Characteristics of Secondary, Primary, and Compensated Hypogonadism in Aging Men: Evidence from the European Male Ageing Study
Abstract
CONTEXT: The diagnosis of late-onset hypogonadism (LOH) in older men with age-related declines in testosterone (T) is currently not well characterized. OBJECTIVE: Our objective was to investigate whether different forms of hypogonadism can be distinguished among aging men. DESIGN: The study was a cross-sectional survey on 3369 community-dwelling men aged 40-79 yr in eight European centers. METHODS: Four groups of subjects were defined: eugonadal (normal T and normal LH), secondary (low T and low/normal LH), primary (low T and elevated LH), and compensated (normal T and elevated LH) hypogonadism. Relationships between the defined gonadal status with potential risk factors and clinical symptoms were investigated by multilevel regression models. RESULTS: Among the men, 11.8, 2.0, and 9.5% were classified into the secondary, primary, and compensated hypogonadism categories, respectively. Older men were more likely to have primary [relative risk ratio (RRR) = 3.04; P < 0.001] and compensated (RRR = 2.41; P < 0.001) hypogonadism. Body mass index of 30 kg/m(2) or higher was associated with secondary hypogonadism (RRR = 8.74; P < 0.001). Comorbidity was associated with both secondary and primary hypogonadism. Sexual symptoms were more prevalent in secondary and primary hypogonadism, whereas physical symptoms were more likely in compensated hypogonadism. CONCLUSIONS: Symptomatic elderly men considered to have LOH can be differentiated on the basis of endocrine and clinical features and predisposing risk factors. Secondary hypogonadism is associated with obesity and primary hypogonadism predominately with age. Compensated hypogonadism can be considered a distinct clinical state associated with aging. Classification of LOH into different categories by combining LH with T may improve the diagnosis and management of LOH.
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Obesity is associated with a multitude of adverse health outcomes including cardiovascular disease, sleep apnea, osteoarthritis, increased risk of certain cancers, and in men, lowered testosterone levels.
“In addition to posing significant societal and environmental challenges, obesity is associated with a multitude of adverse health outcomes including cardiovascular disease, sleep apnea, osteoarthritis, increased risk of certain cancers, and in men, lowered testosterone levels.3”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [3]
In the EMAS cohort of 3219 men, obesity was associated with an 8.7-fold and overweight with a 3.3-fold increased relative risk of secondary hypogonadism (defined as total testosterone <10.5 nmol/L and normal luteinizing hormone), relative to normal weight.
“In a cohort of 3219 men from the European Male Aging Study (EMAS), obesity was associated with an 8.7-fold and overweight with a 3.3-fold increased relative risk (RR) of secondary hypogonadism (defined as total testosterone of <10.5 nmol l−1 and normal luteinizing hormone (LH)), relative to normal weight3.”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [3]
Obesity blunts the age-associated rise in LH, so obesity leads to hypothalamic-pituitary suppression irrespective of age which cannot be compensated for by physiological mechanisms.
“However, because obesity blunts this LH rise, obesity leads to hypothalamic-pituitary suppression irrespective of age which cannot be compensated for by physiological mechanisms.3”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [3]
Serum testosterone levels decline with age, commencing in men in their mid-30s and decreasing at an average annual rate of 1.6%.
“We speculate that this phenomenon may be attributed to the gradual decline in serum testosterone levels with age, commencing in men in their mid-30s and decreasing at an average annual rate of 1.6%38–43.”
From Association between serum cotinine and total testosterone in adult males based on NHANES 2011–2016 (2024) · cites this paper as [38]
Age, BMI, fasting blood glucose, triglycerides, alcohol consumption and estradiol levels have all been reported to be associated with alteration in hormone levels.
“Age, 11,14-17 body mass index (BMI), 12 fasting blood glucose, 1,35 triglycerides, 36 alcohol consumption 13,14 and estradiol levels, 13 which have all been reported to be associated with alteration in hormone levels, were chosen as potential confounding factors in this study.”
From Cigarette smoking has a positive and independent effect on testosterone levels (2013) · cites this paper as [11]
Age, cigarette smoking, BMI, alcohol consumption and physical activity have been reported to be probably or possibly associated with hormone levels.
“Probable and possible associations of several factors, including age, cigarette smoking, body mass index (BMI), alcohol consumption and physical activity with hormone levels have been reported. 11-17”
From Cigarette smoking has a positive and independent effect on testosterone levels (2013) · cites this paper as [11]
Obesity is the single most important factor associated with low testosterone, overriding the effects of age and comorbidities.
“These studies have confirmed that obesity is the single most important factor associated with low testosterone, overriding the effects of age and comorbidities.28,29”
From Hypogonadism and male obesity: Focus on unresolved questions (2018) · cites this paper as [29]
In such men, hypogonadism is caused by functional HPT axis suppression in the presence of an intact HPT axis.
“hypogonadism is caused by functional HPT axis suppression in the presence of an intact HPT axis”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
In most middle-aged and older men with functional hypogonadism, gonadotropin levels are not elevated.
“In most such men, gonadotropin levels are not elevated (6)”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
Many middle-aged and older men (aged 50 years or older), especially when obese and suffering from comorbid illness, present with clinical features resembling organic androgen deficiency and modestly to occasionally severely low testosterone levels, yet they do not have recognizable intrinsic structural HPT pathology.
“many middle-aged and older men (defined here as aged 50 years or older), especially when obese and suffering from comorbid illness, present with clinical features resembling organic androgen deficiency and modestly to occasionally severely low testosterone levels, yet they do not have recognizable intrinsic structural HPT pathology.”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
In EMAS, compared with lean weight, overweight (BMI, 25 to 30 kg/m2) was associated with a 2.3 nmol/L reduction and obesity with a 5.1 nmol/L reduction in total testosterone and, respectively, a 17.6 pmol/L and 53.7 pmol/L reduction in free testosterone.
“In EMAS, compared with lean weight, overweight (BMI, 25 to 30 kg/m2) was associated with a 2.3 nmol/L (66 ng/dL) reduction and obesity with a 5.1 nmol/L (147 ng/dL) reduction in total testosterone and, respectively, a 17.6 pmol/L (5.1 pg/mL) and 53.7 pmol/L (15.5 pg/mL) reduction in free testosterone (6).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
Obesity is the strongest risk factor associated with low testosterone levels in middle-aged and older men.
“Obesity is the strongest risk factor associated with low testosterone levels middle-aged and older men (6).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
Typically, luteinizing hormone levels are not elevated in middle-aged and older men with low testosterone.
“Typically, luteinizing hormone (LH) levels are not elevated (6).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [6]
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
Introducing Multilevel Modeling
Kreft, I., & de Leeuw, J. (1998) · doi:10.4135/9781849209366 · Cited by 2,997 · see citing works
The Clinical Significance of Subclinical Thyroid Dysfunction
Biondi, B., & Cooper, D. S. (2008) · Endocrine Reviews · doi:10.1210/er.2006-0043 · Cited by 1,418 · 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 1,115 · 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
Self-citationInvestigation, treatment and monitoring of late-onset hypogonadism in males
Wang, C., Nieschlag, E., Swerdloff, R., Behre, H. M., Hellstrom, W. J., Gooren, L. J., Kaufman, J. M., Legros, J.-J., Lunenfeld, B., Morales, A., et al. (2008) · European Journal of Endocrinology · doi:10.1530/eje-08-0601 · Cited by 867 · see citing works
Self-citationPrevalence of Symptomatic Androgen Deficiency in Men
Araujo, A. B., Esche, G. R., Kupelian, V., O’Donnell, A. B., Travison, T. G., Williams, R. E., Clark, R. V., & McKinlay, J. B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1245 · Cited by 720 · see citing works
Association of Specific Symptoms and Metabolic Risks with Serum Testosterone in Older Men
Zitzmann, M., Faber, S., & Nieschlag, E. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0401 · Cited by 552 · see citing works
Bhasin, S., Woodhouse, L., Casaburi, R., Singh, A. B., Mac, R. P., Lee, M., Yarasheski, K. E., Sinha-Hikim, I., Dzekov, C., Dzekov, J., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1184 · Cited by 544 · see citing works
Adipocytokines and Insulin Resistance
Pittas, A. G., Joseph, N. A., & Greenberg, A. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031005 · Cited by 515 · see citing works
Leydig cell numbers, daily sperm production, and serum gonadotropin levels in aging men
NEAVES, W. B., JOHNSON, L., PORTER, J. C., PARKER, C. R., & PETTY, C. S. (1984) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-59-4-756 · Cited by 495 · see citing works
Huber, G., Staub, J.-J., Meier, C., Mitrache, C., Guglielmetti, M., Huber, P., & Braverman, L. E. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.7.8678 · Cited by 418 · 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
Insulin Signaling in the Central Nervous System
Porte, D., Baskin, D. G., & Schwartz, M. W. (2005) · Diabetes · doi:10.2337/diabetes.54.5.1264 · Cited by 336 · 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
Sexual dysfunction in men and women with endocrine disorders
Bhasin, S., Enzlin, P., Coviello, A. D., & Basson, R. J. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60280-3 · Cited by 317 · see citing works
Androgen glucuronides, instead of testosterone, as the new markers of androgenic activity in women
Labrie, F., Bélanger, A., Bélanger, P., Bérubé, R., Martel, C., Cusan, L., Gomez, J., Candas, B., Castiel, I., Chaussade, V., et al. (2006) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2006.02.004 · Cited by 296 · see citing works
Self-citationNIESCHLAG, E., SWERDLOFF, R., BEHRE, H. M., GOOREN, L. J., KAUFMAN, J. M., LEGROS, J. ‐., LUNENFELD, B., MORLEY, J. E., SCHULMAN, C., WANG, C., et al. (2005) · International Journal of Andrology · doi:10.1111/j.1365-2605.2005.00553.x · Cited by 282 · see citing works
Self-citationNiskanen, L., Laaksonen, D. E., Punnonen, K., Mustajoki, P., Kaukua, J., & Rissanen, A. (2004) · Diabetes, Obesity and Metabolism · doi:10.1111/j.1462-8902.2004.00335.x · Cited by 275 · see citing works
Institute of Medicine (2004) · National Academies Press eBooks · doi:10.17226/10852 · Cited by 231 · see citing works
Vermeulen, A., & Verdonck, G. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.4.1548361 · Cited by 194 · see citing works
Management of hypothyroidism in adults
Vaidya, B., & Pearce, S. H. S. (2008) · BMJ · doi:10.1136/bmj.a801 · Cited by 178 · see citing works
The Relationship between Libido and Testosterone Levels in Aging Men
Travison, T. G., Morley, J. E., de Araújo, A. B., O’Donnell, A. B., & McKinlay, J. B. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2508 · Cited by 178 · see citing works
Cohen, P. G. (2001) · Medical Hypotheses · doi:10.1054/mehy.2000.1169 · Cited by 172 · see citing works
Aging of the human ovary and testis
Perheentupa, A. H., & Huhtaniemi, I. T. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.11.004 · Cited by 168 · see citing works
Self-citationTestosterone and aging: Clinical research directions
(2003) · PsycEXTRA Dataset · doi:10.1037/e720062007-001 · Cited by 163 · 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
Self-citationNieschlag, E., Swerdloff, R. S., Behre, H. M., Gooren, L. J., Kaufman, J., Legros, J. J., Lunenfeld, B., Morley, J. E., Schulman, C., Wang, C., et al. (2006) · Journal of Andrology · doi:10.2164/jandrol.05047 · Cited by 123 · see citing works
Self-citationHärkönen, K., Huhtaniemi, I. T., Mäkinen, J., Hübler, D., Irjala, K., Koskenvuo, M. J., Oettel, M., Raitakari, O. T., Saad, F., & Pöllänen, P. (2003) · International Journal of Andrology · doi:10.1046/j.1365-2605.2003.00415.x · Cited by 121 · see citing works
Self-citationLetrozole normalizes serum testosterone in severely obese men with hypogonadotropic hypogonadism
De Boer, H., Verschoor, L., Ruinemans‐Koerts, J., & Jansen, M. (2005) · Diabetes, Obesity and Metabolism · doi:10.1111/j.1463-1326.2004.00397.x · Cited by 108 · see citing works
Hypogonadism in Elderly Men — What to Do Until the Evidence Comes
Snyder, P. J. (2004) · New England Journal of Medicine · doi:10.1056/nejmp038207 · Cited by 106 · see citing works
O'Connor, D. B., Corona, G., Forti, G., Tajar, A., Lee, D. M., Finn, J. D., Bártfai, G., Boonen, S., Casanueva, F. F., Giwercman, A., et al. (2008) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2008.00781.x · Cited by 101 · see citing works
Self-citationHormonal cut-offs of partial androgen deficiency: a survey of androgen assays.
Vermeulen, A. (2005) · PubMed · Cited by 72 · see citing works
Luteinizing Hormone and Different Genetic Variants, as Indicators of Frailty in Healthy Elderly Men
van den Beld, A. W., Huhtaniemi, I. T., Pettersson, K. S. I., Pols, H. A. P., Grobbee, D. E., de Jong, F. H., & Lamberts, S. W. J. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.4.5616 · Cited by 59 · see citing works
Self-citationCooper, D. S. (1987) · JAMA · doi:10.1001/jama.1987.03400020088037 · Cited by 40 · see citing works
Liu, P. Y., Pincus, S. M., Takahashi, P. Y., Roebuck, P. D., Iranmanesh, A., Keenan, D. M., & Veldhuis, J. D. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00227.2005 · Cited by 38 · see citing works
Making a diagnosis of androgen deficiency in adult men: what to do until all the facts are in?
Bhasin, S., & Wu, F. C. W. (2006) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0299 · Cited by 17 · see citing works
Self-citationJones, T. H. (2009) · BMJ · doi:10.1136/bmj.b352 · Cited by 9 · see citing works
Svartberg, J. B., & Jorde, R. (2007) · International Journal of Andrology · doi:10.1111/j.1365-2605.2006.00732.x · Cited by 3 · see citing works
Abnormal thyroid stimulating hormone levels: when and who to treat
Weetman, A. P. (2008) · Clinical Medicine · doi:10.7861/clinmedicine.8-2-208 · Cited by 1 · see citing works
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Garvey, W. T., Mechanick, J. I., Brett, E. M., Garber, A. J., Hurley, D. L., Jastreboff, A. M., Nadolsky, K., Pessah-Pollack, R., & Plodkowski, R. (2016) · Endocrine Practice · doi:10.4158/ep161365.gl · Cited by 1,914 · see citing works
Identification of late-onset hypogonadism in middle-aged and elderly men
Wu, F. C. W., Tajar, A., Beynon, J. M., Pye, S. R., Silman, A. J., Finn, J. D., O'Neill, T. W., Bartfai, G., Casanueva, F. F., Forti, G., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0911101 · Cited by 1,544 · see citing works
Self-citationYafi, F. A., Jenkins, L., Albersen, M., Corona, G., Isidori, A. M., Goldfarb, S., Maggi, M., Nelson, C. J., Parish, S., Salonia, A., et al. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.3 · Cited by 853 · see citing works
Corona, G., Goulis, D. G., Huhtaniemi, I., Zitzmann, M., Toppari, J., Forti, G., Vanderschueren, D., & Wu, F. C. (2020) · Andrology · doi:10.1111/andr.12770 · Cited by 431 · see citing works
Self-citationLow Testosterone in Men with Type 2 Diabetes: Significance and Treatment
Grossmann, M. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0118 · Cited by 350 · see citing works
Tajar, A., Huhtaniemi, I. T., O'Neill, T. W., Finn, J. D., Pye, S. R., Lee, D. M., Bartfai, G., Boonen, S., Casanueva, F. F. F., Forti, G., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2513 · Cited by 318 · see citing works
Self-citationUpdate: Hypogonadotropic Hypogonadism in Type 2 Diabetes and Obesity
Dandona, P., & Dhindsa, S. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2724 · Cited by 313 · 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
Paediatric and adult-onset male hypogonadism
Salonia, A., Rastrelli, G., Hackett, G., Seminara, S. B., Huhtaniemi, I. T., Rey, R. A., Hellstrom, W. J. G., Palmert, M. R., Corona, G., Dohle, G. R., et al. (2019) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0087-y · Cited by 286 · see citing works
Self-citationGrossmann, M., & Matsumoto, A. M. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3580 · Cited by 246 · see citing works
Current and investigational medications for the treatment of sarcopenia
Rolland, Y., Dray, C., Vellas, B., & Barreto, P. D. S. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155597 · Cited by 195 · see citing works
Probiotic Microbes Sustain Youthful Serum Testosterone Levels and Testicular Size in Aging Mice
Poutahidis, T., Springer, A., Levkovich, T., Qi, P., Varian, B. J., Lakritz, J. R., Ibrahim, Y. M., Chatzigiagkos, A., Alm, E. J., & Erdman, S. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084877 · Cited by 177 · see citing works
Hypogonadism and male obesity: Focus on unresolved questions
Grossmann, M. (2018) · Clinical Endocrinology · doi:10.1111/cen.13723 · Cited by 164 · see citing works
Risks and benefits of testosterone therapy in older men
Spitzer, M., Huang, G., Basaria, S., Travison, T. G., & Bhasin, S. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.73 · Cited by 154 · see citing works
Obesity and late-onset hypogonadism
Corona, G., Vignozzi, L., Sforza, A., Mannucci, E., & Maggi, M. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.06.031 · Cited by 154 · see citing works
Ng Tang Fui, M., Prendergast, L. A., Dupuis, P., Raval, M., Strauss, B. J., Zajac, J. D., & Grossmann, M. (2016) · BMC Medicine · doi:10.1186/s12916-016-0700-9 · Cited by 124 · see citing works
How to recognize late-onset hypogonadism in men with sexual dysfunction
Corona, G., Rastrelli, G., Vignozzi, L., Mannucci, E., & Maggi, M. (2012) · Asian Journal of Andrology · doi:10.1038/aja.2011.138 · Cited by 108 · see citing works
Lotti, F., Corona, G., Degli Innocenti, S., Filimberti, E., Scognamiglio, V., Vignozzi, L., Forti, G., & Maggi, M. (2013) · Andrology · doi:10.1111/j.2047-2927.2012.00031.x · Cited by 96 · see citing works
Self-citationHypogonadism in the HIV-infected man
Rochira, V., & Guaraldi, G. (2014) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2014.06.005 · Cited by 95 · see citing works
Male late-onset hypogonadism: pathogenesis, diagnosis and treatment
Huhtaniemi, I., & Forti, G. (2011) · Nature Reviews Urology · doi:10.1038/nrurol.2011.47 · Cited by 88 · see citing works
Self-citationTreatment of Functional Hypogonadism Besides Pharmacological Substitution
Corona, G., Rastrelli, G., Morelli, A., Sarchielli, E., Cipriani, S., Vignozzi, L., & Maggi, M. (2020) · The World Journal of Men's Health · doi:10.5534/wjmh.190061 · Cited by 87 · see citing works
Cigarette smoking has a positive and independent effect on testosterone levels
Wang, W., Yang, X., Liang, J., Liao, M., Zhang, H., Qin, X., Mo, L., Lv, W., & Mo, Z. (2013) · Hormones · doi:10.14310/horm.2002.1445 · Cited by 79 · see citing works
Kaminetsky, J., Werner, M., Fontenot, G., & Wiehle, R. D. (2013) · The Journal of Sexual Medicine · doi:10.1111/jsm.12116 · Cited by 78 · see citing works
Golan, R., Scovell, J. M., & Ramasamy, R. (2015) · The Aging Male · doi:10.3109/13685538.2015.1052392 · Cited by 73 · see citing works
O’Reilly, M. W., Glisic, M., Kumarendran, B., Subramanian, A., Manolopoulos, K. N., Tahrani, A. A., Keerthy, D., Muka, T., Toulis, K. A., Hanif, W., et al. (2019) · Clinical Endocrinology · doi:10.1111/cen.13862 · Cited by 72 · see citing works
Sex Differences in the Contributions of Visceral and Total Body Fat to Blood Pressure in Adolescence
Pausova, Z., Mahboubi, A., Abrahamowicz, M., Leonard, G. T., Perron, M., Richer, L., Veillette, S., Gaudet, D., & Paus, T. (2012) · Hypertension · doi:10.1161/hypertensionaha.111.180372 · Cited by 70 · see citing works
Morelli, A., Filippi, S., Comeglio, P., Sarchielli, E., Cellai, I., Pallecchi, M., Bartolucci, G., Danza, G., Rastrelli, G., Corno, C., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00377.2018 · Cited by 59 · see citing works
Colleluori, G., Chen, R., Turin, C. G., Vigevano, F., Qualls, C., Johnson, B., Mediwala, S., Villareal, D. T., & Armamento-Villareal, R. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00277 · Cited by 43 · see citing works
Perspective: Regulatory Agencies' Changes to Testosterone Product Labeling
Corona, G., & Maggi, M. (2015) · The Journal of Sexual Medicine · doi:10.1111/jsm.12951 · Cited by 41 · see citing works
Male Obesity Associated Gonadal Dysfunction and the Role of Bariatric Surgery
Sultan, S., Patel, A. G., El-Hassani, S., Whitelaw, B., Leca, B. M., Vincent, R. P., le Roux, C. W., Rubino, F., Aywlin, S. J. B., & Dimitriadis, G. K. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00408 · Cited by 39 · see citing works
Testosterone administration in older men
Matsumoto, A. M. (2013) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2013.02.011 · Cited by 32 · see citing works
Ageing male (part I): Pathophysiology and diagnosis of functional hypogonadism
Huhtaniemi, I. T., & Wu, F. C. W. (2022) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2022.101622 · Cited by 31 · see citing works
Self-citationTestosterone therapy in older men with late-onset hypogonadism: a counter-rationale
Basaria, S. (2013) · Endocrine Practice · doi:10.4158/ep13318.ra · Cited by 18 · see citing works
Is There Room for SERMs or SARMs as Alternative Therapies for Adult Male Hypogonadism?
Giagulli, V. A., Silvestrini, A., Bruno, C., Triggiani, V., Mordente, A., & Mancini, A. (2020) · International Journal of Endocrinology · doi:10.1155/2020/9649838 · Cited by 14 · see citing works
Mulhall, J. P., Brock, G. B., Glina, S., Baygani, S., Donatucci, C. F., & Maggi, M. (2016) · The Journal of Sexual Medicine · doi:10.1016/j.jsxm.2016.02.163 · Cited by 7 · see citing works
Association between serum cotinine and total testosterone in adult males based on NHANES 2011–2016
Liu, M., Gou, Y., Zou, B., Li, X., & Yang, P. (2024) · Scientific Reports · doi:10.1038/s41598-024-74482-6 · Cited by 3 · see citing works
- Authors
- Tajar, A., Forti, G., O'Neill, T. W., Lee, D. M., Silman, A. J., Finn, J. D., Bartfai, G., Boonen, S., Casanueva, F. F., Giwercman, A., Han, T. S., Kula, K., Labrie, F., Lean, M. E. J., Pendleton, N., Punab, M., Vanderschueren, D., Huhtaniemi, I. T., Wu, F. C. W., & the EMAS Group
- Affiliations
- University of Manchester (GB)
- University of Florence (IT)
- Arthritis Research Campaign Epidemiology Unit (A.T., T.W.O., D.M.L., A.J.S., J.D.F.), The University of Manchester, Manchester M15 6PB, United Kingdom
- Department of Obstetrics, Gynaecology, and Andrology (G.B.), Albert Szent-György Medical University, H-6725 Szeged, Hungary
- KU Leuven (BE)
- Instituto de Salud Carlos III (ES)
- Lund University (SE)
- The Royal Free Hospital (GB)
- Medical University of Lodz (PL)
- Université Laval (CA)
- University of Glasgow (GB)
- Tartu University Hospital (EE)
- Imperial College London (GB)
- Manchester Academic Health Science Centre (GB)
- Corresponding author
- Wu, Frederick C. W.
- ORCID
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2010-04-01
- Volume
- 95
- Issue
- 4
- Pages
- 1810-1818
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2110425298
- Cited by
- 604
- References
- 40
- Citations by year
- 2026: 22 · 2025: 34 · 2024: 39 · 2023: 35 · 2022: 49 · 2021: 46 · 2020: 51 · 2019: 33 · 2018: 46 · 2017: 44 · 2016: 36 · 2015: 34 · 2014: 39 · 2013: 24 · 2012: 29
- FWCI
- 22.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- andropause, secondary hypogonadism, hypergonadotropic hypogonadism, older men, testosterone, luteinizing hormone, obesity, comorbidities, sexual symptoms, somatic symptoms, European Male Ageing Study
- MeSH terms
- Adult, Aged, Aging, Alcohol Drinking, Anthropometry, Cross-Sectional Studies, Estradiol, Europe, Health Status, Humans, Hypogonadism, Erectile Dysfunction, Male, Middle Aged, Motor Activity, Obesity, Surveys and Questionnaires, Regression Analysis, Risk Factors, Smoking, Testosterone, White People
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