Skip to main content

Advertisement

SpringerLink
Log in

Hypogonadal Men with Higher Body Mass Index have Higher Bone Density and Better Bone Quality but Reduced Muscle Density

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

Abstract

Although hypogonadism is a risk factor for bone loss and fractures, the different etiopathophysiology and hormonal profile of classical and obesity-induced hypogonadism may lead to differences in musculoskeletal profile. This is a cross-sectional study of hypogonadal men between 40 and 74 years old. Our outcomes include: areal bone mineral density (aBMD) and body composition by dual-energy X-ray absorptiometry; volumetric BMD (vBMD) and soft tissue composition of the tibia by peripheral quantitative computed tomography. Fracture risk assessment tool (FRAX) scores were evaluated. Testosterone, estradiol, luteinizing hormone, follicle stimulating hormone, sex hormone-binding globulin, C-telopeptide, osteocalcin, and sclerostin were measured. We divided the population into subgroups of BMI: group 1: BMI < 30; group 2: BMI ≥30 to <35 and group 3: BMI ≥ 35 kg/m2. One-hundred five men were enrolled. Spine and hip aBMD, and total and trabecular vBMD at the 4% tibia significantly increased with increasing BMI. Cortical thickness (330.7 ± 53.2, 343.3 ± 35.4, and 358.7 ± 38.2 mm, p = 0.04; groups 1, 2 and 3, respectively) and cortical area (5.3 ± 0.7, 5.5 ± 0.6, and 5.7 ± 0.6 mm, p = 0.01; groups 1, 2 and 3, respectively) at 38% tibia increased with increasing BMI. While absolute lean mass increased with increasing BMI, % lean mass and muscle density (70.2 ± 5.0, 71.3 ± 6.4, and 67.1 ± 5.1 mg/cm3; groups 1, 2 and 3, respectively) were lowest in group 3. Although severely obese hypogondal men have better BMD and bone quality, they have reduced muscle density, the significance of which remains to be determined.

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

References

  1. Barrett-Connor E, Mueller JE, von Muhlen DG et al (2000) Low levels of estradiol are associated with vertebral fractures in older men, but not women: the Rancho Bernardo Study. J Clin Endocrinol Metab 85:219–223

    CAS  PubMed  Google Scholar 

  2. Khosla S, Melton LJ III, Atkinson EJ et al (1998) Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J Clin Endocrinol Metab 83:2266–2274

    CAS  PubMed  Google Scholar 

  3. Falahati-Nini A, Riggs BL, Atkinson EJ et al (2000) Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest 106:1553–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Reid IR (2002) Relationships among body mass, its components, and bone. Bone 31:547–555

    Article  CAS  PubMed  Google Scholar 

  5. Kirschner MA, Schneider G, Ertel NH et al (1982) Obesity, androgens, estrogens and cancer risk. Cancer Res 42:3281s–3285s

    CAS  PubMed  Google Scholar 

  6. Schneider G, Kirschner MA, Berkowitz R et al (1979) Increased estrogen production in obese men. J Clin Endocrinol Metab 48:633–638

    Article  CAS  PubMed  Google Scholar 

  7. Strain GW, Zumoff B, Kream J et al (1982) Mild Hypogonadotropic hypogonadism in obese men. Metabolism 31:871–875

    Article  CAS  PubMed  Google Scholar 

  8. Bhasin S, Cunningham GR, Hayes FJ et al (2010) Testosterone therapy in men with androgen deficiency syndromes: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 95:2536–2559

    Article  CAS  PubMed  Google Scholar 

  9. Aguirre LE, Colleluori G, Fowler KE et al (2015) High aromatase activity in hypogonadal men is associated with higher spine bone mineral density, increased truncal fat and reduced lean mass. Eur J Endocrinol 173:167–174

    Article  CAS  PubMed  Google Scholar 

  10. Aguirre L, Napoli N, Waters D et al (2014) Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J Clin Endocrinol Metab 99:3290–3297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dennison EM, Jameson KA, Edwards MH et al (2014) Peripheral quantitative computed tomography measures are associated with adult fracture risk: the Hertfordshire Cohort Study. Bone 64:13–17

    Article  CAS  PubMed  Google Scholar 

  12. Wong AK, Beattie KA, Min KK et al (2014) Peripheral quantitative computed tomography-derived muscle density and peripheral magnetic resonance imaging-derived muscle adiposity: precision and associations with fragility fractures in women. J Musculoskelet Neuronal Interact 14:401–410

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Sherk VD, Thiebaud RS, Chen Z et al (2014) Associations between pQCT-based fat and muscle area and density and DXA-based total and leg soft tissue mass in healthy women and men. J Musculoskelet Neuronal Interact 14:411–417

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Frank-Wilson AW, Johnston JD, Olszynski WP et al (2015) Measurement of muscle and fat in postmenopausal women: precision of previously reported pQCT imaging methods. Bone 75:49–54

    Article  PubMed  Google Scholar 

  15. Napoli N, Villareal DT, Mumm S et al (2005) Effect of CYP1A1 gene polymorphisms on estrogen metabolism and bone density. J Bone Miner Res 20:232–239

    Article  CAS  PubMed  Google Scholar 

  16. Vermeulen A, Verdonck L, Kaufman JMA (1999) Critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84:3666–3672

    Article  CAS  PubMed  Google Scholar 

  17. Sowers MR, Randolph J Jr, Jannausch M et al (2008) Levels of sex steroid and cardiovascular disease measures in premenopausal and hormone-treated women at midlife: implications for the “timing hypothesis”. Arch Intern Med 168:2146–2153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Giagulli VA, Kaufman JM, Vermeulen A (1994) Pathogenesis of the decreased androgen levels in obese men. J Clin Endocrinol Metab 79:997–1000

    CAS  PubMed  Google Scholar 

  19. Glass AR, Swerdloff RS, Bray GA et al (1977) Low serum testosterone and sex hormone-binding globulin in massively obese men. J Clin Endocrinol Metab 45:1211–1219

    Article  CAS  PubMed  Google Scholar 

  20. Amatruda JM, Hochstein M, Hsu TH et al (1982) Hypothalamic and pituitary dysfunction in obese males. Int J Obes 6:183–189

    CAS  PubMed  Google Scholar 

  21. Kley HK, Deselaers T, Peerenboom H et al (1980) Enhanced conversion of androstenedione to estrogens in obese males. J Clin Endocrinol Metab 51:1128–1132

    Article  CAS  PubMed  Google Scholar 

  22. Zumoff B, Miller LK, Strain GW (2003) Reversal of the hypogonadotropic hypogonadism of obese men by administration of the aromatase inhibitor testolactone. Metabolism 52:1126–1128

    Article  CAS  PubMed  Google Scholar 

  23. Corona G, Monami M, Rastrelli G et al (2011) Type 2 diabetes mellitus and testosterone: a meta-analysis study. Int J Androl 34:528–540

    Article  CAS  PubMed  Google Scholar 

  24. Dhindsa S, Miller MG, McWhirter CL et al (2010) Testosterone concentrations in diabetic and nondiabetic obese men. Diabetes Care 33:1186–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Albala C, Yanez M, Devoto E et al (1996) Obesity as a protective factor for postmenopausal osteoporosis. Int J Obes Relat Metab Disord 20:1027–1032

    CAS  PubMed  Google Scholar 

  26. Felson DT, Zhang Y, Hannan MT et al (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham Study. J Bone Miner Res 8:567–573

    Article  CAS  PubMed  Google Scholar 

  27. Khosla S, Melton LJ III, Robb RA et al (2005) Relationship of volumetric BMD and structural parameters at different skeletal sites to sex steroid levels in men. J Bone Miner Res 20:730–740

    Article  PubMed  Google Scholar 

  28. Nielson CM, Marshall LM, Adams AL et al (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 26:496–502

    Article  PubMed  Google Scholar 

  29. Shen J, Nielson CM, Marshall LM et al (2015) The Association Between BMI and QCT-Derived Proximal Hip Structure and Strength in Older Men: a Cross-Sectional Study. J Bone Miner Res 30:1301–1308

    Article  PubMed  PubMed Central  Google Scholar 

  30. Taes YE, Lapauw B, Vanbillemont G et al (2009) Fat mass is negatively associated with cortical bone size in young healthy male siblings. J Clin Endocrinol Metab 94:2325–2331

    Article  CAS  PubMed  Google Scholar 

  31. De Laet C, Kanis JA, Oden A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338

    Article  Google Scholar 

  32. Estrada M, Kleppinger A, Judge JO et al (2007) Functional impact of relative vs. absolute sarcopenia in healthy older women. J Am Geriatr Soc 55:1712–1719

    Article  PubMed  Google Scholar 

  33. Kalinkovich A, Livshits G (2017) Sarcopenic obesity or obese sarcopenia: a cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res Rev 35:200–221

    Article  CAS  PubMed  Google Scholar 

  34. Goodpaster BH, Carlson CL, Visser M et al (1985) Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study. J Appl Physiol 90:2157–2165

    Google Scholar 

  35. Villareal Dennis T, Banks Marian, Siener Catherine et al (2004) Physical frailty and body composition in obese elderly men and women. Obes Res 12:913–920

    Article  PubMed  Google Scholar 

  36. Herrera-Rangel AB, Aranda-Moreno C, Mantilla-Ochoa T et al (2015) Influence of the body mass index on the occurrence of falls in patients with type 2 diabetes mellitus. Obes Res Clin Pract 9(5):522–526

    Article  PubMed  Google Scholar 

  37. Compston J (2015) Obesity and fractures in postmenopausal women. Curr Opin Rheumatol 27:414–419

    Article  PubMed  Google Scholar 

  38. Baumgartner RN, Koehler KM, Gallagher D et al (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147:755–763

    Article  CAS  PubMed  Google Scholar 

  39. Batsis JA, Mackenzie TA, Lopez-Jimenez F et al (2015) Sarcopenia, sarcopenic obesity and functional impairments in older adults: National Health and Nutrition Examination Surveys 1999–2004. Nutr Res 35:1031–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ng M, Fleming T, Robinson M et al (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766–781

    Article  PubMed  PubMed Central  Google Scholar 

  41. Lamm S, Chidakel A, Bansal R (2016) Obesity and hypogonadism. Urol Clin North Am 43:239–245

    Article  PubMed  Google Scholar 

  42. Kaplan SA, Lee JY, O’Neill EA et al (2013) Prevalence of low testosterone and its relationship to body mass index in older men with lower urinary tract symptoms associated with benign prostatic hyperplasia. Aging Male 16:169–172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the resources at the New Mexico VA Health Care System in Albuquerque, NM, USA; the Biomedical Research of New Mexico Albuquerque, NM, USA; the Michael E. DeBakey VA Medical Center, Houston, TX, USA and the Center for Translational Research in Inflammatory Diseases (CTRID) at the Michael E. DeBakey VA Medical Center, Houston, TX.

Funding

This work was funded by VA Merit Review 5 101 CX00042403.

Author information

Author notes

    Authors and Affiliations

    1. Department of Medicine, New Mexico VA Health Care System, Albuquerque, NM, USA

      Lina E. Aguirre, Richard Dorin, David Robbins & Clifford Qualls

    2. Biomedical Research of New Mexico, Albuquerque, NM, USA

      Lina E. Aguirre & Clifford Qualls

    3. University of New Mexico School of Medicine, Albuquerque, NM, USA

      Lina E. Aguirre, Richard Dorin, David Robbins & Clifford Qualls

    4. University Campus Bio-Medico of Rome, Rome, Italy

      Georgia Colleluori

    5. Department of Medicine, Michael E. DeBakey VA Medical Center, 2002 Holcombe Blvd., Houston, TX, USA

      Georgia Colleluori, Rui Chen, Bryan Jiang, Dennis T. Villareal & Reina Armamento-Villareal

    6. Baylor College of Medicine, Houston, TX, USA

      Georgia Colleluori, Rui Chen, Bryan Jiang, Dennis T. Villareal & Reina Armamento-Villareal

    Authors
    1. Lina E. Aguirre
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Georgia Colleluori
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Richard Dorin
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. David Robbins
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Rui Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Bryan Jiang
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Clifford Qualls
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Dennis T. Villareal
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Reina Armamento-Villareal
      View author publications

      You can also search for this author in PubMed Google Scholar

    Contributions

    Author Contributions

    RAV designed the study. LA, GC, RD, DR, DV, RAV conducted the study and collected the data. LA, GC, CQ, DV, RAV analyzed and interpreted the data. LA, GC, RC, BJ, CQ, DV, RV drafted the manuscript. Revising manuscript content and approving the final version: all take responsibility for the manuscript content, the integrity of the data analysis and approval of the final version of the manuscript.

    Corresponding author

    Correspondence to Reina Armamento-Villareal.

    Ethics declarations

    Conflict of interest

    Lina E. Aguirre, Georgia Colleluori, Richard Dorin, David Robbins, Rui Chen, Bryan Jiang, Clifford Qualls, Dennis T. Villareal, Reina Armamento-Villareal declare that they have no conflict of interest.

    Human and Animal Rights and Informed Consent

    All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

    Additional information

    Lina E. Aguirre and Georgia Colleluori contributed equally to this manuscript and are considered as co-first authors.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Aguirre, L.E., Colleluori, G., Dorin, R. et al. Hypogonadal Men with Higher Body Mass Index have Higher Bone Density and Better Bone Quality but Reduced Muscle Density. Calcif Tissue Int 101, 602–611 (2017). https://doi.org/10.1007/s00223-017-0316-x

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00223-017-0316-x

    Keywords

    Search

    Navigation