Skip to main content

Advertisement

SpringerLink
Log in

Low Skeletal Muscle Mass is Associated with the Risk of Low Bone Mineral Density in Urban Dwelling Premenopausal Women

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

To evaluate the relationship between skeletal muscle mass and bone mineral density (BMD) and to determine the association between low skeletal muscle mass and low BMD in urban dwelling young adults. This study was based on data from the 2008–2011 Korea National Health and Nutrition Examination Surveys. The subjects were 1702 20–49-year-old men and 2192 premenopausal women (age 20–55 years). BMD at the lumbar spine, femoral neck, and total hip and the appendicular skeletal muscle mass (ASM) were measured by dual-energy X-ray absorptiometry. Skeletal muscle mass index (SMI) was defined as weight-adjusted ASM. Mildly and severely low muscle skeletal mass were defined as SMI that was 1–2 and >2 standard deviations below the sex-specific mean ASM of young adults, respectively. Low BMD was defined as T score of less than −1.0 at the lumbar spine, femoral neck, and/or total hip. After adjusting for confounders, skeletal muscle mass was positively associated with BMD at the lumbar spine, femoral neck, and total hip in both men and women. Mildly and severely low skeletal muscle mass increased the risk of low BMD in premenopausal women [OR (95% CI) = 1.4 (1.1–1.9) and 2.4 (1.2–4.6), respectively] but not men. In women, low skeletal muscle mass independently was associated with the risk of low BMD at the femoral neck and total hip but not the lumbar spine. Skeletal muscle mass was independently associated with BMD in urban dwelling young men and women, but low skeletal muscle mass was associated with the risk of low BMD in premenopausal women only.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

25OHD:

25-Hydroxyvitamin D

ALT:

Alanine aminotransferase

ASM:

Appendicular skeletal muscle mass

AST:

Aspartate aminotransferase

BMD:

Bone mineral density

BMI:

Body mass index

DXA:

Dual-energy X-ray absorptiometry

KNHANES:

Korea National Health and Nutrition Examination Surveys

LBM:

Lean body mass

SD:

Standard deviation

SMI:

Skeletal muscle mass index

References

  1. Watts NB, Manson JE (2017) Osteoporosis and fracture risk evaluation and management: shared decision making in clinical practice. JAMA 317(3):253–254. doi:10.1001/jama.2016.19087

    Article  CAS  PubMed  Google Scholar 

  2. Black DM, Rosen CJ (2016) Clinical practice. Postmenopausal osteoporosis. N Engl J Med 374(3):254–262. doi:10.1056/NEJMcp1513724

    Article  CAS  PubMed  Google Scholar 

  3. Giusti A, Bianchi G (2014) Male osteoporosis. Reumatismo 66(2):136–143. doi:10.4081/reumatismo.2014.786

    Article  CAS  PubMed  Google Scholar 

  4. McLendon AN, Woodis CB (2014) A review of osteoporosis management in younger premenopausal women. Womens Health (Lond) 10(1):59–77. doi:10.2217/whe.13.73

    Article  CAS  Google Scholar 

  5. Vondracek SF, Hansen LB, McDermott MT (2009) Osteoporosis risk in premenopausal women. Pharmacotherapy 29(3):305–317. doi:10.1592/phco.29.3.305

    Article  PubMed  Google Scholar 

  6. Mounach A, Abayi DA, Ghazi M, Ghozlani I, Nouijai A, Achemlal L, Bezza A, El Maghraoui A (2009) Discordance between hip and spine bone mineral density measurement using DXA: prevalence and risk factors. Semin Arthritis Rheum 38(6):467–471. doi:10.1016/j.semarthrit.2008.04.001

    Article  CAS  PubMed  Google Scholar 

  7. Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25(3):165–171. doi:10.1007/s00774-006-0747-3

    Article  PubMed  Google Scholar 

  8. Taaffe DR, Cauley JA, Danielson M, Nevitt MC, Lang TF, Bauer DC, Harris TB (2001) Race and sex effects on the association between muscle strength, soft tissue, and bone mineral density in healthy elders: the Health, Aging, and Body Composition Study. J Bone Miner Res 16(7):1343–1352. doi:10.1359/jbmr.2001.16.7.1343

    Article  CAS  PubMed  Google Scholar 

  9. Ahn SH, Lee SH, Kim H, Kim BJ, Koh JM (2014) Different relationships between body compositions and bone mineral density according to gender and age in Korean populations (KNHANES 2008–2010). J Clin Endocrinol Metab 99(10):3811–3820. doi:10.1210/jc.2014-1564

    Article  CAS  PubMed  Google Scholar 

  10. Makovey J, Naganathan V, Sambrook P (2005) Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos Int 16(12):1495–1505. doi:10.1007/s00198-005-1841-4

    Article  PubMed  Google Scholar 

  11. Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. J Bone Miner Res 17(6):1095–1101. doi:10.1359/jbmr.2002.17.6.1095

    Article  PubMed  Google Scholar 

  12. Kirchengast S, Huber J (2012) Sex-specific associations between soft tissue body composition and bone mineral density among older adults. Ann Hum Biol 39(3):206–213. doi:10.3109/03014460.2012.676067

    Article  PubMed  Google Scholar 

  13. Genaro PS, Pereira GA, Pinheiro MM, Szejnfeld VL, Martini LA (2010) Influence of body composition on bone mass in postmenopausal osteoporotic women. Arch Gerontol Geriatr 51(3):295–298. doi:10.1016/j.archger.2009.12.006

    Article  PubMed  Google Scholar 

  14. Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C (2001) Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 47(4):207–212

    Article  CAS  PubMed  Google Scholar 

  15. Pluijm SM, Visser M, Smit JH, Popp-Snijders C, Roos JC, Lips P (2001) Determinants of bone mineral density in older men and women: body composition as mediator. J Bone Miner Res 16(11):2142–2151. doi:10.1359/jbmr.2001.16.11.2142

    Article  CAS  PubMed  Google Scholar 

  16. Korea Centers for Disease Control and Prevention. The Fourth and Fifth Korea National Health and Nutrition Examination Survey (KNHANES IV, V) 2008–2011. Seoul, Korea: Division of Chronic Disease Surveillance, Korea Centers for Disease Control and Prevention

  17. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN Jr (1990) Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 52(2):214–218

    CAS  PubMed  Google Scholar 

  18. Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50(5):889–896

    Article  PubMed  Google Scholar 

  19. Kim BJ, Ahn SH, Kim HM, Lee SH, Koh JM (2015) Low skeletal muscle mass associates with low femoral neck strength, especially in older Korean women: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV). Osteoporos Int 26(2):737–747. doi:10.1007/s00198-014-2959-z

    Article  PubMed  Google Scholar 

  20. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763

    Article  CAS  PubMed  Google Scholar 

  21. Cawthon PM, Peters KW, Shardell MD, McLean RR, Dam TT, Kenny AM, Fragala MS, Harris TB, Kiel DP, Guralnik JM, Ferrucci L, Kritchevsky SB, Vassileva MT, Studenski SA, Alley DE (2014) Cutpoints for low appendicular lean mass that identify older adults with clinically significant weakness. J Gerontol A Biol Sci Med Sci 69(5):567–575. doi:10.1093/gerona/glu023

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wolfe RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84(3):475–482

    CAS  PubMed  Google Scholar 

  23. Moon SS (2014) Relationship of lean body mass with bone mass and bone mineral density in the general Korean population. Endocrine 47(1):234–243. doi:10.1007/s12020-013-0160-3

    Article  CAS  PubMed  Google Scholar 

  24. Sornay-Rendu E, Duboeuf F, Boutroy S, Chapurlat RD (2016) Muscle mass is associated with incident fracture in postmenopausal women: the OFELY study. Bone. doi:10.1016/j.bone.2016.10.024

    Google Scholar 

  25. Hars M, Biver E, Chevalley T, Herrmann F, Rizzoli R, Ferrari S, Trombetti A (2016) Low lean mass predicts incident fractures independently from FRAX: a prospective cohort study of recent retirees. J Bone Miner Res 31(11):2048–2056. doi:10.1002/jbmr.2878

    Article  CAS  PubMed  Google Scholar 

  26. Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A 275(2):1081–1101. doi:10.1002/ar.a.10119

    Article  Google Scholar 

  27. Le Bihan MC, Bigot A, Jensen SS, Dennis JL, Rogowska-Wrzesinska A, Laine J, Gache V, Furling D, Jensen ON, Voit T, Mouly V, Coulton GR, Butler-Browne G (2012) In-depth analysis of the secretome identifies three major independent secretory pathways in differentiating human myoblasts. J Proteom 77:344–356. doi:10.1016/j.jprot.2012.09.008

    Article  Google Scholar 

  28. Sievanen H (2005) Hormonal influences on the muscle-bone feedback system: a perspective. J Musculoskelet Neuronal Interact 5(3):255–261

    CAS  PubMed  Google Scholar 

  29. DiGirolamo DJ, Kiel DP, Esser KA (2013) Bone and skeletal muscle: neighbors with close ties. J Bone Miner Res 28(7):1509–1518. doi:10.1002/jbmr.1969

    Article  PubMed  PubMed Central  Google Scholar 

  30. MacDougall JD, Gibala MJ, Tarnopolsky MA, MacDonald JR, Interisano SA, Yarasheski KE (1995) The time course for elevated muscle protein synthesis following heavy resistance exercise. Can J Appl Physiol 20(4):480–486

    Article  CAS  PubMed  Google Scholar 

  31. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB (2006) Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 576(Pt 2):613–624. doi:10.1113/jphysiol.2006.113175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Suominen H (2006) Muscle training for bone strength. Aging Clin Exp Res 18(2):85–93

    Article  PubMed  Google Scholar 

  33. Ashby RL, Adams JE, Roberts SA, Mughal MZ, Ward KA (2011) The muscle-bone unit of peripheral and central skeletal sites in children and young adults. Osteoporos Int 22(1):121–132. doi:10.1007/s00198-010-1216-3

    Article  CAS  PubMed  Google Scholar 

  34. Wu F, Callisaya M, Wills K, Laslett LL, Jones G, Winzenberg T (2017) Both baseline and change in lower limb muscle strength in younger women are independent predictors of balance in middle-age: a 12-year population-based prospective study. J Bone Miner Res. doi:10.1002/jbmr.3103

    PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), which was funded by the Ministry of Science, ICT & Future Planning (NRF-2014R1A1A1006695).

Author information

Authors and Affiliations

  1. Division of Rheumatology, Department of Internal Medicine, College of Medicine, Ewha Womans University, Seoul, South Korea

    In Je Kim

  2. Division of Rheumatology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, South Korea

    Kwi Young Kang

  3. Division of Rheumatology, Department of Internal Medicine, College of Medicine, Incheon St. Mary’s Hospital, The Catholic University of Korea, #56, Dongsu-Ro, Bupyung-Gu, Incheon, South Korea

    Kwi Young Kang

Authors
  1. In Je Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kwi Young Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kwi Young Kang.

Ethics declarations

Conflict of interest

In Je Kim and Kwi Young Kang have no competing interests to declare.

Human and Animal Rights and Informed Consent

All participants gave informed consent before being included in this study. This study did not need ethical approval of our Institutional Review Board, since the survey data examined were publicly available.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, I.J., Kang, K.Y. Low Skeletal Muscle Mass is Associated with the Risk of Low Bone Mineral Density in Urban Dwelling Premenopausal Women. Calcif Tissue Int 101, 581–592 (2017). https://doi.org/10.1007/s00223-017-0314-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-017-0314-z

Keywords

Search

Navigation