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The association between muscle indicators and bone mass density and related risk factors in the diabetic elderly population: Bushehr Elderly Health (BEH) Program

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Abstract

Background

Loss of muscle mass and strength and bone mass density are complications of the aging process. Studies show that the prevalence of sarcopenia and osteoporosis may be higher in patients with diabetes. Therefore, this study was aimed to investigate the relationship between muscle mass and strength indices and bone mass density in diabetic elderly.

Materials and methods

This cross-sectional study was conducted based on the data collected during the Bushehr Elderly Health (BEH) Program, stage II. Diabetes was defined as FPG ≥ 126 mg/dl or HbA1C ≥ 6.5 or taking anti-diabetic medication. Dual x-ray absorptiometry (DXA, Discovery WI, Hologic Inc, USA) was used to measure bone mineral density, fat mass, trabecular bone score (TBS) and muscle mass. Muscle strength was measured by grip strength.

Osteoporosis was defined as the bone mineral density of ≥ 2.5 standard deviations (SD) below the average value of young normal adults (T-score of ≤ -2.5 SD) in the femoral neck, or lumbar spine (L1-L4) or total hip. To determine the relationship between skeletal muscle index (SMI) and muscle strength on bone status in a continuous scale was used from linear regression. To estimate the effect of SMI and muscle strength on osteoporosis was used from modified Poisson regression for analysis.

Results

This study included 759 diabetic elderly with a mean age of 68.6 years and 56.9% of them were women. Skeletal muscle index (SMI) was related to all sites of BMDs and TBS L1-L4 after adjusted in full models (P-value < 0.001). The largest coefficients were observed for BMD L1-L4 in all models (β: 0.043 g/cm2; 95% CI: 0.030–0.057 in full model). Muscle strength was also associated with BMDs and TBS. Only, in model 2 (adjustments for age and sex effect), there was no significant relationship between muscle strength and BMD L1-L4 and TBS L1-L4. The strongest associations were observed for the total hip BMD and muscle strength (β: 0.034 g/cm2; 95% CI: 0.022- 0.046 in full model). Also, increased SMI and muscle strength was associated with decreased osteoporosis in crude and adjusted models (P < 0.001).

Conclusions

In this study, it was revealed that the reduction of SMI in elderly patients with diabetes was significantly associated with decreased BMD and TBS. The muscle strength was also associated with BMD and TBS. So, muscle strength and muscle mass should be measured separately ever since both are independently associated with BMD and TBS. Muscle strength and muscle mass were negatively associated with osteoporosis in older people with diabetes. Thus, we should pay more attention to muscle strength training in older people with diabetes, particularly in osteoporotic patients.

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References

  1. He W, Goodkind D, Kowal P. An aging world: 2015. United States Census Bureau. 2016. http://www.census.gov/library/publications/2016/demo/P95-16-1.html.

  2. Heidari ME, Naghibi Irvani SS, Dalvand P, Khadem M, Eskandari F, Torabi F, Shahsavari H. Prevalence of depression in older people with hip fracture: A systematic review and meta-analysis. Int J Orthop Trauma Nurs. 2021;40:100813.

  3. Public relations and International Cooperation. Selected Findings of National Population and Housing Census, 2012. Tehran: Statistical Center of Iran; 2011. p. 27.

    Google Scholar 

  4. Ghazanchaei E, Khorasani-Zavareh D , Aghazadeh-Attari J, Mohebbi I. Establishing the status of patients with non-communicable diseases in disaster: A systematic review. Disaster Med Public Health Prep. 2021;1–8. https://doi.org/10.1017/dmp.2020.364.

  5. Khamseh ME, Ansari M, Malek M, Shafiee G, Baradaran H. Effects of a structured self-monitoring of blood glucose method on patient self-management behavior and metabolic outcomes in type 2 diabetes mellitus. J Diabetes Sci Technol. 2011;5(2):388–93.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Fahimfar N, Noorali S, Yousefi S, Gharibzadeh S, Shafiee G, Panahi N, et al. Prevalence of osteoporosis among the elderly population of Iran. Arch Osteoporos. 2021;16(1):16.

    Article  PubMed  Google Scholar 

  7. Zhang J, Dennison E, Prieto-Alhambra D. Osteoporosis epidemiology using international cohorts. Curr Opin Rheumatol. 2020;32(4):387–93.

    Article  PubMed  Google Scholar 

  8. Hemmati F, Sarokhani D, Sayehmiri K, Motadayen M. Prevalence of osteoporosis in postmenopausal women in Iran: A systematic review and meta-analysis. Iran J Obstetrics Gynecol Infertility. 2018;21(3):90–102.

    Google Scholar 

  9. Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet. 2019;393(10191):2636–46.

    Article  PubMed  Google Scholar 

  10. Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R. Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. 2017;16:21.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Shafiee G, Heshmat R, Ostovar A, Nabipour I, Larijani B. Sarcopenia disease in Iran: an overview. J Diabetes Metab Disord. 2019;18(2):665–74.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Shafiee G, Heshmat R, Ostovar A, Khatami F, Fahimfar N, Arzaghi SM, et al. Comparison of EWGSOP-1and EWGSOP-2 diagnostic criteria on prevalence of and risk factors for sarcopenia among Iranian older people: the Bushehr Elderly Health (BEH) program. J Diabetes Metab Disord. 2020;19(2):727–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Janssen I. The epidemiology of sarcopenia. Clin Geriatr Med. 2011;27(3):355–63.

    Article  PubMed  Google Scholar 

  14. Edwards M, Dennison E, Sayer AA, Fielding R, Cooper C. Osteoporosis and sarcopenia in older age. Bone. 2015;80:126–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hunter GR, Plaisance EP, Fisher G. Weight loss and bone mineral density. Curr Opin Endocrinol Diabetes Obes. 2014;21(5):358.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jiang BC, Villareal DT. Weight loss-induced reduction of bone mineral density in older adults with obesity. J Nutr Gerontol Geriatr. 2019;38(1):100–14.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Fan W. Epidemiology in diabetes mellitus and cardiovascular disease. Cardiovasc Endocrinol. 2017;6(1):8.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Cho N, Shaw J, Karuranga S, Huang Y, da Rocha FJ, Ohlrogge A, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271–81.

    Article  CAS  PubMed  Google Scholar 

  19. Ogurtsova K, da Rocha FJ, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40–50.

    Article  CAS  PubMed  Google Scholar 

  20. Esteghamati A, Gouya MM, Abbasi M, Delavari A, Alikhani S, Alaedini F, et al. Prevalence of diabetes and impaired fasting glucose in the adult population of Iran: National Survey of Risk Factors for Non-Communicable Diseases of Iran. Diabetes Care. 2008;31(1):96–8.

    Article  PubMed  Google Scholar 

  21. Sahebkar M, Heidarian Miri H, Noormohammadpour P, Akrami R, Mansournia N, Tavana B, et al. Prevalence and correlates of low physical activity in the Iranian population: national survey on non-communicable diseases in 2011. Scand J Med Sci Sports. 2018;28(8):1916–24.

    Article  CAS  PubMed  Google Scholar 

  22. Shafiee G, Nasli-Esfahani E, Bandarian F, Peimani M, Yazdizadeh B, Razi F, et al. Iran Diabetes Research Roadmap (IDRR): the study protocol. J Diabetes Metab Disord. 2016;15:58.

    Article  PubMed  PubMed Central  Google Scholar 

  23. McKee A, Morley JE, Matsumoto AM, Vinik A. Sarcopenia: an endocrine disorder? Endocr Pract. 2017;23(9):1143–52.

    Article  Google Scholar 

  24. Morley JE. Diabetes, sarcopenia, and frailty. Clin Geriatr Med. 2008;24(3):455–69.

    Article  PubMed  Google Scholar 

  25. Morley JE. Hormones and sarcopenia. Curr Pharm Des. 2017;23(30):4484–92.

    Article  CAS  PubMed  Google Scholar 

  26. Ostovar A, Nabipour I, Larijani B, Heshmat R, Darabi H, Vahdat K, et al. Bushehr Elderly Health (BEH) Programme, phase I (cardiovascular system). BMJ Open. 2015;5(12):e009597.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Shafiee G, Ostovar A, Heshmat R, Darabi H, Sharifi F, Raeisi A, et al. Bushehr Elderly Health (BEH) programme: study protocol and design of musculoskeletal system and cognitive function (stage II). BMJ Open. 2017;7(8):e013606.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 2003;26 Suppl 1:S5–20.

  29. Aadahl M, Jorgensen T. Validation of a new self-report instrument for measuring physical activity. Med Sci Sports Exerc. 2003;35(7):1196–202.

    Article  PubMed  Google Scholar 

  30. Cruz-Jentoft A, European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis. Report of the European Workign Group on Sarcopenia in Older People. Age Ageing. 2010;39:412–23.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2018;48(1):16–31.

    Article  PubMed Central  Google Scholar 

  32. Hill KD, Farrier K, Russell M, Burton E. Dysmobility syndrome: current perspectives. Clin Interv Aging. 2017;12:145–52.

    Article  PubMed  PubMed Central  Google Scholar 

  33. McNutt L-A, Wu C, Xue X, Hafner JP. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am J Epidemiol. 2003;157(10):940–3.

    Article  PubMed  Google Scholar 

  34. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159(7):702–6.

    Article  PubMed  Google Scholar 

  35. Epprecht C, Guégan D, Veiga A, Correa da Rosa J. Variable selection and forecasting via automated methods for linear models: LASSO/adaLASSO and Autometrics. Communications in Statistics - Simulation and Computation. 2021;50(1):103–122.

  36. Fu WJ. Penalized regressions: the bridge versus the lasso. J Comput Graph Stat. 1998;7(3):397–416.

    Google Scholar 

  37. Xie Y, He Z, Tu W, Yu Z. Variable selection for joint models with time-varying coefficients. Stat Methods Med Res. 2020;29(1):309–322.

  38. Zou H, Zhang HH. On the adaptive elastic-net with a diverging number of parameters. Ann Stat. 2009;37(4):1733.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ogutu JO, Schulz-Streeck T, Piepho H-P. Genomic selection using regularized linear regression models: ridge regression, lasso, elastic net and their extensions. BMC Proc. 2012;6 Suppl 2(Suppl 2):S10.

  40. Sarodnik C, Bours S, Schaper N, Van den Bergh J, Van Geel T. The risks of sarcopenia, falls and fractures in patients with type 2 diabetes mellitus. Maturitas. 2018;109:70–7.

    Article  CAS  PubMed  Google Scholar 

  41. Szulc P, Beck TJ, Marchand F, Delmas PD. Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men—the MINOS study. J Bone Miner Res. 2005;20(5):721–9.

    Article  PubMed  Google Scholar 

  42. Sazlina S-G, Lee PY, Chan YM, Hamid MSA, Tan NC. The prevalence and factors associated with sarcopenia among community living elderly with type 2 diabetes mellitus in primary care clinics in Malaysia. PLoS One. 2020;15(5):e0233299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bonewald L. Use it or lose it to age: a review of bone and muscle communication. Bone. 2019;120:212–8.

    Article  PubMed  Google Scholar 

  44. Sanches CP, Vianna AGD, de Carvalho BF. The impact of type 2 diabetes on bone metabolism. Diabetol Metab Syndr. 2017;9(1):1–7.

    Article  Google Scholar 

  45. Di Monaco M, Castiglioni C, Di Monaco R, Tappero R. Association between low lean mass and low bone mineral density in 653 women with hip fracture: does the definition of low lean mass matter? Aging Clin Exp Res. 2017;29(6):1271–6.

    Article  PubMed  Google Scholar 

  46. Jang S-Y, Park J, Ryu S-Y, Choi S-W. Low muscle mass is associated with osteoporosis: a nationwide population-based study. Maturitas. 2020;133:54–9.

    Article  PubMed  Google Scholar 

  47. Kim KM, Lim S, Oh TJ, Moon JH, Choi SH, Lim JY, et al. Longitudinal changes in muscle mass and strength, and bone mass in older adults: gender-specific associations between muscle and bone losses. J Gerontol Ser A. 2018;73(8):1062–9.

    Article  CAS  Google Scholar 

  48. Leslie WD, Krieg M-A, Hans D, Program MBD. Clinical factors associated with trabecular bone score. J Clin Densitom. 2013;16(3):374–9.

    Article  PubMed  Google Scholar 

  49. Hayashi F, Kaibori M, Sakaguchi T, Matsui K, Ishizaki M, Kwon AH, et al. Loss of skeletal muscle mass in patients with chronic liver disease is related to decrease in bone mineral density and exercise tolerance. Hepatol Res. 2018;48(5):345–54.

    Article  CAS  PubMed  Google Scholar 

  50. Compston JE, Flahive J, Hosmer DW, Watts NB, Siris ES, Silverman S, et al. Relationship of weight, height, and body mass index with fracture risk at different sites in postmenopausal women: the Global Longitudinal study of Osteoporosis in Women (GLOW). J Bone Miner Res. 2014;29(2):487–93.

    Article  PubMed  Google Scholar 

  51. Kim Y, Lee J, Park J. Association between bone mineral density and knee osteoarthritis in Koreans: the Fourth and Fifth Korea National Health and Nutrition Examination Surveys. Osteoarthritis Cartilage. 2018;26(11):1511–7.

    Article  CAS  PubMed  Google Scholar 

  52. Rhodes E, Martin A, Taunton J, Donnelly M, Warren J, Elliot J. Effects of one year of resistance training on the relation between muscular strength and bone density in elderly women. Br J Sports Med. 2000;34(1):18–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Krakauer NY, Krakauer JC. Association of Body Shape Index (ABSI) with Hand Grip Strength. Int J Environ Res Public Health. 2020;17(18):6797.

    Article  PubMed Central  Google Scholar 

  54. Cetinus E, Buyukbese MA, Uzel M, Ekerbicer H, Karaoguz A. Hand grip strength in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2005;70(3):278–86.

    Article  PubMed  Google Scholar 

  55. Yz Li, Hf Z, Sq C, Ck L, Pw W, Ls Y, et al. Low grip strength is a strong risk factor of osteoporosis in postmenopausal women. Orthop Surg. 2018;10(1):17–22.

    Article  Google Scholar 

  56. Kaya A, Ozgocmen S, Ardicoglu O, Kamanli A, Gudul H. Relationship between grip strength and hand bone mineral density in healthy adults. Arch Med Res. 2005;36(5):603–6.

    Article  PubMed  Google Scholar 

  57. Dixon W, Lunt M, Pye S, Reeve J, Felsenberg D, Silman A, et al. Low grip strength is associated with bone mineral density and vertebral fracture in women. Rheumatology. 2005;44(5):642–6.

    Article  CAS  PubMed  Google Scholar 

  58. Bayramoğlu M, Sözay S, Karataş M, Kılınç Ş. Relationships between muscle strength and bone mineral density of three body regions in sedentary postmenopausal women. Rheumatol Int. 2005;25(7):513–7.

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank all the personnel of the Bushehr Elderly Health program and all the individuals who took part in the study.

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Authors and Affiliations

  1. Chronic Diseases Research Center, Endocrinology and Metabolism Population Sciences Institute, Tehran University of Medical Sciences, NO 10, Jalale-Al-Ahmad Ave, Chamran Highway, Tehran, Iran

    Marzieh Nikfarjam, Ramin Heshmat & Gita Shafiee

  2. Department of Epidemiology and Biostatistics, Pasteur Institute of Iran, Tehran, Iran

    Safoora Gharibzadeh

  3. Osteoporosis Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran

    Afshin Ostovar

  4. Clinical Cancer Research Center, Milad General Hospital, Tehran, Iran

    Vahid Maleki

  5. Knee and Sport Medicine Research Center, Milad Hospital, Tehran, Iran

    Vahid Maleki

  6. School of Nutrition Sciences and Food Technology, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Jalal Moludi

  7. The Persian Gulf Tropical Medicine Research Center, Bushehr University of Medical Sciences, Bushehr, Iran

    Iraj Nabipour

  8. Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, NO 10, Jalale-Al-Ahmad Ave, Chamran Highway, Tehran, Iran

    Bagher Larijani

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  1. Marzieh Nikfarjam
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Correspondence to Gita Shafiee or Bagher Larijani.

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Nikfarjam, M., Heshmat, R., Gharibzadeh, S. et al. The association between muscle indicators and bone mass density and related risk factors in the diabetic elderly population: Bushehr Elderly Health (BEH) Program. J Diabetes Metab Disord 20, 1429–1438 (2021). https://doi.org/10.1007/s40200-021-00881-5

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