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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In men, bone mineral density at the greater trochanter, femoral neck and the lumbar spine is negatively correlated with concentrations of SHBG.
“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]
Table III (Results) reports negative SHBG–BMD correlation coefficients at the greater trochanter, femoral neck, and lumbar spine in men over 65. However, only the greater-trochanter association was statistically significant, as the Abstract explicitly notes; the claim omits that distinction. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe relationship between testosterone levels in aging and bone health is uncertain because studies have produced conflicting results.
“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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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 · see citing works
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 · see citing works
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 · see citing works
Khosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 934 · see citing works
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 · see citing works
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 · see citing works
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× · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
Slemenda, C. W., Longcope, C., Peacock, M., Hui, S. L., & Johnston, C. C. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118382 · Cited by 301 · see citing works
Self-citationSecular trends in the incidence of hip fractures
Melton, J. J., O’Fallon, W. M., & Riggs, B. L. (1987) · Calcified Tissue International · doi:10.1007/bf02555245 · Cited by 279 · see citing works
Heritability of bone mass: a longitudinal study in aging male twins.
Christian, J. C., Yu, P., Slemenda, C. W., & Johnston, C. C. (1989) · PubMed · Cited by 253 · see citing works
Self-citationLong-Term Bone Loss in Men: Effects of Genetic and Environmental Factors
Slemenda, C. W., Christian, J. C., Reed, T., Reister, T. K., Williams, C. J., & Johnston, C. C. (1992) · Annals of Internal Medicine · doi:10.7326/0003-4819-117-4-286 · Cited by 222 · see citing works
Self-citationSlemenda, C. W., Peacock, M., Hui, S. L., Zhou, L., & Johnston, C. C. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.4.676 · Cited by 211 · see citing works
Self-citationSex hormones and bone mineral density in elderly men
Murphy, S., Khaw, K.-T., Cassidy, A., & Compston, J. E. (1993) · Bone and Mineral · doi:10.1016/s0169-6009(08)80022-0 · Cited by 187 · see citing works
Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
Smith, E. P., Boyd, J. A., Frank, G. R., Takahashi, H., Cohen, R. M., SPECKER, B. L., Williams, T. C., Lubahn, D. B., & Korach, K. S. (1995) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-199503000-00021 · Cited by 149 · see citing works
Meier, D. E., Orwoll, E. S., Keenan, E. J., & Fagerstrom, R. M. (1987) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1987.tb02308.x · Cited by 131 · see citing works
New biomarkers of bone resorption.
Eyre, D. W. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.3.1740477 · Cited by 125 · see citing works
Anderson, F. H., Francis, R. M., & Faulkner, K. (1996) · Bone · doi:10.1016/8756-3282(95)00441-6 · Cited by 119 · see citing works
Bone mineral density, muscle strength, and recreational exercise in men
Snow-Harter, C., Whalen, R. T., Myburgh, K. H., Arnaud, S. B., & Marcus, R. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071108 · Cited by 110 · see citing works
Lima, F. R., Baima Filho, J., Kochem, J., Pereira, R. M. R., & Yoshinari, N. (1997) · PubMed · Cited by 99 · see citing works
Mann, T., Oviatt, S. K., Wilson, D. R., Nelson, D. B., & ORWOLL, E. S. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071120 · Cited by 86 · see citing works
Lack of association between free testosterone and bone density separate from age in elderly males
Drinka, P. J., Olson, J., Bauwens, S. F., Voeks, S. K., Carlson, I. H., & Wilson, M. J. (1993) · Calcified Tissue International · doi:10.1007/bf00675629 · Cited by 80 · see citing works
Free Estradiol, Free Testosterone, and Sex Hormone-Binding Globulin in Perimenopausal Women*
Longcope, C., Hui, S. L., & Johnston, C. C. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-64-3-513 · Cited by 72 · see citing works
Self-citationBone mass and biochemical parameters of bone metabolism in men with spinal osteoporosis
Resch, H., Pietschmann, P., Woloszczuk, W., Krexner, E., Bernecker, P. M., & Willvonseder, R. (1992) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1992.tb01503.x · Cited by 65 · see citing works
Age-adjusted incidence of hip fractures
Kannus, P., Parkkari, J. P., & Niemi, S. T. (1995) · The Lancet · doi:10.1016/s0140-6736(95)92679-8 · Cited by 55 · see citing works
95007346 Estrogen replacement therapy and fractures in older women
Cauley, J. A., Seeley, D. G., Ensrud, K. E., Ettinger, B. B., Black, D., & Cummings, S. R. (1995) · Maturitas · doi:10.1016/0378-5122(95)99336-z · Cited by 34 · see citing works
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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 · see citing works
Riggs, B. L., Khosla, S., & Melton, L. J. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.5.763 · Cited by 1,143 · see citing works
Khosla, S. (1998) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.7.2266 · Cited by 447 · see citing works
Khosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 934 · see citing works
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 · see citing works
Estrogens and androgens in skeletal physiology and pathophysiology
Almeida, M., Laurent, M. R., Dubois, V., Claessens, F., O'Brien, C. A., Bouillon, R., Vanderschueren, D., & Manolagas, S. C. (2017) · Physiological Reviews · doi:10.1152/physrev.00033.2015 · Cited by 860 · see citing works
Falahati-Nini, A., Riggs, B. L., Atkinson, E. J., O’Fallon, W. M., Eastell, R., & Khosla, S. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10942 · Cited by 757 · see citing works
Increased Bone Mass as a Result of Estrogen Therapy in a Man with Aromatase Deficiency
Bilezikian, J. P., Morishima, A., Bell, J., & Grumbach, M. M. (1998) · New England Journal of Medicine · doi:10.1056/nejm199808273390905 · Cited by 624 · see citing works
van den Beld, A. W., de Jong, F. H., Grobbee, D. E., Pols, H. A. P., & Lamberts, S. W. J. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.9.6825 · Cited by 616 · see citing works
Aging and bone loss: new insights for the clinician
Demontiero, O., Vidal, C., & Duque, G. (2011) · Therapeutic Advances in Musculoskeletal Disease · doi:10.1177/1759720x11430858 · Cited by 565 · see citing works
Riggs, B. L., Melton, L. J., Robb, R. A., Camp, J. J., Atkinson, E. J., McDaniel, L. J., Amin, S., Rouleau, P. A., & Khosla, S. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.071020 · Cited by 543 · see citing works
Andropause: clinical implications of the decline in serum testosterone levels with aging in men
Matsumoto, A. M. (2002) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/57.2.m76 · Cited by 490 · see citing works
Kenny, A. M., Prestwood, K. M., Gruman, C. A., Marcello, K. M., & Raisz, L. G. (2001) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/56.5.m266 · Cited by 456 · see citing works
The Estrogen Receptor β Subtype: A Novel Mediator of Estrogen Action in Neuroendocrine Systems
Kuiper, G. G. J. M., Shughrue, P. J., Merchenthaler, I. J., & Gustafsson, J.-Α. (1998) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1998.0170 · Cited by 439 · see citing works
Estrogen: Consequences and Implications of Human Mutations in Synthesis and Action
Grumbach, M. M., & Auchus, R. J. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.12.6290 · Cited by 412 · see citing works
Estrogen receptor specificity in the regulation of skeletal growth and maturation in male mice
Vidal, O., Lindberg, M. K., Hollberg, K., Baylink, D. J., Andersson, G., Lubahn, D. B., Mohan, S., Gustafsson, J.-Α., & Ohlsson, C. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.10.5474 · Cited by 385 · see citing works
Eisman, J. A. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.6.0384 · Cited by 380 · see citing works
Pathophysiology of Age-Related Bone Loss and Osteoporosis
Khosla, S., & Riggs, B. L. (2005) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2005.07.009 · Cited by 376 · see citing works
Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action
Hammond, G. L. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0070 · Cited by 356 · see citing works
Khosla, S., Melton, L. J., & Riggs, B. L. (2010) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.262 · Cited by 338 · see citing works
Mellström, D., Johnell, O., Ljunggren, Ö., Eriksson, A.-L., Lorentzon, M., Mallmin, H., Holmberg, A., Redlund-Johnell, I., Orwoll, E., & Ohlsson, C. (2006) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.060110 · Cited by 337 · see citing works
Estrogen and the Male Skeleton
Khosla, S., Melton, L. J., & Riggs, B. L. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8417 · Cited by 308 · see citing works
Amin, S., Zhang, Y., Sawin, C. T., Evans, S. R., Hannan, M. T., Kiel, D. P., Wilson, P. W. F., & Felson, D. T. (2000) · Annals of Internal Medicine · doi:10.7326/0003-4819-133-12-200012190-00010 · Cited by 290 · see citing works
The Pathophysiology and Treatment of Osteoporosis
Drake, M. T., Clarke, B. L., & Lewiecki, E. M. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.06.006 · Cited by 292 · see citing works
Differential Effects of Androgens and Estrogens on Bone Turnover in Normal Men
Leder, B. Z., LeBlanc, K. M., Schoenfeld, D. A., Eastell, R., & Finkelstein, J. S. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021036 · Cited by 283 · see citing works
Osteoporosis, genetics and hormones
Rizzoli, R., Bonjour, J., & Ferrari, S. (2001) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0260079 · Cited by 275 · see citing works
Armstrong, V. J., Muzylak, M., Sunters, A., Zaman, G., Saxon, L., Price, J. S., & Lanyon, L. E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703224200 · Cited by 273 · see citing works
Older Men With Low Serum Estradiol and High Serum SHBG Have an Increased Risk of Fractures
Mellström, D., Vandenput, L., Mallmin, H., Holmberg, A. H., Lorentzon, M., Odén, A., Johansson, H., Orwoll, E. S., Labrie, F., Karlsson, M. K., et al. (2008) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.080518 · Cited by 279 · see citing works
Bioavailable Estradiol May Be an Important Determinant of Osteoporosis in Men: The MINOS Study
Szulc, P. (2001) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.1.192 · Cited by 169 · see citing works
Clarke, B. L., & Khosla, S. (2010) · Radiologic Clinics of North America · doi:10.1016/j.rcl.2010.02.014 · Cited by 258 · see citing works
Smith, M. R., Fallon, M. A., Lee, H., & Finkelstein, J. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032058 · Cited by 248 · see citing works
Biological Role of Estrogen and Estrogen Receptors
Nilsson, S. V., & Gustafsson, J.-Å. (2002) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230290771438 · Cited by 244 · see citing works
LeBlanc, E. S., Nielson, C. M., Marshall, L. M., Lapidus, J. A., Barrett-Connor, E., Ensrud, K. E., Hoffman, A. R., Laughlin, G., Ohlsson, C., Orwoll, E. S., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0206 · Cited by 240 · see citing works
Osteoprotegerin Serum Levels in Men: Correlation with Age, Estrogen, and Testosterone Status
Szulc, P., Hofbauer, L. C., Heufelder, A. E., Roth, S., & Delmas, P. D. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.7.7657 · Cited by 250 · see citing works
Meier, C. (2008) · Archives of Internal Medicine · doi:10.1001/archinternmed.2007.2 · Cited by 274 · see citing works
Pathogenesis of Age-Related Bone Loss in Humans
Khosla, S. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls163 · Cited by 222 · see citing works
Ferretti, J. L., Capozza, R. F., Cointry, G. R., García, S. L. O., Plotkin, H., Filgueira, M. L. A., & Zanchetta, J. (1998) · Bone · doi:10.1016/s8756-3282(98)00046-5 · Cited by 220 · see citing works
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Hormonal and Metabolic Changes of Aging and the Influence of Lifestyle Modifications
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Bone Aging, Cellular Senescence, and Osteoporosis
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Oh, K. W., Lee, W., Rhee, E., Baek, K. H., Yoon, K., Kang, M. I., Yun, E. J., Park, C., Ihm, S. H., Choi, M. G., et al. (2005) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2005.02312.x · Cited by 198 · see citing works
Bone Has a Sexually Dimorphic Response to Aromatase Deficiency
Öz, O. K., Zerwekh, J. E., Fisher, C., Graves, K. H., Nanu, L., Millsaps, R., & Simpson, E. R. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.3.507 · Cited by 194 · see citing works
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Gennari, L., Merlotti, D., Martini, G., Gonnelli, S., Franci, B., Campagna, S., Lucani, B., Dal Canto, N., Valenti, R., Gennari, C., et al. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030736 · Cited by 235 · see citing works
Estradiol, Testosterone, and the Risk for Hip Fractures in Elderly Men from the Framingham Study
Amin, S., Zhang, Y., Felson, D. T., Sawin, C. T., Hannan, M. T., Wilson, P. W. F., & Kiel, D. P. (2006) · The American Journal of Medicine · doi:10.1016/j.amjmed.2005.10.048 · Cited by 191 · see citing works
Aromatase Activity and Bone Homeostasis in Men
Gennari, L., Nuti, R., & Bilezikian, J. P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1717 · Cited by 190 · see citing works
Khosla, S., Atkinson, E. J., Dunstan, C. R., & O’Fallon, W. M. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8397 · Cited by 191 · see citing works
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Fred Saad, C., Adachi, J. D., Brown, J. P., Canning, L. A., Gelmon, K. A., Josse, R. G., & Pritchard, K. I. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.4184 · Cited by 182 · see citing works
Androgen deprivation therapy for prostate cancer results in significant loss of bone density
Wei, J., Gross, M. D., Jaffe, C. A., Gravlin, K., Lahaie, M., Faerber, G. J., & Cooney, K. A. (1999) · Urology · doi:10.1016/s0090-4295(99)00301-5 · Cited by 170 · see citing works
Bone Resorption and Osteoporotic Fractures in Elderly Men: The Dubbo Osteoporosis Epidemiology Study
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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 168 · see citing works
Osteoporosis in Men Treated With Androgen Deprivation Therapy for Prostate Cancer
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Gennari, L., Masi, L., Merlotti, D., Picariello, L., Falchetti, A., Tanini, A., Mavilia, C., Monte, F. D., Gonnelli, S., Lucani, B., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031342 · Cited by 158 · see citing works
Androgen deprivation therapy for prostate cancer: new concepts and concerns
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Lee, H., McGovern, K., Finkelstein, J. S., & Smith, M. R. (2005) · Cancer · doi:10.1002/cncr.21381 · Cited by 148 · see citing works
Burnett-Bowie, S.-A. M., McKay, E. A., Lee, H., & Leder, B. Z. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0739 · Cited by 146 · see citing works
Goderie-Plomp, H. W., van der Klift, M., de Ronde, W., Albert Hofman, D., de Jong, F. H., & Pols, H. A. P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-022041 · Cited by 146 · see citing works
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Osteoporosis in Men Treated With Androgen Deprivation Therapy for Prostate Cancer
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Determinants of Peak Bone Mass and Mechanisms of Bone Loss
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Anemia as an independent prognostic factor for survival in patients with cancer
Caro, J. J., Salas, M., Ward, A., & Goss, G. D. (2001) · Cancer · doi:10.1002/1097-0142(20010615)91:12 · Cited by 947 · see citing works
Mueller, A., Haeberle, L., Zollver, H., Claassen, T., Kronawitter, D., Oppelt, P. G., Cupisti, S., Beckmann, M. W., & Dittrich, R. (2010) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2010.01912.x · Cited by 132 · see citing works
Movérare, S., Venken, K., Eriksson, A.-L., Andersson, N., Skrtic, S., Wergedal, J. E., Mohan, S., Salmon, P., Bouillon, R., Gustafsson, J.-Α., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2233084100 · Cited by 131 · see citing works
Estrogens as regulators of bone health in men
Vandenput, L., & Ohlsson, C. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.112 · Cited by 129 · see citing works
Amin, S., & Felson, D. T. (2001) · Rheumatic Disease Clinics of North America · doi:10.1016/s0889-857x(05)70186-1 · Cited by 123 · see citing works
Coin, A., Perissinotto, E., Enzi, G., Zamboni, M. M., İnelmen, E., Frigo, A. C., Manzato, E., Busetto, L., Buja, A., & Sergi, G. (2007) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602779 · Cited by 122 · see citing works
Smith, M. R., Malkowicz, S. B., Chu, F. M., Forrest, J. B., Price, D., SIEBER, P. R., Barnette, K. G., Rodriguez, D., & Steiner, M. S. (2007) · The Journal of Urology · doi:10.1016/j.juro.2007.08.137 · Cited by 117 · see citing works
Doran, P. M., Riggs, B. L., Atkinson, E. J., & Khosla, S. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.11.2118 · Cited by 115 · see citing works
Ke, H. Z., Qi, H., Crawford, D. T., Chidsey-Frink, K. L., Simmons, H. A., & Thompson, D. D. (2000) · Endocrinology · doi:10.1210/endo.141.4.7408 · Cited by 115 · see citing works
Dietary Protein Deficiency Induces Osteoporosis in Aged Male Rats
Bourrin, S., Toromanoff, A., Ammann, P., Bonjour, J., & Rizzoli, R. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.8.1555 · Cited by 114 · see citing works
Taxel, P., Kennedy, D., FALL, P. M., Willard, A. K., Clive, J. M., & Raisz, L. G. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7541 · Cited by 113 · see citing works
Determinants of bone density in healthy older men with low testosterone levels
Kenny, A. M., Prestwood, K. M., Marcello, K. M., & Raisz, L. G. (2000) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/55.9.m492 · Cited by 111 · see citing works
Eisman, J. A. (1999) · Endocrine Reviews · doi:10.1210/er.20.6.788 · Cited by 111 · see citing works
Osteoporosis and male age-related hypogonadism: role of sex steroids on bone (patho)physiology
Rochira, V., Balestrieri, A., Madeo, B., Zirilli, L., Granata, A. R. M., & Carani, C. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02088 · Cited by 107 · see citing works
Andropause: is androgen replacement therapy indicated for the aging male?
Hijazi, R. A., & Cunningham, G. R. (2005) · Annual Review of Medicine · doi:10.1146/annurev.med.56.082103.104518 · Cited by 105 · see citing works
Barreto, F. C., Barreto, D. V., Moysés, R. M. A., Neves, C. L., Jorgetti, V., Draibe, S. A., Canziani, M. E. F., & Carvalho, A. B. (2006) · Kidney International · doi:10.1038/sj.ki.5000311 · Cited by 101 · 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
Osteoporosis in men: a potential role for the sex hormone binding globulin
Legrand, E., Hedde, C., Gallois, Y., Degasne, I., Boux de Casson, F., Mathieu, E., Baslé, M.-F., Chappard, D., & Audran, M. (2001) · Bone · doi:10.1016/s8756-3282(01)00478-1 · Cited by 127 · see citing works
The effects of testosterone on osteoporosis in men
Francis (1999) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1999.00730.x · Cited by 102 · see citing works
Genetics of osteoporosis: role of steroid hormone receptor gene polymorphisms
Gennari, L., Becherini, L., Falchetti, A., Masi, L., Massart, F., & Brandi, M. L. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00043-2 · Cited by 102 · see citing works
Osteoporosis during androgen deprivation therapy for prostate cancer
Smith, M. R. (2002) · Urology · doi:10.1016/s0090-4295(02)01579-0 · Cited by 100 · see citing works
Wong, S. Y. S., Lau, E. M. C., Lynn, H., Leung, P., Woo, J., Cummings, S., & ORWOLL, E. S. (2004) · Osteoporosis International · doi:10.1007/s00198-004-1730-2 · Cited by 98 · see citing works
Gennari, L., & Bilezikian, J. P. (2007) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2007.03.008 · Cited by 98 · see citing works
Ebeling, P. R. (1998) · Drugs & Aging · doi:10.2165/00002512-199813060-00002 · Cited by 96 · see citing works
Pottelbergh, I. V., Lumbroso, S., Goemaere, S., Sultan, C., & Kaufman, J. (2001) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2001.01403.x · Cited by 95 · see citing works
Estrogens and Bone Health in Men
Khosla, S., Melton, L. J., & Riggs, B. L. (2001) · Calcified Tissue International · doi:10.1007/s00223-001-1044-8 · Cited by 95 · see citing works
Järvinen, T. L. N., Kannus, P., Pajamäki, I., Vuohelainen, T., Tuukkanen, J., Järvinen, M., & Sievänen, H. T. (2003) · Bone · doi:10.1016/s8756-3282(03)00100-5 · Cited by 95 · see citing works
Anawalt, B. D., & Merriam, G. R. (2001) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70206-1 · Cited by 93 · see citing works
Zaman, G., Saxon, L., Sunters, A., Hilton, H., Underhill, P., Williams, D., Price, J. S., & Lanyon, L. E. (2009) · Bone · doi:10.1016/j.bone.2009.10.021 · Cited by 92 · see citing works
Lindberg, M., Erlandsson, M. C., Alatalo, S., Windahl, S. H., Andersson, G. N., Halleen, J., Carlsten, H., Gustafsson, J., & Ohlsson, C. (2001) · Journal of Endocrinology · doi:10.1677/joe.0.1710425 · Cited by 91 · see citing works
Gillberg, P., Johansson, A. G., & Ljunghall, S. (1999) · Calcified Tissue International · doi:10.1007/s002239900604 · Cited by 91 · see citing works
Christmas, C., O'Connor, K. G., Harman, S. M., Tobin, J. D., Münzer, T., Bellantoni, M. F., Clair, C. S., Pabst, K. M., Sorkin, J. D., & Blackman, M. R. (2002) · The Journals of Gerontology Series A · doi:10.1093/gerona/57.1.m12 · Cited by 90 · see citing works
The importance of oestrogens in males
de Ronde, W., Pols, H. A. P., van Leeuwen, J. P. T. M., & de Jong, F. H. (2003) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2003.01669.x · Cited by 85 · see citing works
Kirchengast, S., Peterson, B., Hauser, G., & Knogler, W. (2001) · Maturitas · doi:10.1016/s0378-5122(01)00205-5 · Cited by 83 · see citing works
ERβ a Novel Estrogen Receptor Offers the Potential for New Drug Development
Nilsson, S. V., Kuiper, G. G. J. M., & Gustafsson, J.-Α. (1998) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(98)00096-4 · Cited by 80 · see citing works
Khosla, S. (2001) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.8.3555 · Cited by 522 · see citing works
Pande, I., & Francis, R. M. (2001) · Best Practice & Research Clinical Rheumatology · doi:10.1053/berh.2001.0158 · Cited by 79 · see citing works
Ke, H. Z., Qi, H., Chidsey-Frink, K. L., Crawford, D. T., & Thompson, D. D. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.4.765 · Cited by 80 · see citing works
Testosterone Prevents Orchidectomy-Induced Bone Loss in Estrogen Receptor-α Knockout Mice
Vandenput, L., EDERVEEN, A. G. H., Erben, R. G., Stähr, K., Swinnen, J. V., Herck, E. V., Verstuyf, A., Boonen, S., Bouillon, R., & Vanderschueren, D. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5101 · Cited by 79 · see citing works
- 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 › Genetics › 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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