The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.
Sex steroids and bone mass in older men. Positive associations with serum estrogens and negative associations with androgens.
Open accessAbstract
The purpose of this study was to determine whether bone density in older men was associated with serum sex steroids or sex hormone binding globulin (SHBG). Bone density and sex steroids were measured in men over age 65 at 6-mo intervals for an average of 2.1 yr. Bone density was significantly positively associated with greater serum E2 concentrations (+0.21 < r < +0.35; 0.01 < P < 0.05) at all skeletal sites. There were weak negative correlations between serum testosterone and bone density (-0.20 < r < -0.28; 0.03 < P < 0.10) at the spine and hip. SHBG was negatively associated only with bone density in the greater trochanter (r = -0.26, P < 0.05). Greater body weight was associated with lower serum testosterone and SHBG, and greater E2. Because of these associations, regression models which adjusted for age, body weight, and serum sex steroids were constructed; these accounted for 10-30% of the variability in bone density, and showed consistent, significant positive associations between bone density and serum E2 concentrations in men, even after adjustments for weight and SHBG. These data suggest that estrogens may play an important role in the development or maintenance of the male skeleton, much as is the case for the female skeleton. These data also indicate that, within the normal range, lower serum testosterone concentrations are not associated with low bone density in men.
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“Moreover, in men, bone mineral density (BMD) at the greater trochanter, femoral neck and the lumbar spine is negatively correlated with concentrations of SHBG [146, 150–152].”
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 [151]
Experimental — accuracy not yet measuredIn the citing paper
“These confounding results leave uncertainty in the relationship between T levels in aging and bone health.”
From Hormonal and Metabolic Changes of Aging and the Influence of Lifestyle Modifications (2021) · cites this paper as [175]
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Citations
Cites
Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., & Korach, K. S. (1994) · New England Journal of Medicine · doi:10.1056/nejm199410203311604 · Cited by 2,471
Cooper, C. C., Atkinson, E. J., MichaelO'Fallon, W., & Melton, J. L. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650070214 · Cited by 1,526
Morishima, A., Grumbach, M. M., Simpson, E. R., Fisher, C., & Qin, K. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.12.8530621 · Cited by 1,416
Khosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 943
LONG-TERM PREVENTION OF POSTMENOPAUSAL OSTEOPOROSIS BY ŒSTROGEN
Lindsay, R., Aitken, J. M., Anderson, L., Hart, D., Macdonald, E., & Clarke, A. (1976) · The Lancet · doi:10.1016/s0140-6736(76)92217-0 · Cited by 875
Estrogen Replacement Therapy and Fractures in Older Women
Cauley, J. A., Seeley, D. G., Ensrud, K. E., Ettinger, B., Black, D., & Cummings, S. R. (1995) · Annals of Internal Medicine · doi:10.7326/0003-4819-122-1-199501010-00002 · Cited by 808
Katznelson, L., Finkelstein, J. S., Schoenfeld, D. A., Rosenthal, D. I., Anderson, E. J., & Klibanski, A. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.12.8954042 · Cited by 791 · cited 2×
“Men with spinal crush fractures have also been shown to have significantly higher serum concentrations of markers of skeletal remodeling (osteocalcin) (22), and it is possible that this mechanism, which is clearly central to the development of low bone mass in women, is also involved in the development of low bone mas…”
BackgroundGenetic Factors in Determining Bone Mass
Smith, D. M., Nance, W. E., Kang, K.-W., Christian, J. C., & Johnston, C. C. (1973) · Journal of Clinical Investigation · doi:10.1172/jci107476 · Cited by 579
Self-citationPrediction of osteoporotic fractures by postural instability and bone density.
Nguyen, T. V., Sambrook, P. N., Kelly, P. J., Jones, G., Lord, S. R., Freund, J., & Eisman, J. A. (1993) · BMJ · doi:10.1136/bmj.307.6912.1111 · Cited by 568
ANDROGENS DIRECTLY STIMULATE PROLIFERATION OF BONE CELLS IN VITRO
Kasperk, C. H., Wergedal, J. E., Farley, J. R., Linkhart, T. A., Turner, R. T., & Baylink (1989) · Endocrinology · doi:10.1210/endo-124-3-1576 · Cited by 398
Cited by
Sorted by citations
Sex Steroids and the Construction and Conservation of the Adult Skeleton
Riggs, B. L., Khosla, S., & Melton, L. J. (2002) · Endocrine Reviews · doi:10.1210/edrv.23.3.0465 · Cited by 1,846
“Several groups have reported substantial decreases in serum levels of free or Bio sex steroid levels with aging (17, 160, 161).”
BackgroundMethodRiggs, B. L., Khosla, S., & Melton, L. J. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.5.763 · Cited by 1,161
Khosla, S. (1998) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.7.2266 · Cited by 447
“(21) found that serum estradiol (E2), but not T, levels were positively associated with BMD in men over age 65 yr.”
InfluentialKhosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 943
The Decline of Androgen Levels in Elderly Men and Its Clinical and Therapeutic Implications
Kaufman, J. M., & Vermeulen, A. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0013 · Cited by 1,079
Metadata
- Authors
- Slemenda, C. W., Longcope, C., Zhou, L., Hui, S. L., Peacock, M., & Johnston, C. C.
- Affiliations
- Indiana University Indianapolis (US)
- University of Massachusetts Chan Medical School (US)
- Indiana University School of Medicine (US)
- Indiana University Bloomington (US)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 1997-10-01
- Volume
- 100
- Issue
- 7
- Pages
- 1755-1759
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508359
- OpenAlex
- W1993231839
- Cited by
- 455
- References
- 28
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 6 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 9 · 2018: 7 · 2017: 6 · 2016: 8 · 2015: 8 · 2014: 6 · 2013: 7 · 2012: 16
- FWCI
- 24.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p01ag005793-15)
- National Institute on Aging (P01-AG-05793)
- National Center for Research Resources (M01RR000750)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Keywords
- sex steroids, bone mineral density, older men, serum estrogen, estradiol, testosterone, sex hormone-binding globulin, bone mass, body weight, male skeleton
- MeSH terms
- Aged, Androgens, Body Constitution, Dehydroepiandrosterone, Estradiol, Estrogens, Estrone, Humans, Longitudinal Studies, Male, Middle Aged, Prospective Studies, Regression Analysis, Sex Hormone-Binding Globulin, Testosterone, Models, Statistical, Bone Density, Dehydroepiandrosterone Sulfate
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