The effect of changes in adiposity on testosterone levels in older men: longitudinal results from the Massachusetts Male Aging Study
Abstract
Objective: Changes in adiposity affecting total testosterone (TT) and free testosterone (FT) levels have not been examined in a population-based survey. We aimed to determine whether changes in adiposity predict follow-up levels and rates of change in TT, FT and sex hormone-binding globulin (SHBG) in men. Design: The Massachusetts Male Aging Study is a randomly sampled, population-based cohort interviewed at baseline (T1, 1987–1989; n = 1709; aged 40–70 years) and followed-up approximately 9 years later (T2, 1995–1997; n = 1156). Men were categorized as overweight (body mass index (BMI) ≥ 25 kg/m 2) or having obesity (BMI ≥ 30 kg/m 2), waist obesity (waist circumference ≥ 102 cm), or waist-to-hip ratio (WHR) obesity (WHR>0.95). For each adiposity group, we constructed four categories to represent changes between T1 and T2: overweight (or obese, etc.) at neither wave, T1 only, T2 only, or both waves. Results: After adjustment for confounding variables, men who were overweight at T2 only, or at both waves, had significantly lower mean T2 TT and SHBG levels than men in the neither group (P<0.05). Mean FT did not differ between any overweight group and the neither group. Men who were obese at both times, had the highest mean BMI, the highest fraction of severely obese men, and significantly greater rate of decline in FT than the neither group. Conclusions: In men who become overweight, the greater rate of decline in TT, but not FT, is related mostly to a lesser age-related increase in SHBG. Since weight gain is highly prevalent in older men, over-reliance on TT levels in the diagnosis of androgen deficiency could result in substantial misclassification.
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Obese men are prone to lower total T as well as lower SHBG concentrations, implying a substantial risk for misclassification when using 'normal' reference ranges.
“Imposed by their obese status, these men are prone to lower total T as well as lower SHBG concentrations, implying a substantial risk for misclassification when using ‘normal’ reference ranges [180, 181].”
From Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology (2022) · cites this paper as [180]
Cites
Chobanian, A. V., Bakris, G. L., Black, H. R., Cushman, W. C., Green, L. A., Izzo, J. L., Jones, D. W., Materson, B. J., Oparil, S., Wright, J. T., et al. (2003) · Hypertension · doi:10.1161/01.hyp.0000107251.49515.c2 · Cited by 13,271 · see citing works
A Critical Evaluation of Simple Methods for the Estimation of Free Testosterone in Serum
Vermeulen, A., Verdonck, L., & Kaufman, J. M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.10.6079 · Cited by 3,824 · see citing works
Feldman, H. A., Longcope, C., Derby, C. A., Johannes, C. B., Araujo, A. B., Coviello, A. D., Bremner, W. J., & McKinlay, J. B. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.2.8201 · Cited by 1,861 · see citing works
Self-citation(1998) · Obesity Research · doi:10.1002/j.1550-8528.1998.tb00690.x · Cited by 758 · see citing works
Ferrini, R. L., & Barrett-Connor, E. (1998) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009519 · Cited by 473 · see citing works
Vermeulen, A. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.5.1821 · Cited by 455 · see citing works
Low serum testosterone and sex-hormone-binding-globulin in massively obese men
GLASS, A. R., SWERDLOFF, R. S., BRAY, G. A., DAHMS, W. T., & ATKINSON, R. L. (1977) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-45-6-1211 · Cited by 430 · see citing works
Leifke, E., Gorenoi, V., Wichers, C., Von Zur Mühlen, A., Von Büren, E., & Brabant, G. (2000) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2000.01159.x · Cited by 262 · see citing works
PLYMATE, S. R., TENOVER, J. S., & BREMNER, W. J. (1989) · Journal of Andrology · doi:10.1002/j.1939-4640.1989.tb00120.x · Cited by 239 · see citing works
Birkeland, K. I., Hanssen, K. F., Torjesen, P. A., & Vaaler, S. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.2.8432768 · Cited by 161 · see citing works
Pasquali, R., Vicennati, V., Bertazzo, D., Casimirri, F., Pascal, G., Tortelli, O., & Labate, A. M. M. (1997) · Metabolism · doi:10.1016/s0026-0495(97)90159-1 · Cited by 130 · see citing works
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Bhasin, S., Cunningham, G. R., Hayes, F. J., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., & Montori, V. M. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2354 · Cited by 1,954 · see citing works
Self-citationTestosterone Therapy in Men With Hypogonadism: An Endocrine Society Clinical Practice Guideline.
Bhasin, S., Brito, J. P., Cunningham, G. R., Hayes, F. J., Hodis, H. N., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., Wu, F. C., & Yialamas, M. A. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00229 · Cited by 1,736 · see citing works
Self-citationWu, F. C. W., Tajar, A., Pye, S. R., Silman, A. J., Finn, J. D., O'Neill, T. W., Bartfai, G., Casanueva, F., Forti, G., Giwercman, A., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1972 · Cited by 939 · see citing works
Prevalence of Symptomatic Androgen Deficiency in Men
Araujo, A. B., Esche, G. R., Kupelian, V., O’Donnell, A. B., Travison, T. G., Williams, R. E., Clark, R. V., & McKinlay, J. B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1245 · Cited by 720 · see citing works
Self-citationEndogenous Testosterone and Mortality in Men: A Systematic Review and Meta-Analysis
Araujo, A. B., Dixon, J. M., Suarez, E. A., Murad, M. H., Guey, L. T., & Wittert, G. A. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1137 · Cited by 671 · see citing works
Camacho, E. M., Huhtaniemi, I. T., O'Neill, T. W., Finn, J. D., Pye, S. R., Lee, D. M., Tajar, A., Bartfai, G., Boonen, S., Casanueva, F. F., et al. (2013) · European Journal of Endocrinology · doi:10.1530/eje-12-0890 · Cited by 392 · see citing works
Travison, T. G., Vesper, H. W., Orwoll, E., Wu, F., Kaufman, J. M., Wang, Y., Lapauw, B., Fiers, T., Matsumoto, A. M., & Bhasin, S. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-2935 · Cited by 326 · see citing works
Self-citationMichalakis, K., Mintziori, G., Kaprara, A., Tarlatzis, B. C., & Goulis, D. G. (2013) · Metabolism · doi:10.1016/j.metabol.2012.08.012 · Cited by 321 · see citing works
Clark, J. E. (2015) · Journal of Diabetes & Metabolic Disorders · doi:10.1186/s40200-015-0154-1 · Cited by 158 · see citing works
Risks 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 · see citing works
Self-citationHormone Replacement Therapy and Physical Function in Healthy Older Men. Time to Talk Hormones?
Giannoulis, M. G., Martin, F. C., Nair, K. S., Umpleby, A. M., & Sonksen, P. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1002 · Cited by 132 · see citing works
Cooper, L. A., Page, S. T., Amory, J. K., Anawalt, B. D., & Matsumoto, A. M. (2015) · Clinical Endocrinology · doi:10.1111/cen.12768 · Cited by 117 · see citing works
Narinx, N., David, K., Walravens, J., Vermeersch, P., Claessens, F., Fiers, T., Lapauw, B., Antonio, L., & Vanderschueren, D. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04562-1 · Cited by 96 · see citing works
Testosterone replacement therapy: for whom, when and how?
Tsametis, C. P., & Isidori, A. M. (2018) · Metabolism · doi:10.1016/j.metabol.2018.03.007 · Cited by 96 · see citing works
Travison, T. G., Shackelton, R., Araujo, A. B., Hall, S. A., Williams, R. E., Clark, R. V., O'Donnell, A. B., & McKinlay, J. B. (2008) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2008.01679.x · Cited by 89 · see citing works
Self-citationHaider, A., Gooren, L. J. G., Padungtod, P., & Saad, F. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1202774 · Cited by 83 · see citing works
Haring, R., Xanthakis, V., Coviello, A., Sullivan, L., Bhasin, S., Wallaschofski, H., Murabito, J. M., & Vasan, R. S. (2012) · International Journal of Andrology · doi:10.1111/j.1365-2605.2012.01285.x · Cited by 22 · see citing works
Self-citationClark, J. E. (2012) · Journal of Diabetes & Metabolic Disorders · doi:10.1186/2251-6581-11-19 · Cited by 19 · see citing works
- Authors
- Mohr, B. A., Bhasin, S., Link, C. L., O’Donnell, A. B., & McKinlay, J. B.
- Affiliations
- New England Research Institutes (US)
- ORCID
- Bhasin, Shalender
- Venue
- European Journal of Endocrinology
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-09
- Volume
- 155
- Issue
- 3
- Pages
- 443-452
- ISSN
- 0804-4643 (ISSN-L)
- 1479-683X
- OpenAlex
- W2104301254
- Cited by
- 163
- References
- 11
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 1 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 8 · 2019: 6 · 2018: 6 · 2017: 8 · 2016: 12 · 2015: 13 · 2014: 6 · 2013: 8 · 2012: 14
- FWCI
- 8.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (7p01ag004673-05)
- National Institute on Aging (AG 04673)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 51345, R01DK044995, DK44995, R01DK051345)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- adiposity, testosterone, free testosterone, sex hormone-binding globulin, older men, obesity, overweight, waist circumference, waist-to-hip ratio, body mass index, androgen deficiency, weight gain, longitudinal change
- MeSH terms
- Adult, Aged, Aging, Anthropometry, Body Composition, Follow-Up Studies, Humans, Life Style, Longitudinal Studies, Male, Massachusetts, Middle Aged, Motor Activity, Sex Hormone-Binding Globulin, Testosterone, Body Mass Index, Adiposity
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