Influence of some biological indexes on sex hormone-binding globulin and androgen levels in aging or obese males
Abstract
Several aspects of the regulation of androgen secretion and plasma levels in males remain controversial. Among these, we cite the problem of whether the age-related decrease in testosterone (T) levels is an intrinsic aging phenomenon or is a sequel of previous illness, the mechanisms underlying the increase in sex hormone-binding globulin (SHBG)-binding capacity in aging men and the supranormal capacity observed immediately after a weight-reducing diet, and the role of insulin in the age-associated decrease in dehydroepiandrosterone (sulfate) [DHEA (DHEAS)] levels. To gain further insight into these issues, we investigated the influence of age, smoking, body mass index (BMI), serum albumin, insulin, GH, and insulin-like growth factor I (IGF-I) levels, respectively, on androgen levels and SHBG-binding capacity in a nonobese healthy population (n = 250) as well as in an obese population (n = 50) before and after weight loss. The influence of GH supplementation on SHBG, DHEAS, DHEA, and insulin levels was studied in a small group of men (n = 8) with isolated GH deficiency. In nonobese healthy men, age was inversely correlated with serum levels of all androgens studied (although total T levels stayed relatively stable until age 55 yr) as well as with albumin, GH, and IGF-I levels and positively correlated with BMI, insulin levels, and SHBG-binding capacity. Nevertheless, SHBG levels were significantly negatively correlated with insulin levels (P < 0.001) as well as with mean 24-h GH and IGF-I levels. Among possible confounding factors affecting (free) T [(FT)] levels in healthy men, smoking appeared to be accompanied by higher (F)T levels than those in nonsmokers. BMI increased with age, but although BMI was negatively correlated with T, FT, and SHBG, respectively, the age-dependent decrease in T levels persisted after correction for BMI. Data not corrected for BMI may, nevertheless, overestimate the age-associated decrease in T levels. The albumin concentration decreased with age, and if FT is the feedback regulator of plasma T levels, albumin concentration might be a codeterminant (although, evidently, less important than SHBG) of T levels and contribute to the age-associated decrease in T levels. In any case, albumin concentration is a codeterminant of DHEAS concentration. T, DHEA, and DHEAS levels were significantly correlated, but this correlation disappeared after controlling for age; hence, there is no evidence for an adrenal-gonadal interaction in men. In obese men, T, FT, and SHBG levels were significantly lower than those in the nonobese men and inversely correlated with BMI; DHEAS levels were slightly lower than those in the nonobese controls, but no significant correlation between DHEA or DHEAS, and insulin levels was observed. After a weight-reducing, protein-rich diet, resulting in a mean weight loss of +/- 15 kg, SHBG-binding capacity increased to normal values notwithstanding the fact that the subjects were still obese and that the insulin levels remained higher than those in the nonobese controls. Considering that after weight loss, GH and IGF-I levels remained lower than those in the nonobese controls, that adult men with isolated GH deficiency presented with higher SHBG levels than normal controls, which decreased to normal levels during GH substitution, and that elderly men have elevated SHBG levels notwithstanding high insulin levels, we suggest that the low GH and/or IGF-I levels might play a role in the elevated SHBG levels observed in both elderly males and obese men after a weight-reducing diet. As weight loss did not influence DHEAS levels notwithstanding an important decrease in insulin levels, our data do not support a role of insulin in the regulation of plasma DHEAS levels.
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?
Peripheral androgen aromatization is enhanced in subjects with increased body mass index.
“Peripheral androgen aromatization is enhanced in subjects with increased body mass index [40].”
From Aromatase inhibitors in men: effects and therapeutic options (2011) · cites this paper as [40]
Several additional causes can have a key role in bringing about functional hypogonadism.
“Moreover, several additional causes can have a key role in bringing about this clinical condition (27).”
From Effects of liraglutide on obesity-associated functional hypogonadism in men (2019) · cites this paper as [27]
Cites
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
Testosterone Secretion and Metabolism in Male Senescence
Vermeulen, A., Rubens, R. D., & Verdonck, L. (1972) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-34-4-730 · Cited by 536 · see citing works
Self-citationThe Apparent Free Testosterone Concentration, An Index of Androgenicity
Vermeulen, A., Stoica, T., & Verdonck, L. (1971) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-33-5-759 · Cited by 388 · see citing works
Self-citationThe Influence of Age, Alcohol Consumption, and Body Build on Gonadal Function in Men*
Sparrow, D., Bossé, R., & Rowe, J. W. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-3-508 · Cited by 171 · see citing works
Nyctohemeral Growth Hormone Profiles in Young and Aged Men: Correlation with Somatomedin-C Levels*
Vermeulen, A. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-64-5-884 · Cited by 170 · see citing works
Self-citationCIGARETTE SMOKING AND SERUM SEX HORMONES IN MEN
Dai, W. S., Gutai, J. P., Kuller, L. H., & Cauley, J. A. (1988) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a115033 · Cited by 166 · see citing works
Leenen, R. C. A., Kooy, K. V. D., Seidell, J. C., Deurenberg, P., & Koppeschaar, H. P. F. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.6.8200956 · Cited by 155 · see citing works
The relationship of sex hormones to hyperinsulinemia and hyperglycemia
Haffner, S. M., Katz, M. S., Stern, M. P., & Dunn, J. F. (1988) · Metabolism · doi:10.1016/0026-0495(88)90091-1 · Cited by 140 · see citing works
Adrenocortical function in old age: response to acute adrenocorticotropin stimulation.
VERMEULEN, A., DESLYPERE, J. P., SCHELFHOUT, W., VERDONCK, L., & RUBENS, R. (1982) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-54-1-187 · Cited by 135 · see citing works
Self-citationRelationship between serum sex hormones and the glucose-insulin-lipid defect in men with obesity
Phillips, G. B. (1993) · Metabolism · doi:10.1016/0026-0495(93)90181-m · Cited by 116 · see citing works
O'Neal, D., Kalfas, A., Dunning, P., Christopher, M., SAWYER, S., Ward, G. M., & ALFORD, F. P. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.4.7962308 · Cited by 113 · see citing works
Regulation of sex hormone-binding globulin production by growth factors
Plymate, S. R., Hoop, R. C., Jones, R. E., & Matej, L. A. (1990) · Metabolism · doi:10.1016/0026-0495(90)90309-z · Cited by 92 · see citing works
Androgens, Estrogens, and Sex Hormone-Binding Globulin in Middle-Aged Men*
Longcope, C., GOLDFIELD, S. R. W., Brambilla, D. J., & McKinlay, J. B. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-6-1442 · Cited by 84 · see citing works
MOOR, P. D., & Jv, J. (1970) · PubMed · Cited by 75 · see citing works
Diamond, M. P., GRAINGER, D. A., LAUDANO, A. J., Starick-Zych, K., & DeFronzo, R. A. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-72-4-883 · Cited by 74 · see citing works
Decreased adrenal androgen sensitivity to ACTH during aging
Parker, L., Grál, T., Perrigo, V., & Skowsky, R. (1981) · Metabolism · doi:10.1016/0026-0495(81)90139-6 · Cited by 71 · see citing works
Strain, G., Zumoff, B., Rosner, W., & Pi-Sunyer, X. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.4.7962291 · Cited by 69 · see citing works
Peripheral hormone levels in healthy subjects during controlled fasting
Tegelman, R., Lindeskog, P., Carlström, K., Pousette, Å., & Blomstrand, R. (1986) · European Journal of Endocrinology · doi:10.1530/acta.0.1130457 · Cited by 45 · see citing works
Comparison of quick methods for the estimation of estradiol in plasma by radioimmunoassay
Verdonck, L., & Vermeulen, A. (1974) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(74)90046-6 · Cited by 36 · see citing works
Self-citationBinding of Dehydroepiandrosterone Sulfate to Serum Albumin
Puche, R. C., & Nes, W. R. (1962) · Endocrinology · doi:10.1210/endo-70-6-857 · Cited by 33 · see citing works
Adrenal and Testicular Androgen Levels Are Correlated
Parker, L., & Lifrak, E. T. (1981) · Hormone and Metabolic Research · doi:10.1055/s-2007-1019366 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ding, E. L., Song, Y., Malik, V. S., & Liu, S. (2006) · JAMA · doi:10.1001/jama.295.11.1288 · Cited by 1,354 · see citing works
Wu, 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
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
Self-citationBody mass index in relation to semen quality and reproductive hormonesamong 1,558 Danish men
Jensen, T. K., Andersson, A., Jørgensen, N., Andersen, A., Carlsen, E., Petersen, J. H., & Skakkebæk, N. E. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.03.056 · Cited by 818 · see citing works
Energy balance and cancer: the role of insulin and insulin-like growth factor-I
Kaaks, R., & Lukanova, A. (2001) · Proceedings of The Nutrition Society · doi:10.1079/pns200070 · Cited by 610 · see citing works
Acne vulgaris: a disease of Western civilization
Cordain, L., Lindeberg, S., Hurtado, M., Hill, K., Eaton, S. B., & Brand-Miller, J. (2002) · Archives of Dermatology · doi:10.1001/archderm.138.12.1584 · Cited by 500 · 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
Mechanisms of the Age-Associated Deterioration in Glucose Tolerance
Basu, R., Breda, E., Oberg, A. L., Powell, C. C., Dalla Man, C., Basu, A., Vittone, J. L., Klee, G. G., Arora, P., Jensen, M. D., et al. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1738 · Cited by 440 · see citing works
Travison, T. G., Araujo, A. B., Kupelian, V., O’Donnell, A. B., & McKinlay, J. B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1859 · Cited by 410 · see citing works
Hypogonadism in men consuming sustained-action oral opioids
Daniell, H. W. (2002) · The Journal of Pain · doi:10.1054/jpai.2002.126790 · Cited by 401 · 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
The benefits and risks of testosterone replacement therapy: a review
Morley, J. E. (2009) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s3025 · Cited by 375 · see citing works
Laughlin, G. A., Barrett-Connor, E. L., Kritz‐Silverstein, D. C., & von Mühlen, D. G. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6405 · Cited by 381 · 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
Pope, H. G., Cohane, G. H., Kanayama, G., Siegel, A. J., & Hudson, J. I. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.1.105 · Cited by 341 · see citing works
A Population-Level Decline in Serum Testosterone Levels in American Men
Travison, T. G., de Araújo, A. B., O’Donnell, A. B., Kupelian, V. A., & McKinlay, J. B. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1375 · Cited by 335 · see citing works
The Metabolic Syndrome and Male Infertility
Kasturi, S. S., Tannir, J. R., & Brannigan, R. E. (2008) · Journal of Andrology · doi:10.2164/jandrol.107.003731 · Cited by 306 · see citing works
Association of Bioavailable, Free, and Total Testosterone With Insulin Resistance
Tsai, E. C., Matsumoto, A. M., Fujimoto, W. Y., & Boyko, E. J. (2004) · Diabetes Care · doi:10.2337/diacare.27.4.861 · Cited by 307 · see citing works
Frailty and sarcopenia: definitions and outcome parameters
Cooper, C. C., Dere, W. H., Evans, W. J., Kanis, J. A., Rizzoli, R., Sayer, A. A., Sieber, C. C., Kaufman, J., van Kan, G. A., Boonen, S., et al. (2012) · Osteoporosis International · doi:10.1007/s00198-012-1913-1 · Cited by 302 · see citing works
Lowered testosterone in male obesity: Mechanisms, morbidity and management
Grossmann, M., Tang Fui, M., & Dupuis, P. (2014) · Asian Journal of Andrology · doi:10.4103/1008-682x.122365 · Cited by 293 · see citing works
Brain levels of sex steroid hormones in men and women during normal aging and in Alzheimer's disease
Rosario, E. R., Chang, L., Head, E. H., Stanczyk, F. Z., & Pike, C. J. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.008 · Cited by 289 · see citing works
Population variation in age-related decline in male salivary testosterone.
Ellison, P. T. (2002) · Human Reproduction · doi:10.1093/humrep/17.12.3251 · Cited by 263 · 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
Testosterone Substitution Normalizes Elevated Serum Leptin Levels in Hypogonadal Men
Jockenhövel, F., Blum, W. F., Vogel, E., Englaro, P., Müller-Wieland, D., Reinwein, D., Rascher, W., & Krone, W. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.8.4174 · Cited by 261 · see citing works
Mohr, B. A., Guay, A. T., O’Donnell, A. B., & McKinlay, J. B. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02174.x · Cited by 248 · see citing works
Zitzmann, M., & Nieschlag, E. (2001) · European Journal of Endocrinology · doi:10.1530/eje.0.1440183 · Cited by 248 · see citing works
Health, A. A. B. C. S., Visser, M., Kritchevsky, S. B., Newman, A. B., Goodpaster, B. H., Tylavsky, F. A., Nevitt, M. C., & Harris, T. B. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn.82.3.531 · Cited by 246 · see citing works
Kolonel, L. N. (1996) · Cancer Causes & Control · doi:10.1007/bf00115640 · Cited by 244 · 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
Physiopathological Mechanism of Sarcopenia
Walrand, S., Guillet, C., Salles, J., Cano, N., & Boirie, Y. (2011) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2011.03.005 · Cited by 235 · see citing works
Laaksonen, D. E., Niskanen, L., Punnonen, K., Nyyssönen, K., Tuomainen, T.-P., Valkonen, V.-P., & Salonen, J. T. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0970 · Cited by 230 · see citing works
Androgen Replacement Therapy in the Aging Male--A Critical Evaluation
Vermeulen, A. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7630 · Cited by 226 · see citing works
Self-citationHyperinsulinemic diseases of civilization: more than just Syndrome X
Cordain, L., Eades, M. R., & Eades, M. D. (2003) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(03)00011-4 · Cited by 209 · see citing works
Anthropometry in Relation to Prostate Cancer Risk in the Netherlands Cohort Study
Schuurman, A. G., Goldbohm, R. A., Dorant, E., & van den Brandt, P. A. (2000) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a010241 · Cited by 208 · see citing works
Insulin-Like Growth Factor-I and Cognitive Function in Healthy Older Men
Aleman, A., Verhaar, H. J. J., de Haan, E. H. F., de Vries, W. R., Samson, M., Drent, M. L., van der Veen, E. A., & Koppeschaar, H. P. F. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5455 · Cited by 208 · see citing works
Bjørnerem, Å., Straume, B., Midtby, M., Fønnebø, V., Sundsfjord, J., Svartberg, J., Acharya, G., Øian, P., & Berntsen, G. K. R. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0735 · Cited by 199 · see citing works
Kahn, B. E., & Brannigan, R. E. (2017) · Current Opinion in Urology · doi:10.1097/mou.0000000000000417 · Cited by 198 · see citing works
Gray, P. B., Jeffrey Yang, C.-F., & Pope, H. G. (2006) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2005.3311 · Cited by 192 · see citing works
Mazer, N. A. (2009) · Steroids · doi:10.1016/j.steroids.2009.01.008 · Cited by 189 · see citing works
Dehydroepiandrosterone, obesity and cardiovascular disease risk: a review of human studies
Tchernof, A., & Labrie, F. (2004) · European Journal of Endocrinology · doi:10.1530/eje.0.1510001 · Cited by 183 · 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
Self-citationEnergy balance and cancer: the role of sex hormones
Key, T. J., Allen, N. E., Verkasalo, P. K., & Banks, E. (2001) · Proceedings of The Nutrition Society · doi:10.1079/pns200068 · Cited by 180 · see citing works
Functional relationship between obesity and male reproduction: from humans to animal models
Teerds, K. J., de Rooij, D. G., & Keijer, J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr017 · Cited by 183 · see citing works
Obesity and testicular function
Mah, P., & Wittert, G. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.06.007 · Cited by 179 · see citing works
Zitzmann, M., Gromoll, J., von Eckardstein, A., & Nieschlag, E. (2003) · Diabetologia · doi:10.1007/s00125-002-0980-9 · Cited by 173 · see citing works
Antonio, L., Wu, F. C. W., O'Neill, T. W., Pye, S. R., Ahern, T. B., Laurent, M. R., Huhtaniemi, I. T., Lean, M. E. J., Keevil, B. G., Rastrelli, G., et al. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-4106 · Cited by 174 · see citing works
Bobjer, J., Katrinaki, M., Tsatsanis, C., Giwercman, Y. L., & Giwercman, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061466 · Cited by 173 · see citing works
Testosterone and Depression in Aging Men
Seidman, S. N., & Walsh, B. T. (1999) · American Journal of Geriatric Psychiatry · doi:10.1097/00019442-199902000-00004 · Cited by 162 · 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
Khoo, J. J. C., Piantadosi, C., Duncan, R. F., Worthley, S. G., Jenkins, A. J., Noakes, M., Worthley, M. I., Lange, K. M., & Wittert, G. (2011) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2011.02417.x · Cited by 157 · see citing works
Aromatase inhibitors in men: effects and therapeutic options
de Ronde, W., & de Jong, F. H. (2011) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-9-93 · Cited by 155 · see citing works
Smoking Is Associated with Lower Bone Mineral Density and Reduced Cortical Thickness in Young Men
Lorentzon, M., Mellström, D., Haug, E., & Ohlsson, C. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1294 · Cited by 154 · see citing works
Reis, L. O., Fávaro, W. J., Barreiro, G. C., de Oliveira, L. C., Chaim, É. A., Fregonesi, A., & Ferreira, U. (2009) · International Journal of Andrology · doi:10.1111/j.1365-2605.2009.01017.x · Cited by 151 · see citing works
Winters, S. J., Brufsky, A., Weissfeld, J. L., Trump, D. L., Dyky, M. A., & Hadeed, V. (2001) · Metabolism · doi:10.1053/meta.2001.26714 · Cited by 152 · see citing works
Nielsen, T. L., Hagen, C., Wraae, K., Brixen, K., Petersen, P. H., Haug, E., Larsen, R., & Andersen, M. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1847 · Cited by 149 · see citing works
Vermeulen, A. (2000) · Maturitas · doi:10.1016/s0378-5122(99)00075-4 · Cited by 147 · see citing works
Self-citationIncreased Bone Resorption in Moderate Smokers with Low Body Weight: The Minos Study
Szulc, P. (2002) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.87.2.666 · Cited by 144 · see citing works
Aging and the Male Reproductive System.
Kaufman, J., Lapauw, B., Mahmoud, A., T'sjoen, G., & Huhtaniemi, I. (2019) · Endocrine reviews · doi:10.1210/er.2018-00178 · Cited by 97 · see citing works
Aging and sex hormones in males
Decaroli, M. C., & Rochira, V. (2016) · Virulence · doi:10.1080/21505594.2016.1259053 · Cited by 141 · see citing works
Ukkola, O., Gagnon, J., Rankinen, T., Thompson, P., Hong, Y., Leon, A., Rao, D., Skinner, J., Wilmore, J., & Bouchard, C. (2001) · European Journal of Endocrinology · doi:10.1530/eje.0.1450001 · Cited by 138 · see citing works
Implications for the Role of Diet in Acne
Cordain, L. (2005) · Seminars in Cutaneous Medicine and Surgery · doi:10.1016/j.sder.2005.04.002 · Cited by 140 · see citing works
Open-label pilot study of testosterone patch therapy in men with opioid-induced androgen deficiency
Daniell, H. W., Lentz, R., & Mazer, N. A. (2006) · The Journal of Pain · doi:10.1016/j.jpain.2005.10.009 · Cited by 135 · see citing works
Rohrmann, S. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh060 · Cited by 135 · see citing works
Raven, G., de Jong, F. H., Kaufman, J.-M., & de Ronde, W. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0462 · Cited by 134 · see citing works
Self-citationSaad, F., Gooren, L. J., Haider, A., & Yassin, A. (2008) · Journal of Andrology · doi:10.2164/jandrol.107.002774 · Cited by 132 · see citing works
Diet and Sex Hormone-Binding Globulin
Longcope, C., Feldman, H. A., McKinlay, J. B., & de Araújo, A. B. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.1.6291 · Cited by 133 · see citing works
Lima, N., Cavaliere, H., Knobel, M., Halpern, A., & Medeiros-Neto, G. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801406 · Cited by 130 · see citing works
Calculation of Bioavailable and Free Testosterone in Men: A Comparison of 5 Published Algorithms
de Ronde, W., van der Schouw, Y. T., Pols, H. A., Gooren, L. J., Muller, M., Grobbee, D. E., & de Jong, F. H. (2006) · Clinical Chemistry · doi:10.1373/clinchem.2005.063354 · Cited by 131 · see citing works
Crabbe, P., Bogaert, V., Bacquer, D. D., Goemaere, S., Zmierczak, H., & Kaufman, J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0117 · Cited by 129 · 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
Hougaku, H., Fleg, J. L., Najjar, S. S., Lakatta, E. G., Harman, S. M., Blackman, M. R., & Metter, E. J. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00059.2005 · Cited by 123 · 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
Hao, Z., Li, Y., Li, H., Wei, B., Liao, X., Liang, T., & Yu, J. (2015) · Chemosphere · doi:10.1016/j.chemosphere.2015.01.057 · Cited by 123 · see citing works
The health of normally aging men: The Massachusetts Male Aging Study (1987–2004)
O’Donnell, A. B., de Araújo, A. B., & McKinlay, J. B. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2004.03.023 · Cited by 122 · see citing works
Effects of a low-energy diet on sexual function and lower urinary tract symptoms in obese men
Khoo, J. J. C., Piantadosi, C., Worthley, S. G., & Wittert, G. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.76 · Cited by 121 · see citing works
Mucci, L. A., Tamimi, R. M., Λάγιου, Π., Trichopoulou, A., Benetou, V., Spanos, E., & Trichopoulos, D. (2001) · British Journal of Urology · doi:10.1046/j.1464-410x.2001.02191.x · Cited by 121 · see citing works
The analog free testosterone assay: are the results in men clinically useful?
Winters, S. J., Kelley, D. E., & Goodpaster, B. (1998) · Clinical Chemistry · doi:10.1093/clinchem/44.10.2178 · Cited by 160 · see citing works
Gooren, L. J., & Bunck, M. C. M. (2004) · Drugs · doi:10.2165/00003495-200464170-00002 · Cited by 118 · 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
Testosterone and ill-health in aging men
Yeap, B. B. (2009) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet1050 · Cited by 112 · see citing works
Sex hormones and skeletal muscle weakness
Sipilä, S., Narici, M., Kjaer, M., Pöllänen, E., Atkinson, R. A., Hansen, M., & Kovanen, V. (2013) · Biogerontology · doi:10.1007/s10522-013-9425-8 · Cited by 106 · see citing works
Testosterone deficiency in the aging male
McBride, J. A., Carson, C. C., & Coward, R. M. (2015) · Therapeutic Advances in Urology · doi:10.1177/1756287215612961 · Cited by 105 · see citing works
Body fatness and sex steroid hormone concentrations in US men: results from NHANES III
Rohrmann, S., Shiels, M. S., López, D. S., Rifai, N., Nelson, W. G., Kanarek, N., Güallar, E., Menke, A., Joshu, C. E., Feinleib, M., et al. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9790-z · Cited by 105 · 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
The ageing male reproductive tract
Sampson, N., Untergasser, G., Plas, E., & Berger, P. (2007) · The Journal of Pathology · doi:10.1002/path.2077 · Cited by 100 · see citing works
Effects of liraglutide on obesity-associated functional hypogonadism in men
Jensterle, M., Podbregar, A., Goricar, K., Gregoric, N., & Janez, A. (2019) · Endocrine Connections · doi:10.1530/ec-18-0514 · Cited by 101 · see citing works
Langlois, J. A., Visser, M., Davidovic, L. S., Maggi, S., Li, G., & Harris, T. B. (1998) · Archives of Internal Medicine · doi:10.1001/archinte.158.9.990 · Cited by 101 · see citing works
Zhao, J., Leung, J. Y. Y., Lin, S. L., & Mary Schooling, C. (2016) · Preventive Medicine · doi:10.1016/j.ypmed.2015.12.021 · Cited by 101 · see citing works
Evidence for geographical and racial variation in serum sex steroid levels in older men
Orwoll, E. S., Nielson, C. M., Labrie, F., Barrett-Connor, E., Cauley, J. A., Cummings, S. R., Ensrud, K., Karlsson, M., Lau, E., Leung, P. C., et al. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2435 · Cited by 100 · see citing works
Sexual Dysfunction Is Common in the Morbidly Obese Male and Improves after Gastric Bypass Surgery
Dallal, R. M., Chernoff, A., O’Leary, M. P., Smith, J. A., Braverman, J. D., & Quebbemann, B. B. (2008) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2008.08.006 · Cited by 100 · see citing works
Androgen regulation of β-amyloid protein and the risk of Alzheimer's disease
Rosario, E. R., & Pike, C. J. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.04.012 · Cited by 100 · see citing works
de Ronde, W., van der Schouw, Y. T., Muller, M., Grobbee, D. E., Gooren, L. J., Pols, H. A. P., & de Jong, F. H. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0422 · Cited by 97 · see citing works
Bioavailable testosterone in men with rheumatoid arthritis--high frequency of hypogonadism
Tengstrand, B. (2002) · British journal of rheumatology · doi:10.1093/rheumatology/41.3.285 · Cited by 97 · see citing works
T'Sjoen, G. G., Goemaere, S., Meyere, M. D., & Kaufman, J. M. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00023-4 · Cited by 95 · see citing works
Low androgenization index in elderly women and elderly men with Alzheimer’s disease
Paoletti, A. M., Congia, S., Lello, S., Tedde, D., Orrù, M., Pistis, M., Pilloni, M., Zedda, P., Loddo, A., & Melis, G. B. (2004) · Neurology · doi:10.1212/01.wnl.0000094199.60829.f5 · Cited by 96 · see citing works
Lee, I.-M. M., Sesso, H. D., & Paffenbarger, R. S. (2001) · Cancer Causes & Control · doi:10.1023/a:1008952528771 · Cited by 94 · see citing works
Kaufman, J., & Vermeulen, A. (1998) · Springer eBooks · doi:10.1007/978-3-642-72185-4_16 · Cited by 92 · see citing works
Self-citationRIPK1-RIPK3-MLKL-dependent necrosis promotes the aging of mouse male reproductive system
Li, D., Meng, L., Xu, T., Su, Y., Liu, X., Zhang, Z., & Wang, X. (2017) · eLife · doi:10.7554/elife.27692 · Cited by 94 · see citing works
Laughlin, G. A., Barrett-Connor, E. L., Kritz‐Silverstein, D. C., & von Mühlen, D. G. (2000) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-200007000-00020 · Cited by 94 · see citing works
Bauer, J. M., Cruz-Jentoft, A. J., Fielding, R. A., Kanis, J. A., Reginster, J.-Y., Bruyère, O., Cesari, M., Chapurlat, R., Al-Daghri, N., Dennison, E., et al. (2019) · Calcified Tissue International · doi:10.1007/s00223-019-00561-w · Cited by 83 · see citing works
Self-citation
- Authors
- Vermeulen, A.
- Affiliations
- Ghent University Hospital (BE)
- ORCID
- Vermeulen, A.
- Venue
- Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1996-05-01
- Volume
- 81
- Issue
- 5
- Pages
- 1821-1826
- ISSN
- 0021-972X (ISSN-L)
- OpenAlex
- W1985489419
- Cited by
- 455
- References
- 21
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 7 · 2023: 3 · 2022: 12 · 2021: 7 · 2020: 11 · 2019: 8 · 2018: 6 · 2017: 12 · 2016: 6 · 2015: 14 · 2014: 12 · 2013: 19 · 2012: 23
- FWCI
- 7.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- 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
- sex hormone-binding globulin, androgens, older men, obesity, testosterone, free testosterone, dehydroepiandrosterone sulfate, insulin, insulin-like growth factor I, growth hormone, body mass index, smoking, serum albumin, weight loss, weight loss diet, GH deficiency, androgen regulation, healthy men, healthy women, menopausal women
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Androgens, Dehydroepiandrosterone, Humans, Insulin, Insulin-Like Growth Factor I, Male, Middle Aged, Obesity, Serum Albumin, Sex Hormone-Binding Globulin, Smoking, Growth Hormone, Testosterone, Body Mass Index, Dehydroepiandrosterone Sulfate
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