Skip to main content

Advertisement

SpringerLink
Log in

Dehydroepiandrosterone Sulfate and Free Testosterone but not Estradiol are Related to Muscle Strength and Bone Microarchitecture in Older Adults

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

Abstract

The study aimed to elucidate the relationship between sex steroids and muscle mass, muscle strength, and trabecular bone score (TBS) in a community-dwelling aged population. We analyzed 922 men > 60 years of age and 1244 postmenopausal women. Weak muscle strength was defined as hand grip strength < 26 kg for men and < 18 kg for women, whereas degraded bone microarchitecture was defined as a TBS ≤ 1.2. The mean age was 70.2 ± 6.8 years for men and 71.2 ± 6.7 years for women. Participants within higher dehydroepiandrosterone sulfate (DHEAS) and free testosterone (FT) tertiles were likely to be younger, have greater muscle mass, and have stronger hand grip strength. Based on logistic regression models, men within the lowest FT tertile had weaker muscle strength compared to those in the highest tertile (adjusted odds ratio [OR] 2.28; 95% confidence interval [CI] 1.33–3.91). Women within the lowest DHEAS and FT tertile had weaker muscle strength compared to those in the highest tertile (adjusted OR for DHEAS 1.42; 95% CI 1.02–1.99; adjusted OR for FT 1.77, 95% CI 1.26–2.48). Moreover, men within the lowest FT tertile exhibited degraded bone microarchitecture compared to those in the highest tertile (adjusted OR 2.57, 95% CI 1.46–4.51). However, estradiol was not related to muscle strength or bone microarchitecture in both sexes. In conclusion, in aged men, serum FT was closely associated with muscle strength and bone microarchitecture and in postmenopausal women, serum DHEAS and FT were related to muscle strength.

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
Fig. 2

Similar content being viewed by others

References

  1. Dutta C (1997) Significance of sarcopenia in the elderly. J Nutr 127(5):992S–993S

    CAS  PubMed  Google Scholar 

  2. Curtis E, Litwic A, Cooper C, Dennison E (2015) Determinants of muscle and bone aging. J Cell Physiol 230(11):2618–2625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Arango-Lopera V, Arroyo P, Gutiérrez-Robledo L, Pérez-Zepeda M (2012) Prevalence of sarcopenia in Mexico City. Eur Geriatr Med 3(3):157–160

    Article  Google Scholar 

  4. Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52(1):80–85

    Article  PubMed  Google Scholar 

  5. Korean Society of Bone and Mineral Research (2018) Physician’s guide for osteoporosis

  6. Lamberts S (2003) The endocrinology of gonadal involution: menopause and andropause. Ann Endocrinol 64:77–81

    CAS  Google Scholar 

  7. Lamberts SW, Beld AW, Lely A-J (1997) The endocrinology of aging. Science 278(5337):419–424

    Article  CAS  PubMed  Google Scholar 

  8. Maggio M, Lauretani F, Ceda GP (2013) Sex hormones and sarcopenia in older persons. Curr Opin Clin Nutr Metab Care 16(1):3–13

    CAS  PubMed  Google Scholar 

  9. Valenti G, Denti L, Maggio M, Ceda G, Volpato S, Bandinelli S, Ceresini G, Cappola A, Guralnik JM, Ferrucci L (2004) Effect of DHEAS on skeletal muscle over the life span: the InCHIANTI study. J Gerontol Ser A 59(5):M466–M472

    Article  Google Scholar 

  10. Bonnefoy M, Patricot M, Lacour J, Rahmani A, Berthouze S, Kostka T (2002) Relation between physical activity, muscle function and IGF-1, testosterone and DHEAS concentrations in the elderly. Rev Med Interne 23(10):819–827

    Article  CAS  PubMed  Google Scholar 

  11. Enea C, Boisseau N, Fargeas-Gluck MA, Diaz V, Dugue B (2011) Circulating androgens in women: exercise-induced changes. Sport Med (Auckland, NZ) 41(1):1–15. https://doi.org/10.2165/11536920-000000000-00000

    Article  Google Scholar 

  12. Enea C, Boisseau N, Fargeas-Gluck MA, Diaz V, Dugué B (2011) Circulating androgens in women. Sport Med 41(1):1–15

    Article  Google Scholar 

  13. Bhasin S, Storer TW, Berman N, Yarasheski KE, Clevenger B, Phillips J, Lee WP, Bunnell TJ, Casaburi R (1997) Testosterone replacement increases fat-free mass and muscle size in hypogonadal men. J Clin Endocrinol Metab 82(2):407–413

    CAS  PubMed  Google Scholar 

  14. Snyder PJ, Peachey H, Hannoush P, Berlin JA, Loh L, Lenrow DA, Holmes JH, Dlewati A, Santanna J, Rosen CJ (1999) Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age. J Clin Endocrinol Metab 84(8):2647–2653

    CAS  PubMed  Google Scholar 

  15. van Geel TA, Geusens PP, Winkens B, Sels J-PJ, Dinant G-J (2009) Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol 160(4):681–687

    Article  CAS  PubMed  Google Scholar 

  16. Yuki A, Ando F, Otsuka R, Shimokata H (2015) Low free testosterone is associated with loss of appendicular muscle mass in J apanese community-dwelling women. Geriatr Gerontol Int 15(3):326–333

    Article  PubMed  Google Scholar 

  17. Baumgartner RN, Waters DL, Gallagher D, Morley JE, Garry PJ (1999) Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev 107(2):123–136

    Article  CAS  PubMed  Google Scholar 

  18. Chin K-Y, Soelaiman I-N, Naina Mohamed I, Shahar S, Teng NIMF, Suhana Mohd Ramli E, Ahmad F, Aminuddin A, Zurinah Wan Ngah W (2012) Testosterone is associated with age-related changes in bone health status, muscle strength and body composition in men. Aging Male 15(4):240–245

    Article  CAS  PubMed  Google Scholar 

  19. Iannuzzi-Sucich M, Prestwood KM, Kenny AM (2002) Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J Gerontol Ser A 57(12):M772–M777

    Article  Google Scholar 

  20. Hwang A-C, Liu L-K, Lee W-J, Chen L-Y, Lin M-H, Peng L-N, Won CW, Chen L-K (2013) Association of androgen with skeletal muscle mass and muscle function among men and women aged 50 years and older in Taiwan: results from the I-Lan longitudinal aging study. Rejuvenation Res 16(6):453–459

    Article  CAS  PubMed  Google Scholar 

  21. Ohlsson C, Nethander M, Kindmark A, Ljunggren Ö, Lorentzon M, Rosengren BE, Karlsson MK, Mellström D, Vandenput L (2017) Low serum DHEAS predicts increased fracture risk in older men: the MrOS Sweden study. J Bone Miner Res 32(8):1607–1614

    Article  CAS  PubMed  Google Scholar 

  22. Mellström D, Johnell O, Ljunggren Ö, Eriksson AL, Lorentzon M, Mallmin H, Holmberg A, Redlund-Johnell I, Orwoll E, Ohlsson C (2006) Free testosterone is an independent predictor of BMD and prevalent fractures in elderly men: MrOS Sweden. J Bone Miner Res 21(4):529–535

    Article  PubMed  Google Scholar 

  23. LeBlanc ES, Nielson CM, Marshall LM, Lapidus JA, Barrett-Connor E, Ensrud KE, Hoffman AR, Laughlin G, Ohlsson C, Orwoll ES (2009) The effects of serum testosterone, estradiol, and sex hormone binding globulin levels on fracture risk in older men. J Clin Endocrinol Metab 94(9):3337–3346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bousson V, Bergot C, Sutter B, Levitz P, Cortet B (2012) Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos Int 23(5):1489–1501

    Article  CAS  PubMed  Google Scholar 

  25. Baik I, Kim J, Abbott RD, Joo S, Jung K, Lee S, Shim J, Kang K, Yoo S, Shin C (2008) Association of snoring with chronic bronchitis. Arch Int Med 168(2):167–173

    Article  Google Scholar 

  26. Cho YS, Go MJ, Kim YJ, Heo JY, Oh JH, Ban HJ, Yoon D, Lee MH, Kim DJ, Park M, Cha SH, Kim JW, Han BG, Min H, Ahn Y, Park MS, Han HR, Jang HY, Cho EY, Lee JE, Cho NH, Shin C, Park T, Park JW, Lee JK, Cardon L, Clarke G, McCarthy MI, Lee JY, Lee JK, Oh B, Kim HL (2009) A large-scale genome-wide association study of Asian populations uncovers genetic factors influencing eight quantitative traits. Nat Genet 41(5):527–534. https://doi.org/10.1038/ng.357

    Article  CAS  PubMed  Google Scholar 

  27. Ainsworth BE, Haskell WL, Leon AS, Jacobs DR Jr, Montoye HJ, Sallis JF, Paffenbarger RS Jr (1993) Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sport Exerc 25(1):71–80

    Article  CAS  Google Scholar 

  28. Cormier C, Lamy O, Poriau S (2012) TBS in routine clinical practice: proposals of use. Atlas of TBS use. Edition—2012—16 p

  29. Chen L-K, Liu L-K, Woo J, Assantachai P, Auyeung T-W, Bahyah KS, Chou M-Y, Chen L-Y, Hsu P-S, Krairit O (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Direct Assoc 15(2):95–101

    Article  Google Scholar 

  30. Labrie F (2003) Extragonadal synthesis of sex steroids: intracrinology. Ann Endocrinol 64:95–107

    CAS  Google Scholar 

  31. Pollanen E, Sipila S, Alen M, Ronkainen PH, Ankarberg-Lindgren C, Puolakka J, Suominen H, Hamalainen E, Turpeinen U, Konttinen YT, Kovanen V (2011) Differential influence of peripheral and systemic sex steroids on skeletal muscle quality in pre- and postmenopausal women. Aging Cell 10(4):650–660. https://doi.org/10.1111/j.1474-9726.2011.00701.x

    Article  CAS  PubMed  Google Scholar 

  32. Orwoll E, Lambert LC, Marshall LM, Blank J, Barrett-Connor E, Cauley J, Ensrud K, Cummings SR (2006) Endogenous testosterone levels, physical performance, and fall risk in older men. Arch Int Med 166(19):2124–2131

    Article  Google Scholar 

  33. La Colla A, Pronsato L, Milanesi L, Vasconsuelo A (2015) 17β-Estradiol and testosterone in sarcopenia: role of satellite cells. Ageing Res Rev 24:166–177

    Article  CAS  PubMed  Google Scholar 

  34. Haren MT, Siddiqui A, Armbrecht H, Kevorkian R, Kim M, Haas M, Mazza A, Kumar VB, Green M, Banks W (2011) Testosterone modulates gene expression pathways regulating nutrient accumulation, glucose metabolism and protein turnover in mouse skeletal muscle. Int J Androl 34(1):55–68

    Article  CAS  PubMed  Google Scholar 

  35. Sinha-Hikim I, Cornford M, Gaytan H, Lee ML, Bhasin S (2006) Effects of testosterone supplementation on skeletal muscle fiber hypertrophy and satellite cells in community-dwelling older men. J Clin Endocrinol Metab 91(8):3024–3033

    Article  CAS  PubMed  Google Scholar 

  36. Benito M, Gomberg B, Wehrli FW, Weening RH, Zemel B, Wright AC, Song HK, Cucchiara A, Snyder PJ (2003) Deterioration of trabecular architecture in hypogonadal men. J Clin Endocrinol Metab 88(4):1497–1502

    Article  CAS  PubMed  Google Scholar 

  37. Kasperk CH, Wergedal JE, Farley JR, Linkhart TA, Turner RT (1989) Androgens directly stimulate proliferation of bone cells in vitro. Endocrinology 124(3):1576–1578

    Article  CAS  PubMed  Google Scholar 

  38. Takeuchi M, Kakushi H, Tohkin M (1994) Androgens directly stimulate mineralization and increase androgen receptors in human osteoblast-like osteosarcoma cells. Biochem Biophys Res Comm 204(2):905–911

    Article  CAS  PubMed  Google Scholar 

  39. van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW (2000) Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab 85(9):3276–3282

    PubMed  Google Scholar 

  40. Sipilä S (2003) Body composition and muscle performance during menopause and hormone replacement therapy. J Endocrinol Investig 26(9):893–901

    Article  Google Scholar 

  41. Greising SM, Baltgalvis KA, Lowe DA, Warren GL (2009) Hormone therapy and skeletal muscle strength: a meta-analysis. J Gerontol Ser A 64(10):1071–1081

    Article  CAS  Google Scholar 

  42. Slemenda CW, Longcope C, Zhou L, Hui SL, Peacock M, Johnston CC (1997) Sex steroids and bone mass in older men. Positive associations with serum estrogens and negative associations with androgens. J Clin Investig 100(7):1755–1759

    Article  CAS  PubMed  Google Scholar 

  43. Mazer NA (2009) A novel spreadsheet method for calculating the free serum concentrations of testosterone, dihydrotestosterone, estradiol, estrone and cortisol: with illustrative examples from male and female populations. Steroid 74(6):512–519

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The research did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Seoul National University College of Medicine, Seoul, South Korea

    Sung Hye Kong, Jung Hee Kim & Chan Soo Shin

  2. Department of Internal Medicine, Veterans Health Service Medical Center, Seoul, South Korea

    Ji Hyun Lee

  3. Department of Internal Medicine, Chonnam National University Hwasun Hospital, Chonnam, South Korea

    A Ram Hong

  4. Department of Preventive Medicine, Ajou University School of Medicine, #5 Wonchon-Dong, Youngtong-Gu, Suwon, 443-721, South Korea

    Nam H. Cho

Authors
  1. Sung Hye Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jung Hee Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ji Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A Ram Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chan Soo Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nam H. Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nam H. Cho.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

All procedures performed in the study involving human participants were in accordance with the ethical standards of the Korea Centers for Disease Control and Prevention Institutional Review Board and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

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

Sung Hye Kong and Jung Hee Kim have contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kong, S.H., Kim, J.H., Lee, J.H. et al. Dehydroepiandrosterone Sulfate and Free Testosterone but not Estradiol are Related to Muscle Strength and Bone Microarchitecture in Older Adults. Calcif Tissue Int 105, 285–293 (2019). https://doi.org/10.1007/s00223-019-00566-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-019-00566-5

Keywords

Search

Navigation