Age‐related changes of serum sex hormones, insulin‐like growth factor‐1 and sex‐hormone binding globulin levels in men: cross‐sectional data from a healthy male cohort
Abstract
The age‐dependent decline of the gonadal and somatotopic axis has been causally linked to frailty in the elderly by their effects on muscle mass and bone mineral density. However, for healthy men data on serum oestrogens and androgens, as well as IGF‐1, as a common outcome measure covering the whole adult age range are scarce. We therefore studied healthy, nonobese male subjects between 20 and 80 years of age to asses their morning concentrations of total (T), free (FT), bioavailable testosterone (bT), oestradiol (E2), bioavailable oestradiol (bE2), oestrone (E1), sex‐hormone binding globulin (SHBG), and insulin‐like growth factor 1 (IGF‐1). Five hundred and seventy‐two male healthy volunteers with a BMI < 30 kg/m 2 recruited from regular blood donors and senior sports clubs participated in the study. Serum samples were obtained during morning hours and T, FT, E2, E1, SHBG, albumin and IGF‐1 were measured by radio‐immunoassay systems. In addition, bT and bE2 were calculated. A potential relationship between sex hormones and IGF‐1 was tested by multiple regression analysis including age and BMI. Ageing was negatively related to serum levels of sex steroids and IGF‐1 (both P < 0·0001) with a mean decrease (youngest vs. oldest) of 51% for T, 64% for FT, 78% for bT, 32% for E2, 62% for bE2, 29% for E1 and 51% for IGF‐1 starting in early adulthood whereas SHBG increased after the 5th decade of life (anovaP < 0·001). The decline of sex hormones and IGF‐1 remained relatively unchanged after adjustment for BMI. Multiple regression analysis revealed an age‐and BMI– independent association between oestradiol and IGF‐1. In contrast to the female situation sex hormones in healthy, nonobese men decline continuously with age. This process has already started in the third decade, and is paralleled by a decline of IGF‐1 serum levels leading to a substantial proportion of elderly men with markedly lowered serum levels of bioavailable sex hormones and IGF‐1 compared to the young adult male range. With the recent demonstration of beneficial effects of androgen replacement therapy in healthy males on general well being, muscle mass and bone mineral density the present data may underline the importance of more detailed studies on the biological significance of hormonal changes in men with age.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Mean total and bioavailable testosterone levels in diabetic men were lower in all age groups compared with data reported by Leifke et al. in healthy nonobese males and by Muller et al. in independently living men.
“The mean total and bioavailable testosterone levels in our diabetic men were also lower in all age-groups compared with data reported by Leifke et al. (11) in healthy nonobese males and by Muller et al. (33) in independently living men.”
From Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes (2007) · cites this paper as [11]
In our laboratory, bioavailable testosterone below the normal range (<2.5 nmol/l) is consistent with overt hypogonadism in young healthy men, whereas a significant proportion of patients with bioavailable testosterone between 2.5 and 4 nmol/l are also hypogonadal as shown by Leifke et al.
“In our laboratory, bioavailable testosterone below the normal range (Ͻ2.5 nmol/l) is consistent with overt hypogonadism in young healthy men, whereas a significant proportion of patients with bioavailable testosterone between 2.5 and 4 nmol/l are also hypogonadal as shown in the study by Leifke et al. (11).”
From Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes (2007) · cites this paper as [11]
SHBG rises with age, and thus free testosterone decreases more rapidly than total testosterone in older men.
“A confounding factor is that SHBG rises with age, and thus free testosterone decreases more rapidly than total testosterone in older men (11).”
From Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes (2007) · cites this paper as [11]
Cites
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
Effects of Human Growth Hormone in Men over 60 Years Old
Rudman, D. R., Feller, A. G., Nagraj, H. S., Gergans, G. A., Lalitha, P. Y., Goldberg, A. F., Schlenker, R. A., Cohn, L., Rudman, I. W., & Mattson, D. E. (1990) · New England Journal of Medicine · doi:10.1056/nejm199007053230101 · Cited by 1,551 · see citing works
Gray, A., Feldman, H. A., McKinlay, J. B., & Longcope, C. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-73-5-1016 · Cited by 1,104 · see citing works
Södergard, R., Bäckström, T., Shanbhag, V., & Carstensen, H. (1982) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(82)90038-3 · Cited by 1,080 · see citing works
Lamberts, S. W. J., van den Beld, A. W., & van der Lely, A.-J. (1997) · Science · doi:10.1126/science.278.5337.419 · Cited by 980 · see citing works
Human growth hormone and human aging
CORPAS, E., HARMAN, S. M., & BLACKMAN, M. R. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-1-20 · Cited by 911 · see citing works
Morley, J. E., Kaiser, F. E., Perry, H. M., Patrick, P., Morley, P. M. K., Stauber, P. M., Vellas, B., Baumgartner, R. N., & Garry, P. J. (1997) · Metabolism · doi:10.1016/s0026-0495(97)90057-3 · Cited by 830 · see citing works
Anker, S. D., Chua, T. P., Ponikowski, P., Harrington, D., Swan, J. W., Kox, W. J., Poole-Wilson, P. A., & Coats, A. J. S. (1997) · Circulation · doi:10.1161/01.cir.96.2.526 · Cited by 800 · 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 · see citing works
PLYMATE, S. R., MATEJ, L. A., JONES, R. E., & FRIEDL, K. E. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-3-460 · Cited by 693 · see citing works
Rosenbaum, M. S., Leibel, R. L., & Hirsch, J. (1997) · New England Journal of Medicine · doi:10.1056/nejm199708073370606 · Cited by 581 · see citing works
Effect of Testosterone Treatment on Body Composition and Muscle Strength in Men Over 65 Years of Age
Snyder, P. J. (1999) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.8.2647 · Cited by 531 · 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
Bioavailable Testosterone and Depressed Mood in Older Men: The Rancho Bernardo Study
Barrett-Connor, E., von Mühlen, D. G., & Kritz-Silverstein, D. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5495 · Cited by 472 · see citing works
Effect of Testosterone Treatment on Bone Mineral Density in Men Over 65 Years of Age
Snyder, P. J. (1999) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.6.1966 · Cited by 460 · see citing works
Vermeulen, A. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.5.1821 · Cited by 455 · see citing works
Testosterone replacement therapy improves mood in hypogonadal men--a clinical research center study
Wang, C., Alexander, G. M., Berman, N., Salehian, B., Davidson, T., McDonald, V., Steiner, B., Hull, L., Callegari, C. C., & Swerdloff, R. S. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.10.8855804 · Cited by 453 · see citing works
Khosla, S. (1998) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.7.2266 · Cited by 447 · see citing works
Stepan, J. J., Lachman, M., ZVĚŘINA, J., Pacovský, V., & Baylink, D. J. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-69-3-523 · Cited by 423 · see citing works
Field, A. E., Colditz, G. A., Willett, W. C., Longcope, C., & McKinlay, J. B. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.5.7962322 · Cited by 421 · see citing works
Testosterone Action, Deficiency, Substitution
Rajfer, J. (2005) · The Journal of Urology · doi:10.1097/01.ju.0000163660.02216.be · Cited by 323 · see citing works
Testosterone, body composition and aging.
Vermeulen, A. T., Goemaere, S., & Kaufman, J. (1999) · PubMed · Cited by 280 · see citing works
Björntorp, P. A. (1997) · The Lancet · doi:10.1016/s0140-6736(97)04503-0 · Cited by 234 · see citing works
Weissberger, A. J., & Ho, K. K. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.6.8501143 · Cited by 185 · see citing works
Declining gonadal function in elderly men
Kaufman, J. M., & Vermeulen, A. (1997) · Baillière s Clinical Endocrinology and Metabolism · doi:10.1016/s0950-351x(97)80302-3 · Cited by 181 · see citing works
The influence of aging on plasma sex hormones in men: the Telecom study.
Simon, D., Preziosi, P., Barrett-Connor, E., Roger, M., Saint-Paul, M., Nahoul, K., & Papoz, L. (1992) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116365 · Cited by 166 · cited 1× · see citing works
“Studies results with respect to age-dependent changes of serum oestrogens are conflicting (Gray et al., 1991; Simon et al., 1992; Vermeulen et al., 1996; Khosla et al., 1998).”
ResultTestosterone administration increases insulin-like growth factor-I levels in normal men
Hobbs, C., Plymate, S. R., Rosen, C. J., & Adler, R. A. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.3.7690364 · Cited by 163 · see citing works
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 · see citing works
Self-citationDonaghy, A. J., Ross, R. J. M., Gimson, A., Hughes, S. C., Holly, J. M. P., & Williams, R. L. (1995) · Hepatology · doi:10.1002/hep.1840210313 · Cited by 148 · see citing works
Long-Term Effects of Growth Hormone (GH) Replacement in Men with Childhood-Onset GH Deficiency1
ter Maaten, J. C., de Boer, H., Otto Kamp, B., Stuurman, L. M., & van der Veen, E. A. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.7.5851 · Cited by 142 · see citing works
Liu, L. L., Merriam, G. R., & Sherins, R. J. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-64-4-651 · Cited by 134 · see citing works
Ulloa‐Aguirre, A., Blizzard, R. M., Garcı́a-Rubi, E., Rogol, A. D., Link, K., Christie, C. M., JOHNSON, M. L., & Veldhuis, J. D. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-4-846 · Cited by 127 · see citing works
Mulligan, T., Iranmanesh, A., Kerzner, R., Demers, L., & Veldhuis, J. (1999) · European Journal of Endocrinology · doi:10.1530/eje.0.1410257 · Cited by 121 · see citing works
Abbasi, A. A., Drinka, P. J., Mattson, D. E., & Rudman, D. (1993) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1993.tb06764.x · Cited by 93 · see citing works
Moll, G., ROSENFIEL, R. L., & Helke, J. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-52-5-868 · Cited by 92 · see citing works
Long-Term Effects of Growth Hormone (GH) Replacement in Men with Childhood-Onset GH Deficiency
ter Maaten, J. C. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.7.2373 · Cited by 89 · see citing works
Metzger, D. L., & Kerrigan, J. R. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.5.8496305 · Cited by 77 · see citing works
Cuneo, R. C., Hickman, P. E., Wallace, J. D., Teh, B. T., Ward, G., Veldhuis, J. D., & Waters, M. J. (1995) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1995.tb02031.x · Cited by 69 · see citing works
Serum Leptin in Elderly People: Associations with Sex Hormones, Insulin, and Adipose Tissue Volumes
Baumgartner, R., Ross, R. R., Waters, D. L., Brooks, W. M., Morley, J. E., Montoya, G. D., & Garry, P. J. (1999) · Obesity Research · doi:10.1002/j.1550-8528.1999.tb00695.x · Cited by 69 · see citing works
Wallymahmed, Foy, & Macfarlane (1999) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1999.00802.x · Cited by 59 · see citing works
Pardridge, W. M. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb48863.x · Cited by 48 · see citing works
Duclos, M., Corcuff, J., Rashedi, M., Fougere, V., & Manier, G. (1996) · European Journal of Applied Physiology · doi:10.1007/bf00334419 · Cited by 45 · see citing works
Belgorosky, A., Martínez, A., Domené, H. M., Heinrich, J. J., Bergadá, C., & Rivarola, M. A. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-6-1107 · Cited by 40 · see citing works
Unanswered Questions Concerning the Treatment of Hyposomatotropism and Hypogonadism in Elderly Men
Rudman, D., & Shetty, K. R. (1994) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1994.tb04975.x · Cited by 35 · see citing works
Deijen, J. B., & van der Veen, E. A. (1999) · PubMed · Cited by 17 · see citing works
Growth Hormone and Growth Hormone Secretagogues in Adults
Cummings, D. E., & Merriam, G. R. (1999) · Humana Press eBooks · doi:10.1007/978-1-59259-700-0_4 · Cited by 10 · see citing works
Androgen Replacement Therapy of Male Hypogonadism
Meikle, A. W. (1999) · Humana Press eBooks · doi:10.1007/978-1-59259-700-0_16 · Cited by 7 · see citing works
Flagged first, then by citations
3 of the 50 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Physical activity and exercise: Strategies to manage frailty
Angulo, J., El Assar, M., Álvarez-Bustos, A., & Rodríguez-Mañas, L. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101513 · Cited by 771 · see citing works
Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes
Kapoor, D., Aldred, H., Clark, S., Channer, K. S., & Jones, T. H. (2007) · Diabetes Care · doi:10.2337/dc06-1426 · Cited by 493 · 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
Cooke, P. S., Nanjappa, M. K., Ko, C. J., Prins, G. S., & Hess, R. A. (2017) · Physiological Reviews · doi:10.1152/physrev.00018.2016 · Cited by 475 · see citing works
Vermeulen, A., Kaufman, J. M., Goemaere, S., & Van Pottelberg, I. (2002) · The Aging Male · doi:10.1080/tam.5.2.98.102 · Cited by 452 · see citing works
Endogenous sex hormones in men aged 40-80 years
Muller, M., den Tonkelaar, I., Thijssen, J., Grobbee, D., & van der Schouw, Y. (2003) · European Journal of Endocrinology · doi:10.1530/eje.0.1490583 · Cited by 346 · see citing works
Endogenous Sex Hormones and Progression of Carotid Atherosclerosis in Elderly Men
Muller, M., van den Beld, A. W., Bots, M. L., Grobbee, D. E., Lamberts, S. W. J., & van der Schouw, Y. T. (2004) · Circulation · doi:10.1161/01.cir.0000125854.51637.06 · Cited by 318 · see citing works
Testosterone and Estradiol among Older Men
ORWOLL, E. S., Lambert, L. C., Marshall, L. M., Phipps, K. R., Blank, J. B., Barrett-Connor, E. L., Cauley, J. A., Ensrud, K. E., & Cummings, S. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1830 · Cited by 319 · see citing works
Evaluation of assays available to measure free testosterone
Morley, J. E., Patrick, P., & Perry, H. M. (2002) · Metabolism · doi:10.1053/meta.2002.31975 · Cited by 309 · see citing works
Allan, C. A., Strauss, B. J. G., Burger, H. G., Forbes, E. A., & McLachlan, R. I. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1291 · Cited by 298 · see citing works
Dihydrotestosterone: Biochemistry, Physiology, and Clinical Implications of Elevated Blood Levels
Swerdloff, R. S., Dudley, R. E., Page, S. T., Wang, C., & Salameh, W. A. (2017) · Endocrine Reviews · doi:10.1210/er.2016-1067 · Cited by 247 · see citing works
Hormones and Prostate Cancer: What's Next?
Hsing, A. W. (2001) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a000795 · Cited by 216 · see citing works
Shefer, G., Rauner, G., Yablonka‐Reuveni, Z., & Benayahu, D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013307 · Cited by 211 · see citing works
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Phillips, B. E., Szewczyk, N. J., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2016) · The Journal of Physiology · doi:10.1113/jp272857 · Cited by 204 · see citing works
Hormonal and Metabolic Changes of Aging and the Influence of Lifestyle Modifications
Pataky, M. W., Young, W. F., & Nair, K. S. (2021) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2020.07.033 · Cited by 207 · see citing works
Testosterone levels and cognition in elderly men: A review
Holland, J., Bandelow, S., & Hogervorst, E. (2011) · Maturitas · doi:10.1016/j.maturitas.2011.05.012 · Cited by 194 · see citing works
Angulo, J., Assar, M. E., & Rodríguez‐Mañas, L. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.06.001 · Cited by 185 · see citing works
Neuroprotective role of testosterone in the nervous system.
Białek, M., Zaremba, P., Borowicz, K. K., & Czuczwar, S. J. (2004) · PubMed · Cited by 170 · see citing works
Testosterone and cognitive function: current clinical evidence of a relationship.
Beauchet, O. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02306 · Cited by 177 · see citing works
Comparison of screening questionnaires for the diagnosis of hypogonadism
Morley, J. E., Perry, H. M., Kevorkian, R. T., & Patrick, P. (2006) · Maturitas · doi:10.1016/j.maturitas.2005.07.004 · Cited by 168 · see citing works
Allan, C. A., & McLachlan, R. I. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e3283398ee2 · Cited by 168 · see citing works
Frailty in the elderly: contributions of sarcopenia and visceral protein depletion
VanItallie, T. B. (2003) · Metabolism · doi:10.1016/s0026-0495(03)00297-x · Cited by 161 · see citing works
The European Male Ageing Study (EMAS): design, methods and recruitment
Lee, D. M., O’Neill, T. W., Pye, S. R., Silman, A. J., Finn, J. D., Pendleton, N., Tajar, A., Bártfai, G., Casanueva, F. F., Forti, G., et al. (2008) · International Journal of Andrology · doi:10.1111/j.1365-2605.2008.00879.x · Cited by 161 · see citing works
Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men
Allen, N. E., Appleby, P. N., Davey, G. K., & Key, T. J. (2002) · Cancer Causes & Control · doi:10.1023/a:1015238102830 · Cited by 153 · see citing works
Kelsey, T., Li, L. Q., Mitchell, R. T., Whelan, A. D., Anderson, R. A., & Wallace, W. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109346 · Cited by 147 · see citing works
Hormone 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
Age‐related changes in testosterone and the role of replacement therapy in older men
Allan, C. A., & McLachlan, R. I. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02002.x · Cited by 128 · see citing works
Molecular Endocrinology and Physiology of the Aging Central Nervous System
Smith, R. G., Betancourt, L., & Sun, Y. (2005) · Endocrine Reviews · doi:10.1210/er.2002-0017 · Cited by 127 · see citing works
Yeap, B. B., Almeida, O. P., Hyde, Z., Norman, P. E., Chubb, S. A. P., Jamrozik, K. D., & Flicker, L. A. (2007) · European Journal of Endocrinology · doi:10.1530/eje-06-0714 · Cited by 126 · see citing works
Contributions of sex to cerebrovascular function and pathology
Robison, L. S., Gannon, O. J., Salinero, A. E., & Zuloaga, K. L. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.030 · Cited by 124 · see citing works
Mohr, B. A., Bhasin, S., Link, C. L., O’Donnell, A. B., & McKinlay, J. B. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02241 · Cited by 163 · see citing works
Vikan, T., Schirmer, H., Njølstad, I., & Svartberg, J. (2010) · European Journal of Endocrinology · doi:10.1530/eje-09-0943 · Cited by 151 · see citing works
Erlandson, K. M., Allshouse, A. A., Jankowski, C. M., MaWhinney, S., Kohrt, W. M., & Campbell, T. (2013) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/qai.0b013e318289bb7e · Cited by 119 · 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
Manuck, S. B., Marsland, A. L., Flory, J. D., Gorka, A. X., Ferrell, R. E., & Hariri, A. R. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.04.013 · Cited by 114 · see citing works
Testosterone and Atherosclerosis in Aging Men
Jones, R. D., Nettleship, J. E., Kapoor, D., Jones, H. T., & Channer, K. S. (2005) · American Journal of Cardiovascular Drugs · doi:10.2165/00129784-200505030-00001 · Cited by 111 · see citing works
Chubb, S. A. P., Hyde, Z., Almeida, O. P., Flicker, L. A., Norman, P. E., Jamrozik, K. D., Hankey, G. J., & Yeap, B. B. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0893 · Cited by 109 · see citing works
The Association Between IGF-1 Levels and the Histologic Severity of Nonalcoholic Fatty Liver Disease
Dichtel, L. E., Corey, K. E., Misdraji, J., Bredella, M. A., Haines, M. S., Osganian, S. A., Young, B. J., Sung, J. C., & Miller, K. K. (2017) · Clinical and Translational Gastroenterology · doi:10.1038/ctg.2016.72 · Cited by 106 · see citing works
Life history context of reproductive aging in a wild primate model
Jeanne Altmann, A., Gesquiere, L. R., Galbany, J., Onyango, P. O., & Alberts, S. C. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05531.x · Cited by 102 · see citing works
Deletion of IGF-1 Receptors in Cardiomyocytes Attenuates Cardiac Aging in Male Mice
Ock, S., Lee, W. S., Ahn, J., Kim, H. M., Kang, H., Kim, H.-S., Jo, D., Abel, E. D., Lee, T. J., & Kim, J. (2015) · Endocrinology · doi:10.1210/en.2015-1709 · Cited by 101 · see citing works
Ishunina, T. A., van Beurden, D., van der Meulen, G., Unmehopa, U. A., Hol, E. M., Huitinga, I., & Swaab, D. F. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.03.010 · Cited by 100 · see citing works
Body mass index in early and mid-adulthood, and subsequent mortality: a historical cohort study
Jeffreys, M., McCarron, P. A., Gunnell, D., McEwen, J., & Smith, G. D. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802414 · Cited by 98 · see citing works
van Beek, R. D., Smit, M., van den Heuvel‐Eibrink, M. M., de Jong, F. H., Hakvoort-Cammel, F. G. A. J., van den Bos, C., van den Berg, H., Weber, R. F. A., Pieters, R., & Keizer‐Schrama, S. M. P. F. D. M. (2007) · Human Reproduction · doi:10.1093/humrep/dem313 · Cited by 96 · see citing works
Tunçdoğan, A., Acar, O. A., & Stam, D. A. (2016) · The Leadership Quarterly · doi:10.1016/j.leaqua.2016.10.011 · Cited by 94 · see citing works
Jasuja, G. K., Travison, T. G., Davda, M. N., Murabito, J. M., Basaria, S. S., Zhang, A., Kushnir, M. M., Rockwood, A. L., Meikle, W. A., Pencina, M. J., et al. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls216 · Cited by 90 · see citing works
Endocrinological derangements in COPD
Laghi, F. A., Adıgüzel, N., & Tobin, M. J. (2009) · European Respiratory Journal · doi:10.1183/09031936.00103708 · Cited by 90 · see citing works
Emmerson, E., Campbell, L., Davies, F. C. J., Ross, N. L., Ashcroft, G. S., Krust, A., Chambon, P., & Hardman, M. J. (2012) · Journal of Investigative Dermatology · doi:10.1038/jid.2012.228 · Cited by 88 · see citing works
Fabbri, E., An, Y., González‐Freire, M., Zoli, M., Maggio, M. G., Studenski, S. A., Egan, J. M., Chia, C. W., & Ferrucci, L. (2016) · The Journals of Gerontology Series A · doi:10.1093/gerona/glw021 · Cited by 87 · see citing works
Shamloul, R. M., Ghanem, H. M., Fahmy, I., El-Meleigy, A., Ashoor, S., El-Nashaar, A., & Kamel, I. (2005) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2005.00071.x · Cited by 86 · see citing works
Mechanisms of sex and age differences in ventricular repolarization in humans
Vicente, J., Johannesen, L., Galeotti, L., & Strauss, D. G. (2014) · American Heart Journal · doi:10.1016/j.ahj.2014.07.010 · Cited by 85 · see citing works
Frequent occurrence of pituitary apoplexy in patients with non‐functioning pituitary adenoma
Nielsen, E., Lindholm, J., Bjerre, P., Christiansen, J. S., Hagen, C., Juul, S., Jørgensen, J. O. L., Kruse, A., & Laurberg, P. T. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02463.x · Cited by 83 · see citing works
Off-label use of hormones as an antiaging strategy: a review
Samaras, N., Papadopoulou, M.-A., Samaras, D., & Ongaro, F. (2014) · Clinical Interventions in Aging · doi:10.2147/cia.s48918 · Cited by 81 · see citing works
Edelstein, R. S., Wardecker, B. M., Chopik, W. J., Moors, A. C., Shipman, E. L., & Lin, N. J. (2014) · American Journal of Human Biology · doi:10.1002/ajhb.22670 · Cited by 79 · see citing works
Hypogonadism in Men with Chronic Obstructive Pulmonary Disease
Laghi, F. A., Antonescu-Turcu, A., Collins, E. G., Segal, J. P., Tobin, D. E., Jubran, A., & Tobin, M. J. (2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200501-037oc · Cited by 78 · see citing works
Childhood body mass index and later cancer risk: A 50‐year follow‐up of the Boyd Orr study
Jeffreys, M., Smith, G. D., Martin, R. M., Frankel, S., & Gunnell, D. (2004) · International Journal of Cancer · doi:10.1002/ijc.20423 · Cited by 78 · see citing works
Age and testosterone mediate influenza pathogenesis in male mice
Steeg, L. G. V., Vermillion, M. S., Hall, O. J., Alam, O., McFarland, R., Chen, H., Zirkin, B. R., & Klein, S. L. (2016) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00352.2016 · Cited by 77 · see citing works
Growth Factors, Nutrient Signaling, and Cardiovascular Aging
Fontana, L., Vinciguerra, M., & Longo, V. D. (2012) · Circulation Research · doi:10.1161/circresaha.111.246470 · Cited by 76 · see citing works
Are declining testosterone levels a major risk factor for ill-health in aging men?
Yeap, B. B. (2008) · International Journal of Impotence Research · doi:10.1038/ijir.2008.60 · Cited by 75 · see citing works
Edelstein, R. S., Chopik, W. J., Saxbe, D. E., Wardecker, B. M., Moors, A. C., & LaBelle, O. P. (2017) · Developmental Psychobiology · doi:10.1002/dev.21469 · Cited by 73 · see citing works
“To be eligible, both partners had to be between the ages of 18 and 45 (because of agerelated changes in hormones; Leifke et al., 2000), living together, expecting their first child, and within the first two trimesters of”
Riquelme (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00027 · Cited by 71 · see citing works
Rolf, C., von Eckardstein, S., Koken, U. H., & Nieschlag, E. (2002) · European Journal of Endocrinology · doi:10.1530/eje.0.1460505 · Cited by 72 · see citing works
The role of testosterone in the pathogenesis of prostate cancer
Imamoto, T., Suzuki, H., Yano, M., Kawamura, K., Kamiya, N., Araki, K., Komiya, A., Nihei, N., Naya, Y., & Ichikawa, T. (2008) · International Journal of Urology · doi:10.1111/j.1442-2042.2008.02074.x · Cited by 70 · see citing works
Firtser, S., Juonala, M., Magnussen, C. G., Jula, A., Loo, B.-M., Marniemi, J., Viikari, J. S. A., Toppari, J., Perheentupa, A. H., Hutri‐Kähönen, N., et al. (2012) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2012.02.020 · Cited by 69 · see citing works
Hypopituitarism and mortality in pituitary adenoma
Lindholm, J., Nielsen, E. H., Bjerre, P., Christiansen, J. S., Hagen, C., Juul, S., Jørgensen, J., Kruse, A., Laurberg, P., & Stochholm, K. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02545.x · Cited by 68 · see citing works
Body composition, metabolic syndrome and testosterone in ageing men
Allan, C. A., Strauss, B. J. G., & McLachlan, R. I. (2007) · International Journal of Impotence Research · doi:10.1038/sj.ijir.3901552 · Cited by 67 · see citing works
Growth Factors as Mediators of Exercise Actions on the Brain
Llorens-Martı́n, M., Torres‐Alemán, I., & Trejo, J. L. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8026-1 · Cited by 65 · see citing works
Allan, C. A., Forbes, E. A., Strauss, B. J., & McLachlan, R. I. (2008) · International Journal of Impotence Research · doi:10.1038/ijir.2008.22 · Cited by 65 · see citing works
Reference Ranges for Serum Dehydroepiandrosterone Sulfate and Testosterone in Adult Men
Friedrich, N., Völzke, H., Rosskopf, D., Steveling, A., Krebs, A., Nauck, M. A., & Wallaschofski, H. (2008) · Journal of Andrology · doi:10.2164/jandrol.108.005561 · Cited by 64 · see citing works
Wong, H., DeLellis, K., Probst-Hensch, N. M., Koh, W., Berg, D. V. D., Lee, H.-P., Yu, M. C., & Ingles, S. A. (2005) · PubMed · doi:10.5167/uzh-18854 · Cited by 61 · see citing works
Techniques that acquire donor profiling information from fingermarks — A review
van Dam, A., van Beek, F. T., Aalders, M. C. G., van Leeuwen, T. G. J. M., & Lambrechts, S. A. G. (2016) · Science & Justice · doi:10.1016/j.scijus.2015.12.002 · Cited by 60 · see citing works
Morley, J. E., & Perry, H. M. (2003) · Clinics in Geriatric Medicine · doi:10.1016/s0749-0690(02)00105-2 · Cited by 60 · see citing works
White, E. C., & Graham, B. M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.011 · Cited by 59 · see citing works
The serum level of free testosterone is reduced in amyotrophic lateral sclerosis
Militello, A., Vitello, G., Lunetta, C., Toscano, A., Maiorana, G., Piccoli, T., & Bella, V. L. (2002) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(01)00688-8 · Cited by 60 · see citing works
Circulating levels of IGF1 are associated with muscle strength in middle-aged- and oldest-old women
Taekema, D. G., Ling, C. H. Y., Blauw, G. J., Meskers, C. G. M., Westendorp, R. G. J., de Craen, A. J. M., & Maier, A. B. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0703 · Cited by 56 · see citing works
Tendon stem/progenitor cell ageing: Modulation and rejuvenation
Dai, G.-C., Li, Y., Chen, M., Lu, P., & Rui, Y. (2019) · World Journal of Stem Cells · doi:10.4252/wjsc.v11.i9.677 · Cited by 55 · see citing works
Rohrmann, S., Platz, E. A., Selvin, E., Shiels, M. S., Joshu, C. E., Menke, A., Feinleib, M., Basaria, S. S., Rifai, N., Dobs, A. S., et al. (2011) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2011.04043.x · Cited by 54 · see citing works
Healthier lifestyle predicts higher circulating testosterone in older men: the Health In Men Study
Yeap, B. B., Almeida, O. P., Hyde, Z., Norman, P. E., Chubb, S. A. P., Jamrozik, K. D., Hankey, G. J., & Flicker, L. A. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03372.x · Cited by 53 · see citing works
Salini, V., Vanni, D., Pantalone, A., & Abate, M. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00228 · Cited by 51 · see citing works
Fortier, L. A., KORNATOWSKI, M. A., Mohammed, H. O., JORDAN, M. T., O'CAIN, L. C., & Stevens, W. B. (2005) · Equine Veterinary Journal · doi:10.2746/0425164054406838 · Cited by 51 · see citing works
Hsu, B., Seibel, M. J., Cumming, R. G., Blyth, F., Naganathan, V., Bleicher, K., Couteur, D. G. L., Waite, L. M., & Handelsman, D. J. (2016) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2904 · Cited by 49 · see citing works
Genes within the serotonergic system are differentially expressed in human brain
Sugden, K., Tichopád, A., Khan, N., Craig, I., & D’Souza, U. M. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-50 · Cited by 45 · see citing works
Plasma IGF-1 is negatively correlated with body mass in a comparison of 36 mammalian species
Stuart, J. A., & Page, M. M. (2010) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2010.08.005 · Cited by 45 · see citing works
Maggio, M. G., Vita, F. D., Fisichella, A., Lauretani, F., Ticinesi, A., Ceresini, G., Cappola, A. R., Ferrucci, L., & Ceda, G. P. (2015) · International Journal of Endocrinology · doi:10.1155/2015/292574 · Cited by 44 · see citing works
Temporal Trend in Androgen Status and Androgen-Sensitive Outcomes in Older Men
Hsu, B., Cumming, R. G., Hirani, V., Blyth, F., Naganathan, V., Couteur, D. G. L., Seibel, M. J., Waite, L. M., & Handelsman, D. J. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3810 · Cited by 45 · see citing works
Endocrine Alterations in the Aging Male
Elmlinger, M. W., Dengler, T., Weinstock, C., & Kuehnel, W. (2003) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2003.142 · Cited by 45 · see citing works
The Potential Roles of Tendon Stem/Progenitor Cells in Tendon Aging
Li, Y., Dai, G.-C., Shi, L., Lin, Y., Chen, M., Li, G., & Rui, Y. (2018) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x13666181017112233 · Cited by 44 · see citing works
Effects of Boron-Containing Compounds on Liposoluble Hormone Functions
Estevez-Fregoso, E., Kılıç, A., Rodríguez-Vera, D., Nicanor-Juárez, L. E., Romero-Rizo, C. E. M., Farfán‐García, E. D., & Soriano-Ursua, M. A. (2023) · Inorganics · doi:10.3390/inorganics11020084 · Cited by 45 · see citing works
Maggio, M. G., Lauretani, F., Vita, F., Basaria, S. S., Lippi, G., Buttò, V., Luci, M., Cattabiani, C., Ceresini, G., Verzicco, I., et al. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113196660062 · Cited by 44 · see citing works
Envejecimiento y composición corporal: la obesidad sarcopénica en España
Gómez‐Cabello, A., Rodríguez, G. V., Vila‐Maldonado, S., Casajús, J. A., & Ara, I. (2012) · Redalyc (Universidad Autónoma del Estado de México) · doi:10.3305/nh.2012.27.1.5502 · Cited by 43 · see citing works
The Relationship between Testosterone and Sexual Function in Depressed and Healthy Men
Rizvi, S. J., Kennedy, S. H., Ravindran, L. N., Giacobbe, P., Eisfeld, B. S., Mancini, D., & McIntyre, R. S. (2009) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01504.x · Cited by 44 · see citing works
Decline of serum levels of free testosterone in aging healthy Chinese men
Li, J., Li, X. Y., Li, M., Zhang, G. K., Ma, F. L., Liu, Z. M., Zhang, N. Y., & Meng, P. (2005) · The Aging Male · doi:10.1080/13685530500356010 · Cited by 43 · see citing works
The association between obesity and the diagnosis of androgen deficiency in symptomatic ageing men
Allan, C. A., Strauss, B. J., Burger, H., Forbes, E. A., & McLachlan, R. I. (2006) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.2006.tb00639.x · Cited by 43 · see citing works
Kacker, R., Traish, A. M., & Morgentaler, A. (2012) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2012.02726.x · Cited by 42 · see citing works
Wong, H., DeLellis, K., Probst-Hensch, N. M., Koh, W., Berg, D. V. D., Lee, H.-P., Yu, M. C., & Ingles, S. A. (2005) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.144.14.1 · Cited by 62 · see citing works
Gender Differences in Skin Aging and the Changing Profile of the Sex Hormones with Age
Farage, M. A. (2012) · Journal of Steroids & Hormonal Science · doi:10.4172/2157-7536.1000109 · Cited by 41 · see citing works
Gonadal sex steroid status and bone health in middle-aged and elderly European men
The EMAS Study Group, Vanderschueren, D., Pye, S. R., Venken, K., Borghs, H., Gaytant, J., Huhtaniemi, I. T., Adams, J. E., Ward, K. A., Bártfai, G., et al. (2009) · Osteoporosis International · doi:10.1007/s00198-009-1144-2 · Cited by 39 · see citing works
The neurobiology of insulin-like growth factor I: From neuroprotection to modulation of brain states
Núñez, Á., Zegarra-Valdivia, J. A., de Sevilla, D. F., Pignatelli, J., & Aleman, I. T. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02136-6 · Cited by 40 · see citing works
Boesen, A., Dideriksen, K., Couppé, C., Magnusson, S. P., Schjerling, P., Boesen, M., Aagaard, P., Kjær, M., & Langberg, H. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01077.2013 · Cited by 39 · see citing works
Brabant, G. E. (2003) · European Journal of Endocrinology · doi:10.1530/eje.0.148s015 · Cited by 39 · see citing works
Self-citationHaren, M. T., Morley, J. E., Chapman, I. M., O’Loughlin, P. D., & Wittert, G. (2002) · Climacteric · doi:10.1080/cmt.5.1.15.25 · Cited by 38 · see citing works
- Authors
- Leifke, E., Gorenoi, V., Wichers, C., Von Zur Mühlen, A., Von Büren, E., & Brabant, G.
- Affiliations
- Medizinische Hochschule Hannover (DE)
- ORCID
- Brabant, Georg
- Venue
- Clinical Endocrinology
- Publisher
- Wiley
- Published
- 2000-12-19
- Volume
- 53
- Issue
- 6
- Pages
- 689-695
- ISSN
- 0300-0664 (ISSN-L)
- 1365-2265
- OpenAlex
- W2075284108
- Cited by
- 262
- References
- 50
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 10 · 2019: 9 · 2018: 11 · 2017: 8 · 2016: 14 · 2015: 12 · 2014: 16 · 2013: 7 · 2012: 18
- FWCI
- 5.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- age-related decline, sex hormones, testosterone, estradiol, estrone, sex hormone-binding globulin, insulin-like growth factor I, healthy men, aging, body mass index, frailty, healthy aging, gonadal axis, somatotropic axis, blood donors, sports club members, bone mineral density, muscle mass
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Cross-Sectional Studies, Estradiol, Humans, Insulin-Like Growth Factor I, Male, Middle Aged, Serum Albumin, Sex Hormone-Binding Globulin, Gonadal Steroid Hormones, Testosterone, Body Mass Index, Multivariate Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review