Exp. Med. Biol. 2017, 987, 213–218. [Google Scholar]
- Choo, Y.J.; Chang, M.C. Prevalence of sarcopenia among the elderly in Korea: A meta-analysis. J. Prev. Med. Public Health 2021, 54, 96–102. [Google Scholar] [CrossRef]
- Sung, Y.K.; Yoshida, K.; Prince, F.H.M.; Frits, M.L.; Cho, S.K.; Choe, J.Y.; Lee, H.S.; Lee, J.; Lee, S.S.; Yoo, D.H.; et al. Prevalence and predictors for sustained remission in rheumatoid arthritis. PLoS ONE 2019, 14, e0214981. [Google Scholar]
- Won, S.; Cho, S.K. Update on the prevalence and incidence of rheumatoid arthritis in Korea and an analysis of medical care and drug utilization. Rheumatol. Int. 2018, 38, 649–656. [Google Scholar] [CrossRef]
- Lee, J.H.; Kim, S.; Kim, M.K.; Yun, B.H.; Cho, S.; Choi, Y.S.; Lee, B.S.; Seo, S.K. Relationships between 25(OH)D concentration, sarcopenia and HOMA-IR in postmenopausal Korean women. Climacteric 2018, 21, 40–46. [Google Scholar] [CrossRef]
- Heymsfield, S.B.; Smith, R.; Aulet, M.; Bensen, B.; Lichtman, S.; Wang, J.; Pierson, R.N., Jr. Appendicular skeletal muscle mass: Measurement by dual-photon absorptiometry. Am. J. Clin. Nutr. 1990, 52, 214–218. [Google Scholar] [CrossRef]
- Li, T.H.; Chang, Y.S.; Liu, C.W.; Su, C.F.; Tsai, H.C.; Tsao, Y.P.; Liao, H.T.; Chen, M.H.; Chuang, C.C.; Yang, Y.Y.; et al. The prevalence and risk factors of sarcopenia in rheumatoid arthritis patients: A systematic review and meta-regression analysis. Semin. Arthritis Rheum. 2020, 51, 236–245. [Google Scholar] [CrossRef]
- Hong, S.; Oh, H.J.; Choi, H.; Kim, J.G.; Lim, S.K.; Kim, E.K.; Pyo, E.Y.; Oh, K.; Kim, Y.T.; Wilson, K.; et al. Characteristics of body fat, body fat percentage and other body composition for Koreans from KNHANES IV. J. Korean Med. Sci. 2011, 26, 1599–1605. [Google Scholar] [CrossRef]
- Messier, V.; Rabasa-Lhoret, R.; Barbat-Artigas, S.; Elisha, B.; Karelis, A.D.; Aubertin-Leheudre, M. Menopause and sarcopenia: A potential role for sex hormones. Maturitas 2011, 68, 331–336. [Google Scholar] [CrossRef] [PubMed]
- Anderson, L.J.; Liu, H.; Garcia, J.M. Sex differences in muscle wasting. Adv. Exp. Med. Biol. 2017, 1043, 153–197. [Google Scholar] [PubMed]
- Kim, S.; Park, S. Association between age at natural menopause and prevalence of obesity, hypertension, diabetes, and hypercholesterolemia. Korean Public Health Res. 2021, 47, 1–9. [Google Scholar]
- Pahor, M.; Manini, T.; Cesari, M. Sarcopenia: Clinical evaluation, biological markers and other evaluation tools. J. Nutr. Health Aging 2009, 13, 724–728. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.M.; Jang, H.C.; Lim, S. Differences among skeletal muscle mass indices derived from height-, weight-, and body mass index-adjusted models in assessing sarcopenia. Korean J. Int. Med. 2016, 31, 643–650. [Google Scholar] [CrossRef]
- Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 16–31. [Google Scholar] [CrossRef]
- Tekgoz, E.; Colak, S.; Ozalp Ates, F.S.; Sonaeren, I.; Yilmaz, S.; Cinar, M. Sarcopenia in rheumatoid arthritis: Is it a common manifestation? Int. J. Rheum. Dis. 2020, 23, 1685–1691. [Google Scholar] [CrossRef]
- Bian, A.L.; Hu, H.Y.; Rong, Y.D.; Wang, J.; Wang, J.X.; Zhou, X.Z. A study on relationship between elderly sarcopenia and inflammatory factors IL-6 and TNF-α. Eur. J. Med. Res. 2017, 22, 25. [Google Scholar] [CrossRef]
- Cooper, C.; Fielding, R.; Visser, M.; van Loon, L.J.; Rolland, Y.; Orwoll, E.; Reid, K.; Boonen, S.; Dere, W.; Epstein, S.; et al. Tools in the assessment of sarcopenia. Calcif. Tissue Int. 2013, 93, 201–210. [Google Scholar] [CrossRef]
- Aloia, J.F.; McGowan, D.M.; Vaswani, A.N.; Ross, P.; Cohn, S.H. Relationship of menopause to skeletal and muscle mass. Am. J. Clin. Nutr. 1991, 53, 1378–1383. [Google Scholar] [CrossRef]
- Rolland, Y.M.; Perry, H.M.; Patrick, P.; Banks, W.A.; Morley, J.E. Loss of appendicular muscle mass and loss of muscle strength in young menopausal women. J. Gerontol. A Biol. Sci. Med. Sci. 2007, 62, 330–335. [Google Scholar] [CrossRef]
- Chianca, V.; Albino, D.; Messina, C.; Gitto, S.; Ruffo, G.; Guarino, S.; Del Grande, F.; Sconfienza, L.M. Sarcopenia: Imaging assessment and clinical application. Abdom. Radiol. 2022, 47, 3205–3216. [Google Scholar] [CrossRef]
Men (n = 7389) | Women (n = 9798) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
RA (n = 26) | Non-RA (n = 7363) | RA (n = 130) | Non-RA (n = 9668) | |||||||
n | % | n | % | p | n | % | n | % | p | |
Age (in years) | 67.54 ± 12.281 | 48.95 ± 16.012 | 0.001 | 61.92 ± 13.273 | 48.62 ± 16.071 | 0.001 | ||||
Obesity | 0.087 | 0.394 | ||||||||
Underweight | 0 | 0.0 | 241 | 3.3 | 7 | 5.4 | 534 | 5.5 | ||
Normal weight | 13 | 50.0 | 4534 | 61.6 | 91 | 70.0 | 6375 | 65.9 | ||
Overweight | 13 | 50.0 | 2588 | 35.1 | 32 | 24.6 | 2759 | 28.5 | ||
Menopause | - | 0.001 | ||||||||
Yes | - | - | - | - | 105 | 80.8 | 4099 | 42.4 | ||
No | - | - | - | - | 25 | 19.2 | 5569 | 57.6 | ||
Hypertension | 0.041 | 0.001 | ||||||||
Normal | 8 | 30.8 | 2484 | 33.7 | 32 | 24.6 | 5029 | 52.0 | ||
Pre-hypertension | 3 | 11.5 | 2220 | 30.2 | 35 | 26.9 | 1967 | 20.3 | ||
Hypertension | 15 | 57.7 | 2659 | 36.1 | 63 | 48.5 | 2672 | 27.6 | ||
Diabetes mellitus | 0.000 | 0.036 | ||||||||
Normal | 15 | 57.7 | 4867 | 66.1 | 90 | 69.2 | 7386 | 76.4 | ||
Impaired fasting glucose | 2 | 7.7 | 1683 | 22.9 | 21 | 16.2 | 1464 | 15.1 | ||
Diabetes mellitus | 9 | 34.6 | 813 | 11.0 | 19 | 14.6 | 818 | 8.5 | ||
Dyslipidemia | 0.604 | 0.051 | ||||||||
Normal | 10 | 38.5 | 2477 | 33.6 | 25 | 19.2 | 2597 | 26.9 | ||
Dyslipidemia | 16 | 61.5 | 4886 | 66.4 | 105 | 80.8 | 7071 | 73.1 | ||
Alcohol consumption | 0.001 | 0.000 | ||||||||
None | 16 | 61.5 | 1857 | 25.2 | 101 | 77.7 | 5881 | 60.8 | ||
Moderate | 8 | 30.8 | 3981 | 54.1 | 28 | 21.5 | 3378 | 34.9 | ||
Heavy | 2 | 7.7 | 1525 | 20.7 | 1 | 0.8 | 409 | 4.2 | ||
Smoking status | 0.039 | 0.779 | ||||||||
Never | 4 | 15.4 | 1406 | 19.1 | 113 | 86.9 | 8592 | 88.9 | ||
Past | 14 | 53.8 | 2803 | 38.1 | 8 | 6.2 | 518 | 5.4 | ||
Current | 8 | 30.8 | 3154 | 42.8 | 9 | 6.9 | 558 | 5.8 | ||
Household income | 0.001 | 0.001 | ||||||||
Lowest | 15 | 57.7 | 1281 | 17.4 | 57 | 43.8 | 2020 | 20.9 | ||
Lower middle | 5 | 19.2 | 1848 | 25.1 | 30 | 23.1 | 2451 | 25.4 | ||
Upper middle | 1 | 3.8 | 2141 | 29.1 | 26 | 20.0 | 2631 | 27.2 | ||
Highest | 5 | 19.2 | 2092 | 28.4 | 17 | 13.1 | 2566 | 26.5 | ||
Education | 0.001 | 0.000 | ||||||||
Primary school or lower | 13 | 50.0 | 1315 | 17.9 | 89 | 68.5 | 3051 | 31.6 | ||
Middle school | 5 | 19.2 | 913 | 12.4 | 19 | 14.6 | 1008 | 10.4 | ||
High school | 6 | 23.1 | 2658 | 36.1 | 13 | 10.0 | 3238 | 33.5 | ||
University or higher | 2 | 7.7 | 2477 | 33.6 | 9 | 6.9 | 2371 | 24.5 | ||
Sarcopenia | 0.001 | 0.053 | ||||||||
Absent | 10 | 38.5 | 5683 | 77.2 | 88 | 67.7 | 7260 | 75.1 | ||
Present | 16 | 61.5 | 1680 | 22.8 | 42 | 32.3 | 2408 | 24.9 |
Men | Women | |||||
---|---|---|---|---|---|---|
OR | 95% CI | p | OR | 95% CI | p | |
Crude | 5.41 | 2.45–11.95 | 0.001 | 1.44 | 0.99–2.08 | 0.054 |
Model I | 2.95 | 1.25–6.97 | 0.014 | 1.32 | 0.88–1.97 | 0.183 |
Model II | 3.15 | 1.25–6.97 | 0.010 | 1.32 | 0.88–1.98 | 0.174 |
Model III | 3.02 | 1.26–7.20 | 0.013 | 1.32 | 0.88–1.97 | 0.184 |
Model IV | 3.11 | 1.29–7.46 | 0.011 | 1.36 | 0.91–2.04 | 0.139 |
Men (n = 2399) | Women (n = 3239) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Age < 40 Years | RA (n = 1) | Non-RA (n = 2398) | RA (n = 11) | Non-RA (n = 3228) | ||||||
n | % | n | % | p | n | % | n | % | p | |
Sarcopenia | 0.153 | 0.713 | ||||||||
Absent | 0 | 0 | 2031 | 84.7% | 10 | 90.9% | 2743 | 85.0% | ||
Present | 1 | 100.0% | 367 | 15.3% | 1 | 9.1% | 485 | 15.0% | ||
Men (n = 2802) | Women (n = 3760) | |||||||||
40 ≤ Age < 59 years | RA (n = 4) | Non-RA (n = 2798) | RA (n = 31) | Non-RA (n = 3729) | ||||||
n | % | n | % | p | n | % | n | % | p | |
Sarcopenia | 0.849 | 0.039 | ||||||||
Absent | 3 | 75.0% | 2207 | 78.9% | 18 | 58.1% | 2772 | 74.3% | ||
Present | 1 | 25.0% | 591 | 21.1% | 13 | 41.9% | 957 | 25.7% | ||
Men (n = 2188) | Women (n = 2799) | |||||||||
Age ≥ 60 years | RA (n = 21) | Non-RA (n = 2167) | RA (n = 88) | Non-RA (n = 2711) | ||||||
n | % | n | % | p | n | % | n | % | p | |
Sarcopenia | 0.001 | 0.462 | ||||||||
Absent | 7 | 33.3% | 1445 | 66.7% | 60 | 68.2% | 1745 | 64.4% | ||
Present | 14 | 66.7% | 722 | 33.3% | 28 | 31.8% | 966 | 35.6% |
Men | Women | |||||
---|---|---|---|---|---|---|
OR | 95% CI | p | OR | 95% CI | p | |
All age | 3.11 | 1.29–7.46 | 0.011 | 1.36 | 0.91–2.04 | 0.139 |
Age < 40 years | - | 0.56 | 0.07–4.82 | 0.598 | ||
40 ≤ Age < 59 years | 0.79 | 0.08–7.97 | 0.839 | 2.29 | 1.05–5.00 | 0.038 |
Age ≥ 60 years | 4.12 | 1.48–11.44 | 0.007 | 1.30 | 0.78–2.16 | 0.317 |
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Kim, D.; Lee, Y.J.; Song, E.S.; Kim, A.; Bang, C.H.; Jung, J.H. The High Prevalence of Sarcopenia in Rheumatoid Arthritis in the Korean Population: A Nationwide Cross-Sectional Study. Healthcare 2023, 11, 1401. https://doi.org/10.3390/healthcare11101401
Kim D, Lee YJ, Song ES, Kim A, Bang CH, Jung JH. The High Prevalence of Sarcopenia in Rheumatoid Arthritis in the Korean Population: A Nationwide Cross-Sectional Study. Healthcare. 2023; 11(10):1401. https://doi.org/10.3390/healthcare11101401
Chicago/Turabian StyleKim, Dongwoo, Yu Jin Lee, Eui Seop Song, Ahreum Kim, Cho Hee Bang, and Jae Hyun Jung. 2023. "The High Prevalence of Sarcopenia in Rheumatoid Arthritis in the Korean Population: A Nationwide Cross-Sectional Study" Healthcare 11, no. 10: 1401. https://doi.org/10.3390/healthcare11101401
APA StyleKim, D., Lee, Y. J., Song, E. S., Kim, A., Bang, C. H., & Jung, J. H. (2023). The High Prevalence of Sarcopenia in Rheumatoid Arthritis in the Korean Population: A Nationwide Cross-Sectional Study. Healthcare, 11(10), 1401. https://doi.org/10.3390/healthcare11101401