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Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism.
Abstract
Acquired hypogonadism is being increasingly recognized in adult men. However, the effects of long term testosterone replacement on bone density and body composition are largely unknown. We investigated 36 adult men with acquired hypogonadism (age, 22-69 yr; median, 58 yr), including 29 men with central hypogonadism and 7 men with primary hypogonadism, and 44 age-matched eugonadal controls. Baseline evaluation included body composition analysis by bioimpedance, determination of site-specific adipose area by dual energy quantitative computed tomography scan (QCT) of the lumbar spine, and measurements of spinal bone mineral density (BMD) using dual energy x-ray absortiometry, spinal trabecular BMD with QCT, and radial BMD with single photon absorptiometry. Percent body fat was significantly greater in the hypogonadal men compared to eugonadal men (mean +/- SEM, 26.4 +/- 1.1% vs. 19.2 +/- 0.8%; P < 0.01). The mean trabecular BMD determined by QCT for the hypogonadal men was 115 +/- 6 mg K2HPO4/cc. Spinal BMD was significantly lower than that in eugonadal controls (1.006 +/- 0.024 vs. 1.109 +/- 0.028 g/cm2; P = 0.02, respectively). Radial BMD was similar in both groups. Testosterone enanthate therapy was initiated in 29 hypogonadal men at a dose of 100 mg/week, and the subjects were evaluated at 6-month intervals for 18 months. During testosterone therapy, the percent body fat decreased 14 +/- 4% (P < 0.001). There was a 13 +/- 4% decrease in subcutaneous fat (P < 0.01) and a 7 +/- 2% increase in lean muscle mass (P = 0.01) during testosterone therapy. Spinal BMD and trabecular BMD increased by 5 +/- 1% (P < 0.001) and 14 +/- 3% (P < 0.001), respectively. Radial BMD did not change. Serum bone-specific alkaline phosphatase and urinary deoxypyridinoline excretion, markers of bone formation and resorption, respectively, decreased significantly over the 18 months (P = 0.003 and P = 0.04, respectively). We conclude that testosterone therapy given to adult men with acquired hypogonadism decreases sc fat and increases lean muscle mass. In addition, testosterone therapy reduces bone remodeling and increases trabecular bone density. The beneficial effects of androgen administration on body composition and bone density may provide additional indications for testosterone therapy in hypogonadal men.
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“Testosterone replacement in men with authentic, pathologically-based hypogonadism reduces fat mass by 10%–15%.7778”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [77]
In the citing paper
“T replacement increases libido, sexual motivation and sexual function (134,135,138-143), mood (144), sense of well being, concentration (135,139,143,145-147), self-reported sense of energy (134,135), muscle mass and strength (132,148,149), and the recovery of anemia related to T deficiency (134).”
From Hormonal Replacement in Hypopituitarism in Adults: An Endocrine Society Clinical Practice Guideline (2016) · cites this paper as [134]
In the citing paper
“Treatment increases BMD (132-135) and improves trabecular structure (136) and bone mechanical properties (137).”
From Hormonal Replacement in Hypopituitarism in Adults: An Endocrine Society Clinical Practice Guideline (2016) · cites this paper as [134]
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Corona, G., Giagulli, V. A., Maseroli, E., Vignozzi, L., Aversa, A., Zitzmann, M., Saad, F., Mannucci, E., & Maggi, M. (2016) · European Journal of Endocrinology · doi:10.1530/eje-15-0262 · Cited by 217
Bhasin, S., Taylor, W. E., Singh, R., Artaza, J., Sinha-Hikim, I., Jasuja, R., Choi, H., & Gonzalez-Cadavid, N. F. (2003) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/58.12.m1103 · Cited by 215
The impact of sleep on age-related sarcopenia: Possible connections and clinical implications
Piovezan, R. D., Abucham, J., dos Santos, R. V. T., de Mello, M. T., Tufik, S., & Poyares, D. R. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.003 · Cited by 222
“GH deficiency syndrome and hypogonadism at a young age lead to decline in body composition, muscle strength and physical performance, resembling those found in healthy aged individuals (Cuneo et al., 1990; Katznelson et al., 1996).”
BackgroundEndogenous Sex Hormones and Cardiovascular Disease in Men
Muller, M., van der Schouw, Y. T., Thijssen, J. H. H., & Grobbee, D. E. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030611 · Cited by 210
Testosterone for the aging male; current evidence and recommended practice
Jones, H. (2008) · Clinical Interventions in Aging · doi:10.2147/cia.s190 · Cited by 204
“A large number of trials have demonstrated a positive effect of testosterone treatment on bone mineral density (Katznelson et al 1996; Behre et al 1997; Leifke et al 1998; Snyder et al 2000; Zacharin et al 2003; Wang, Cunningham et al 2004; Aminorroaya et al 2005; Benito et al 2005) and bone…”
Sims, N. A., Clément-Lacroix, P., Minet, D., Fraslon, C., Gaillard-Kelly, M., Resche-Rigon, M., & Baron, R. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200317246 · Cited by 200
Gonadal steroid–dependent effects on bone turnover and bone mineral density in men
Finkelstein, J. S., Lee, H., Leder, B. Z., Burnett-Bowie, S.-A. M., Goldstein, D. W., Hahn, C. W., Hirsch, S. C., Linker, A., Perros, N., Servais, A. B., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84137 · Cited by 198
Self-citationBone Loss in Men with Prostate Cancer Treated with Gonadotropin-Releasing Hormone Agonists
Stoch, S. A., Parker, R. A., Chen, L., Bubley, G. J., Ko, Y., Vincelette, A., & Greenspan, S. L. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7558 · Cited by 206
“Testosterone withdrawal is associated with an increase in total body fat and loss of lean body mass (15, 25); this is consistent with our findings.”
BackgroundResultInfluentialGao, W., Reiser, P. J., Coss, C. C., Phelps, M. A., Kearbey, J. D., Miller, D. D., & Dalton, J. T. (2005) · Endocrinology · doi:10.1210/en.2005-0572 · Cited by 196
Sinha‐Hikim, I., Arver, S., Beall, G. N., Shen, R., Guerrero, M., Sattler, F. R., Shikuma, C., Nelson, J. C., Landgren, B.-M., Mazer, N. A., et al. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.4.4718 · Cited by 192
Short-Term Oxandrolone Administration Stimulates Net Muscle Protein Synthesis in Young Men1
Sheffield-Moore, M., Urban, R. J., Wolf, S. E., Jiang, J., Catlin, D. H., Herndon, D. N., Wolfe, R. R., & Ferrando, A. A. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5923 · Cited by 199
Effect of testosterone replacement on trabecular architecture in hypogonadal men
Benito, M., Vasilic, B., Wehrli, F. W., Bunker, B., Wald, M., Gomberg, B., Wright, A. C., Zemel, B., Cucchiara, A., & Snyder, P. J. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.050606 · Cited by 188
Smith, M. R., Goode, M., Zietman, A. L., McGovern, F. J., Lee, H., & Finkelstein, J. S. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.01.174 · Cited by 188
Self-citationCorona, G., Giagulli, V. A., Maseroli, E., Vignozzi, L., Aversa, A., Zitzmann, M., Saad, F., Mannucci, E., & Maggi, M. (2016) · Journal of Endocrinological Investigation · doi:10.1007/s40618-016-0480-2 · Cited by 185
Mazziotti, G., Frara, S., & Giustina, A. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00005 · Cited by 181
Obesity and testicular function
Mah, P., & Wittert, G. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.06.007 · Cited by 179
Wang, C. E., Swerdloff, R. S., Iranmanesh, A., Dobs, A. S., Snyder, P. J., Cunningham, G. R., Matsumoto, A. M., Weber, T. J., Berman, N., & the Testosterone Gel Study Group (2001) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2001.01271.x · Cited by 176
The pathogenesis, diagnosis, investigation and management of osteoporosis
Sandhu, S. K., & Hampson, G. (2011) · Journal of Clinical Pathology · doi:10.1136/jcp.2010.077842 · Cited by 177
Dose-Dependent Effects of Testosterone on Regional Adipose Tissue Distribution in Healthy Young Men
Woodhouse, L. J., Gupta, N., Bhasin, M., Singh, A. B., Ross, R., Phillips, J., & Bhasin, S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031492 · Cited by 173
Osteoporosis in men: Epidemiology, diagnosis, prevention, and treatment
Olszynski, W. P., Davison, K. S., Adachi, J. D., Brown, J. P., Cummings, S. R., Hanley, D. A., Harris, S. P., Hodsman, A. B., Kendler, D. L., McClung, M. R., et al. (2004) · Clinical Therapeutics · doi:10.1016/s0149-2918(04)90002-1 · Cited by 166
New horizons in treatment of osteoporosis
Tabatabaei‐Malazy, O., Salari, P., Khashayar, P., & Larijani, B. A. (2017) · DARU Journal of Pharmaceutical Sciences · doi:10.1186/s40199-017-0167-z · Cited by 164
“Data of clinical trials confirms the beneficial effect of testosterone on BMD for at least 2 years [99].”
BackgroundMünzer, T., Harman, S. M., Hees, P. S., Shapiro, E., Christmas, C., Bellantoni, M. F., Stevens, T. E., O’Connor, K. G., Pabst, K. M., Clair, C. S., et al. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.8.7773 · Cited by 164
“Nonelderly GH-deficient patients and hypogonadal men, like healthy aged individuals, exhibit increases in total-body fat and abdominal sc and V fat, which are improved after GH administration (24 –28) or T treatment ( 29 ), respectively.”
BackgroundInfluentialBhasin, S., Storer, T. W., Asbel-Sethi, N., Kilbourne, A. M., Hays, R. D., Sinha‐Hikim, I., Shen, R., Arver, S., & Beall, G. N. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.9.5079 · Cited by 165
Gupta, V., Bhasin, S., Guo, W., Singh, R., Miki, R., Chauhan, P., Choong, K., Tchkonia, T., Lebrasseur, N. K., Flanagan, J. N., et al. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.08.019 · Cited by 162
“…of testosterone administration on fat mass and distribution in men have been inconsistent across trials (Snyder et al., 2000; Wang et al., 2000; Katznelson et al., 1996); although many trials in middle-aged and older men have reported a reduction in whole body fat mass during testosterone…”
ResultAllan, C. A., & McLachlan, R. I. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e3283398ee2 · Cited by 168
Androgen deprivation therapy for prostate cancer: new concepts and concerns
Smith, M. R. (2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e32814db88c · Cited by 157
ORWOLL, E. S. (1998) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70009-8 · Cited by 155
Miller, K. K., Meenaghan, E. M., Lawson, E. A., Misra, M., Gleysteen, S., Schoenfeld, D., Herzog, D. B., & Klibanski, A. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0380 · Cited by 160
Self-citationDeterioration of Trabecular Architecture in Hypogonadal Men
Benito, M., Gomberg, B. R., Wehrli, F. W., Weening, R., Zemel, B. S., Wright, A. C., Song, H. K., Cucchiara, A. J., & Snyder, P. J. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021429 · Cited by 155
“photon absorptiometry of the distal radius (10) and 9% in another study by dual energy x-ray absorptiometry of the lumbar spine (11).”
BackgroundRisks and benefits of testosterone therapy in older men
Spitzer, M., Huang, G., Basaria, S., Travison, T. G., & Bhasin, S. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.73 · Cited by 154
Erben, R. G., Eberle, J., Stähr, K., & Goldberg, M. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.6.1085 · Cited by 152
“((1,19,20))In a longitudinal study in a small group of ORX men, Stepa ́n et al.”
BackgroundMECHANISMS IN ENDOCRINOLOGY: The sexually dimorphic role of androgens in human metabolic disease
Schiffer, L., Kempegowda, P., Arlt, W., & O’Reilly, M. (2017) · European Journal of Endocrinology · doi:10.1530/eje-17-0124 · Cited by 162
Leifke, E., Korner, H., Link, T. M., Behre, H. M., Peters, P., & Nieschlag, E. (1998) · European Journal of Endocrinology · doi:10.1530/eje.0.1380051 · Cited by 150
“A recent study has demonstrated a change in biochemical serum markers of bone metabolism in response to testosterone replacement therapy, suggesting a reduction in bone remodelling ( 8 ).”
Influential
Metadata
- Authors
- Katznelson, L., Finkelstein, J. S., Schoenfeld, D. A., Rosenthal, D. I., Anderson, E. J., & Klibanski, A.
- Affiliations
- Massachusetts General Hospital (US)
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1996-12
- Volume
- 81
- Issue
- 12
- Pages
- 4358-4365
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W1974568933
- Semantic Scholar
- 829db808d1847d263af6c33d3397743284ea9f83
- Cited by
- 791
- References
- 38
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 12 · 2023: 13 · 2022: 16 · 2021: 15 · 2020: 15 · 2019: 14 · 2018: 17 · 2017: 18 · 2016: 22 · 2015: 24 · 2014: 17 · 2013: 29 · 2012: 35
- FWCI
- 19.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5f32dk008738-02)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-08738)
- National Center for Research Resources (RR 01066, M01RR001066)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Keywords
- testosterone replacement therapy, testosterone enanthate, bone mineral density, trabecular bone density, lean body mass, body composition, fat mass, central hypogonadism, hypergonadotropic hypogonadism, bone-specific alkaline phosphatase, urinary deoxypyridinoline, bone turnover markers, men's health, osteoporosis prevention
- MeSH terms
- Adult, Aged, Body Composition, Bone Development, Humans, Hypogonadism, Cholesterol, HDL, Longitudinal Studies, Male, Middle Aged, Parathyroid Hormone, Growth Hormone, Testosterone, Bone Density
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