Low Testosterone in Men with Type 2 Diabetes: Significance and Treatment

Grossmann, Mathis

doi:10.1210/jc.2011-0118

Cited by 350Hormonal and reproductive studiesDiabetes, Cardiovascular Risks, and LipoproteinsSperm and Testicular Function

Low Testosterone in Men with Type 2 Diabetes: Significance and Treatment

Grossmann, Mathis·2011·The Journal of Clinical Endocrinology & Metabolism

DOI 10.1210/jc.2011-0118

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Abstract

CONTEXT: The relationship between testosterone and diabetes in men is an important issue, given that one third of U.S. men aged 65 yr or older have diabetes, with a similar percentage having low testosterone levels. EVIDENCE ACQUISITION: The medical literature from 1970 to March 2011 was reviewed for key articles. EVIDENCE SYNTHESIS: In population-based studies, low testosterone is commonly associated with type 2 diabetes and the metabolic syndrome, and it identifies men with an adverse metabolic profile. The difference in testosterone levels between men with diabetes compared to men without diabetes is moderate and comparable in magnitude to the effects of other chronic diseases, suggesting that low testosterone may be a marker of poor health. Although the inverse association of testosterone with diabetes is partially mediated by SHBG, low testosterone is linked to diabetes via a bidirectional relationship with visceral fat, muscle, and possibly bone. There is consistent evidence from randomized trials that testosterone therapy alters body composition in a metabolically favorable manner, but changes are modest and have not consistently translated into reductions in insulin resistance or improvements in glucose metabolism. CONCLUSIONS: The key response to the aging, overweight man with type 2 diabetes and subnormal testosterone levels should be implementation of lifestyle measures such as weight loss and exercise, which, if successful, raise testosterone and provide multiple health benefits. Although approved therapy for diabetes should be used, testosterone therapy should not be given to such men until benefits and risks are clarified by adequately powered clinical trials.

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Weight loss, whether by diet or surgery, increases testosterone levels proportional to the amount of weight lost.
“Finally, as discussed in more detail in section 5, weight loss, whether by diet or surgery, increases testosterone levels proportional to the amount of weight lost.1934”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [19]
Given that VAT is more closely related to insulin resistance and cardiovascular risk than SAT, inconsistent effect of testosterone on VAT may be one possible explanation as to why testosterone treatment, despite reduction of fat mass, has not consistently led to improvements in measures of glucose metabolism.
“Given that VAT is more closely related to insulin resistance and cardiovascular risk than SAT, inconsistent effect of testosterone on VAT may be one possible explanation as to why testosterone treatment, despite reduction of fat mass, has not consistently led to improvements in measures of glucose metabolism.19”
From Lowered testosterone in male obesity: Mechanisms, morbidity and management (2014) · cites this paper as [19]
Weight loss is associated with marked increases in circulating testosterone that rise in proportion to the amount of weight lost.
“Weight loss is associated with marked increases in circulating testosterone that rise in proportion to the amount of weight lost.46”
From Hypogonadism and male obesity: Focus on unresolved questions (2018) · cites this paper as [46]
Reversal of HPT axis suppression with weight loss suggests a pathogenic role for excess adipose tissue.
“While exact mechanisms are unknown, the reversal of HPT axis suppression with weight loss 43,46,47 suggests a pathogenic role for excess adipose tissue.”
From Hypogonadism and male obesity: Focus on unresolved questions (2018) · cites this paper as [46]
Successful weight loss can lead to increases in testosterone in obese men.
“Consistent with these observational data, successful weight loss can lead to increases in testosterone in obese men (Fig. 2; Supplemental Table 1) (20).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [20]

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Hammoud, A., Gibson, M., Hunt, S. C., Adams, T. D., Carrell, D. T., Kolotkin, R. L., & Meikle, A. W. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1598 · Cited by 207 · see citing works
Late onset of obesity in male androgen receptor-deficient (AR KO) mice
Sato, T., Μatsumoto, T., Yamada, T., Watanabe, T., Kawano, H., & Kato, S. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02774-2 · Cited by 196 · see citing works
Increase in visceral and subcutaneous abdominal fat in men with prostate cancer treated with androgen deprivation therapy
Hamilton, E. J., Gianatti, E., Strauss, B. J., Wentworth, J. M., Joon, D. L., Bolton, D. M., Zajac, J. D., & Grossmann, M. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03942.x · Cited by 196 · see citing works
Self-citation
Association of Testosterone and Sex Hormone–Binding Globulin With Metabolic Syndrome and Insulin Resistance in Men
Li, C., Ford, E. S., Li, B., Giles, W. H., & Liu, S. (2010) · Diabetes Care · doi:10.2337/dc09-1788 · Cited by 194 · see citing works
Testosterone Increases Lipolysis and the Number of β-Adrenoceptors in Male Rat Adipocytes*
Xu, X., Pergola, G. D., & Björntorp, P. A. (1991) · Endocrinology · doi:10.1210/endo-128-1-379 · Cited by 190 · see citing works
The effects of testosterone on insulin sensitivity in male rats
Holmäng, A. B., & Björntorp, P. A. (1992) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1992.tb09452.x · Cited by 189 · see citing works
Sex Steroid Hormones, Upper Body Obesity, and Insulin Resistance
Abate, N., Haffner, S. M., Garg, A., Peshock, R. M., & Grundy, S. M. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020567 · Cited by 187 · see citing works
Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome. A randomized trial
Esposito, K., Marfella, R., & Ciotola, M. (2004) · ACC Current Journal Review · doi:10.1016/j.accreview.2004.11.073 · Cited by 174 · see citing works
ORIGINAL ARTICLE: Accuracy of calculated free testosterone formulae in men
Ly, L. P., Sartorius, G., Hull, L., Leung, A., Swerdloff, R. S., Wang, C., & Handelsman, D. J. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03804.x · Cited by 172 · see citing works
Androgens and obesity
Allan, C. A., & McLachlan, R. I. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e3283398ee2 · Cited by 168 · see citing works
Correlates of low testosterone and symptomatic androgen deficiency in a population-based sample
Hall, S. A., Esche, G. R., Araujo, A. B., Travison, T. G., Clark, R. V., Williams, R. E., & McKinlay, J. B. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0021 · Cited by 167 · see citing works
Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels
Yeap, B. B., Chubb, S. A. P., Flicker, L. A., McCaul, K. A., Ebeling, P. R., Beilby, J. P., & Norman, P. E. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0414 · Cited by 162 · see citing works
The Effect of Weight Loss on Reproductive Hormones in Obese Men*
STANIK, S., DORNFELD, L. P., MAXWELL, M. H., VIOSCA, S. P., & KORENMAN, S. G. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-53-4-828 · Cited by 156 · see citing works
Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men
Vikan, T., Schirmer, H., Njølstad, I., & Svartberg, J. (2010) · European Journal of Endocrinology · doi:10.1530/eje-09-0943 · Cited by 151 · cited 1× · see citing works
“This positive association of estradiol with diabetes has been confirmed in more recent crosssectional (79) and prospective (20) studies and remained significant after multivariate adjustment including waist circumference (20, 79).”
Background
Intensified glucose lowering in type 2 diabetes: time for a reappraisal
Yudkin, J. S., Richter, B., & Gale, E. A. M. (2010) · Diabetologia · doi:10.1007/s00125-010-1864-z · Cited by 147 · see citing works
Genomic actions of the androgen receptor are required for normal male sexual differentiation in a mouse model
Notini, A. J., Davey, R. A., McManus, J. F., Bate, K. L., & Zajac, J. D. (2005) · Journal of Molecular Endocrinology · doi:10.1677/jme.1.01884 · Cited by 145 · see citing works
Inverse Association of Testosterone and the Metabolic Syndrome in Men Is Consistent across Race and Ethnic Groups
Kupelian, V. A., Hayes, F. J., Link, C. L., Rosen, R. C., & McKinlay, J. B. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0054 · Cited by 140 · see citing works
Male Hypogonadism in Systemic Disease
Kalyani, R. R., Gavini, S., & Dobs, A. S. (2007) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2007.03.014 · Cited by 137 · see citing works
Lower serum testosterone is independently associated with insulin resistance in non-diabetic older men: the Health In Men Study
Yeap, B. B., Chubb, S. A. P., Hyde, Z., Jamrozik, K., Hankey, G. J., Flicker, L., & Norman, P. E. (2009) · European Journal of Endocrinology · doi:10.1530/eje-09-0348 · Cited by 128 · see citing works
Hepatic steatosis is associated with low serum testosterone and high serum DHEAS levels in men
Völzke, H., Aumann, N., Krebs, A., Nauck, M. A., Steveling, A., Lerch, M. M., Rosskopf, D., & Wallaschofski, H. (2009) · International Journal of Andrology · doi:10.1111/j.1365-2605.2009.00953.x · Cited by 123 · 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
Reversal of the hypogonadotropic hypogonadism of obese men by administration of the aromatase inhibitor testolactone
Zumoff, B., Miller, L. K., & Strain, G. W. (2003) · Metabolism · doi:10.1016/s0026-0495(03)00186-0 · Cited by 118 · see citing works
Testosterone in Obesity, Metabolic Syndrome and Type 2 Diabetes
Stanworth, R. D., & Jones, T. H. (2008) · Frontiers of hormone research · doi:10.1159/000176046 · Cited by 117 · see citing works
NCEP-ATPIII-Defined Metabolic Syndrome, Type 2 Diabetes Mellitus, and Prevalence of Hypogonadism in Male Patients with Sexual Dysfunction
Corona, G., Mannucci, E., Petrone, L., Balercia, G., Paggi, F., Fisher, A. D., Lotti, F., Chiarini, V., Fedele, D., Forti, G., et al. (2007) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2007.00529.x · Cited by 115 · see citing works
Why Is Androgen Replacement in Males Controversial?
Cunningham, G. R., & Toma, S. M. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0266 · Cited by 111 · see citing works
Testosterone and type 2 diabetes
Grossmann, M., Gianatti, E. J., & Zajac, J. D. (2010) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e32833919cf · Cited by 108 · see citing works
Self-citation
A 1-Year Lifestyle Intervention for Weight Loss in Individuals With Type 2 Diabetes Reduces High C-Reactive Protein Levels and Identifies Metabolic Predictors of Change
Belalcazar, L. M., Reboussin, D. M., Haffner, S. M., Hoogeveen, R. C., Kriska, A. M., Schwenke, D. C., Tracy, R. P., Pi-Sunyer, X., & Ballantyne, C. M. (2010) · Diabetes Care · doi:10.2337/dc10-0728 · Cited by 104 · see citing works
Prevalence, incidence and risk factors of testosterone deficiency in a population-based cohort of men: results from the study of health in Pomerania
Haring, R., Ittermann, T., Völzke, H., Krebs, A., Zygmunt, M., Felix, S. B., Grabe, H. J., Nauck, M. A., & Wallaschofski, H. (2010) · The Aging Male · doi:10.3109/13685538.2010.487553 · Cited by 101 · see citing works
Sex Hormone-Binding Globulin as an Independent Predictor of Incident Type 2 Diabetes Mellitus in Men
Lakshman, K. M., Bhasin, S., & Araujo, A. B. (2010) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glq002 · Cited by 100 · 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
Testosterone modulates gene expression pathways regulating nutrient accumulation, glucose metabolism and protein turnover in mouse skeletal muscle
Haren, M. T., Siddiqui, A. M., Armbrecht, H. J., Kevorkian, R. T., Kim, M. J., Haas, M. J., Mazza, A. D., Kumar, V. B., Green, M., Banks, W. A., et al. (2010) · International Journal of Andrology · doi:10.1111/j.1365-2605.2010.01061.x · Cited by 99 · see citing works
Do the Effects of Testosterone on Muscle Strength, Physical Function, Body Composition, And Quality of Life Persist Six Months after Treatment in Intermediate-Frail and Frail Elderly Men?
O'Connell, M. D. L., Roberts, S. A., Srinivas-Shankar, U., Tajar, A., Connolly, M. J., Adams, J. E., Oldham, J. A., & Wu, F. C. W. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1167 · Cited by 98 · see citing works
Association of Endogenous Sex Hormones With Diabetes andImpaired Fasting Glucose in Men
Colangelo, L. A., Ouyang, P., Liu, K., Kopp, P. A., Golden, S. H., Dobs, A. S., Szklo, M., Vaidya, D. M., Cushman, M., & Gapstur, S. M. (2009) · Diabetes Care · doi:10.2337/dc08-2216 · Cited by 90 · see citing works
Long-Term Effects of Dihydrotestosterone Treatment on Prostate Growth in Healthy, Middle-Aged Men Without Prostate Disease
Idan, A., Griffiths, K. A., Harwood, D. T., Seibel, M. J., Turner, L., Conway, A. J., & Handelsman, D. J. (2010) · Annals of Internal Medicine · doi:10.7326/0003-4819-153-10-201011160-00004 · Cited by 89 · see citing works
Androgens and cardiovascular disease
Yeap, B. B. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283383031 · Cited by 86 · see citing works
Relation of Steroid Hormones to Glucose Tolerance and Plasma Insulin Levels in Men: Importance of visceral adipose tissue
Tchernof, A., Despres, J., Dupont, A., Bélanger, A., Nadeau, A., Prud'homme, D., Moorjani, S., Lupien, P., & Labrie, F. (1995) · Diabetes Care · doi:10.2337/diacare.18.3.292 · Cited by 83 · see citing works
The Role of Testosterone in the Etiology and Treatment of Obesity, the Metabolic Syndrome, and Diabetes Mellitus Type 2
Saad, F., & Gooren, L. J. (2010) · Journal of Obesity · doi:10.1155/2011/471584 · Cited by 81 · see citing works
Hyperleptinemia without Obesity in Male Mice Lacking Androgen Receptor in Adipose Tissue
Yu, I.-C. I., Lin, H., Liu, N.-C., Wang, R.-S., Sparks, J. D., Yeh, S., & Chang, C. (2008) · Endocrinology · doi:10.1210/en.2007-0516 · Cited by 80 · see citing works
Inhibin B in Men with Severe Obesity and After Weight Reduction Following Gastroplasty
Globerman, H., Shen‐Orr, Z., Karnieli, E., Aloni, Y., & CHARUZI, I. (2005) · Endocrine Research · doi:10.1080/07435800500228971 · Cited by 79 · see citing works
Effects of Aerobic and Resistance Training on Hemoglobin A1c Levels in Patients With Type 2 Diabetes: A Randomized Controlled Trial
Schinner, S. (2011) · Yearbook of Medicine · doi:10.1016/s0084-3873(11)00368-3 · Cited by 75 · see citing works
Treatment of Hypogonadism with Testosterone in Patients with Type 2 Diabetes Mellitus
Gopal, R. A., Bothra, N., Acharya, S. V., Ganesh, H. K., Bandgar, T., Menon, P. S., & Shah, N. S. (2010) · Endocrine Practice · doi:10.4158/ep09355.or · Cited by 72 · see citing works
Myocyte Androgen Receptors Increase Metabolic Rate and Improve Body Composition by Reducing Fat Mass
Fernando, S. M., Rao, P., Niel, L., Chatterjee, D., Stagljar, M., & Monks, D. A. (2010) · Endocrinology · doi:10.1210/en.2010-0018 · Cited by 69 · see citing works
Androgen deprivation therapy in men with prostate cancer: how should the side effects be monitored and treated?
Grossmann, M., & Zajac, J. D. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03939.x · Cited by 68 · see citing works
Self-citation
Plasma adrenal, gonadal, and conjugated steroids following long-term exercise-induced negative energy balance in identical twins
Pritchard, J., Després, J.-P., Gagnon, J., Tchernof, A., Nadeau, A., Tremblay, A., & Bouchard, C. (1999) · Metabolism · doi:10.1016/s0026-0495(99)90125-7 · Cited by 62 · see citing works
Low testosterone and anaemia in men with type 2 diabetes
Grossmann, M., Panagiotopolous, S., Sharpe, K., MacIsaac, R. J., Clarke, S., Zajac, J. D., Jerums, G., & Thomas, M. C. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03357.x · Cited by 60 · see citing works
Self-citation
Associations of endogenous testosterone and SHBG with glycated haemoglobin in middle-aged and older men
Brand, J. S., Wareham, N. J., Dowsett, M., Folkerd, E. J., van der Schouw, Y. T., Luben, R., & Khaw, K. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03951.x · Cited by 55 · see citing works
Anabolic Applications of Androgens for Functional Limitations Associated with Aging and Chronic Illness
Bhasin, S., & Storer, T. W. (2008) · Frontiers of hormone research · doi:10.1159/000176052 · Cited by 37 · see citing works
Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts Male Aging Study
(2000) · The Aging Male · doi:10.1080/13685530008500343 · Cited by 30 · see citing works
Effects of Testosterone Undecanoate on Cardiovascular Risk Factors and Atherosclerosis in Middle-Aged Men with Late-Onset Hypogonadism and Metabolic Syndrome: Results from a 24-month, Randomized, Double-Blind, Placebo-Controlled Study
Shindel, A. W. (2011) · Yearbook of Urology · doi:10.1016/j.yuro.2010.12.031 · Cited by 22 · see citing works
Relationship Between Testosterone Levels, Insulin Sensitivity, and Mitochondrial Function in Men
Kaplan, S. A., & Crawford, E. D. (2006) · Diabetes Care · doi:10.2337/diacare.29.03.06.dc05-2100 · Cited by 20 · see citing works
Sex hormone levels in men undergoing bariatric surgery
Omana, J. J., Tamler, R., Strohmayer, E., Herron, D. M., & Kini, S. U. (2009) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2009.06.042 · Cited by 19 · see citing works
Testosterone and modifiable risk factors associated with diabetes in men
Atlantis, E. E., Lange, K. M., Martin, S., Haren, M. T., Taylor, A. W., O’Loughlin, P. D., Marshall, V. R., & Wittert, G. (2011) · Maturitas · doi:10.1016/j.maturitas.2010.12.007 · Cited by 16 · see citing works
The androgen receptor CAG repeat polymorphism
Zitzmann, M., Gromoll, J., & Nieschlag, E. (2005) · Andrologia · doi:10.1111/j.1439-0272.2005.00692.x · Cited by 14 · see citing works

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Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus
Kautzky-Willer, A., Harreiter, J., & Pacini, G. (2016) · Endocrine Reviews · doi:10.1210/er.2015-1137 · Cited by 2,043 · see citing works
Testosterone and obesity
Kelly, D. M., & Jones, T. H. (2015) · Obesity Reviews · doi:10.1111/obr.12282 · Cited by 487 · see citing works
Age-associated changes in hypothalamic-pituitary-testicular function in middle-aged and older men are modified by weight change and lifestyle factors: longitudinal results from the European male ageing study
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
Testosterone treatment to prevent or revert type 2 diabetes in men enrolled in a lifestyle programme (T4DM): a randomised, double-blind, placebo-controlled, 2-year, phase 3b trial
Wittert, G., Bracken, K., Robledo, K. P., Grossmann, M., Yeap, B. B., Handelsman, D. J., Stuckey, B., Conway, A., Inder, W., McLachlan, R., et al. (2021) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(20)30367-3 · Cited by 362 · see citing works
Self-citation
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
Self-citation
Testosterone and insulin resistance in the metabolic syndrome and T2DM in men
Rao, P. M., Kelly, D. M., & Jones, T. H. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.122 · Cited by 292 · see citing works
4. Comprehensive Medical Evaluation and Assessment of Comorbidities: <i>Standards of Medical Care in Diabetes—2022</i>
American Diabetes Association Professional Practice Committee (2022) · Diabetes Care · doi:10.2337/dc22-s004 · Cited by 285 · see citing works
The role of androgens in metabolism, obesity, and diabetes in males and females
Navarro, G., Allard, C., Xu, W., & Mauvais‐Jarvis, F. (2015) · Obesity · doi:10.1002/oby.21033 · Cited by 289 · see citing works
A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management
Grossmann, M., & Matsumoto, A. M. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3580 · Cited by 246 · see citing works
Self-citation
Hypogonadism and male obesity: Focus on unresolved questions
Grossmann, M. (2018) · Clinical Endocrinology · doi:10.1111/cen.13723 · Cited by 164 · see citing works
Self-citation
Reference Ranges and Determinants of Testosterone, Dihydrotestosterone, and Estradiol Levels Measured using Liquid Chromatography-Tandem Mass Spectrometry in a Population-Based Cohort of Older Men
Yeap, B. B., Alfonso, H., Chubb, S. A. P., Handelsman, D. J., Hankey, G. J., Norman, P. E., & Flicker, L. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2265 · Cited by 155 · see citing works
Effects of testosterone treatment on glucose metabolism and symptoms in men with type 2 diabetes and the metabolic syndrome: a systematic review and meta‐analysis of randomized controlled clinical trials
Grossmann, M., Hoermann, R., Wittert, G., & Yeap, B. B. (2015) · Clinical Endocrinology · doi:10.1111/cen.12664 · Cited by 139 · see citing works
Self-citation
Muscle wasting and aging: Experimental models, fatty infiltrations, and prevention
Brioche, T., Pagano, A. F., Py, G., & Chopard, A. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.04.006 · Cited by 129 · see citing works
Effects of testosterone treatment on body fat and lean mass in obese men on a hypocaloric diet: a randomised controlled trial
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
Self-citation
The impact of testosterone replacement therapy on glycemic control, vascular function, and components of the metabolic syndrome in obese hypogonadal men with type 2 diabetes
Groti, K., Žuran, I., Antonič, B., Foršnarič, L., & Pfeifer, M. (2018) · The Aging Male · doi:10.1080/13685538.2018.1468429 · Cited by 117 · see citing works
Late‐onset hypogonadism: metabolic impact
Grossmann, M., Ng Tang Fui, M., & Cheung, A. S. (2020) · Andrology · doi:10.1111/andr.12705 · Cited by 95 · see citing works
Self-citation
Males with obesity and overweight
Kim, K.-B., & Shin, Y.-A. (2020) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes20008 · Cited by 82 · see citing works
Effect of Testosterone Treatment on Constitutional and Sexual Symptoms in Men With Type 2 Diabetes in a Randomized, Placebo-Controlled Clinical Trial
Gianatti, E. J., Dupuis, P., Hoermann, R., Zajac, J. D., & Grossmann, M. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1872 · Cited by 67 · see citing works
Self-citation
Hematological changes during androgen deprivation therapy
Grossmann, M., & Zajac, J. D. (2012) · Asian Journal of Andrology · doi:10.1038/aja.2011.102 · Cited by 62 · see citing works
Self-citation
Associations of insulin‐like growth factor‐I and its binding proteins and testosterone with frailty in older men
Yeap, B. B., Paul Chubb, S. A., Lopez, D., Ho, K. K. Y., Hankey, G. J., & Flicker, L. (2013) · Clinical Endocrinology · doi:10.1111/cen.12052 · Cited by 53 · see citing works
Undiagnosed prediabetes is highly prevalent in primary infertile men - results from a cross-sectional study
Boeri, L., Capogrosso, P., Ventimiglia, E., Pederzoli, F., Frego, N., Cazzaniga, W., Chierigo, F., Alfano, M., Piemonti, L., Viganò, P., et al. (2019) · BJU International · doi:10.1111/bju.14558 · Cited by 45 · see citing works
Prediabetes is associated with an increased risk of testosterone deficiency, independent of obesity and metabolic syndrome
Ho, C.-H., Yu, H.-J., Wang, C.-Y., Jaw, F.-S., Hsieh, J.-T., Liao, W.-C., Pu, Y.-S., & Liu, S.-P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074173 · Cited by 40 · see citing works
Independent Effects of Testosterone on Lipid Oxidation and VLDL-TG Production
Høst, C., Gormsen, L. C., Christensen, B., Jessen, N., Hougaard, D. M., Christiansen, J. S., Pedersen, S. B., Jensen, M. D., Nielsen, S., & Gravholt, C. H. (2013) · Diabetes · doi:10.2337/db12-0440 · Cited by 37 · see citing works
Is polycystic ovary syndrome a sexual conflict? A review
Casarini, L., Simoni, M., & Brigante, G. (2016) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.01.011 · Cited by 28 · see citing works
Increased Free testosterone levels in men with uncontrolled type 2 diabetes five years after randomization to bariatric surgery
Pham, N. H., Bena, J., Bhatt, D. L., Kennedy, L., Schauer, P. R., & Kashyap, S. R. (2018) · Obesity Surgery · doi:10.1007/s11695-017-2881-5 · Cited by 21 · see citing works
The effects of type 1 and type 2 diabetes mellitus on bone health in chronic kidney disease
Aleksova, J., Ebeling, P., & Elder, G. (2025) · Nature Reviews Endocrinology · doi:10.1038/s41574-024-01083-8 · Cited by 20 · see citing works
Stem cell activation in adults can reverse detrimental changes in body composition to reduce fat and increase lean mass in both sexes
Wiren, K. M., Hashimoto, J. G., & Zhang, X.-W. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23288 · Cited by 5 · see citing works

Exogenous Glucocorticoids and a High-Fat Diet Cause Severe Hyperglycemia and Hyperinsulinemia and Limit Islet Glucose Responsiveness in Young Male Sprague-Dawley Rats
Beaudry, J. L., D'souza, A. M., Teich, T., Tsushima, R. G., & Riddell, M. C. (2013) · Endocrinology · doi:10.1210/en.2012-2114 · Cited by 44 · see citing works
The Effect of Fasting on Tissue Cyclic cAMP and Plasma Glucagon in the Obese Hyperglycemic Mouse
VINE, R. L. L., Voyles, N. R., Perrino, P. V., & Recant, L. (1975) · Endocrinology · doi:10.1210/endo-97-3-615 · Cited by 38 · see citing works
Modulation of Adipoinsular Axis in Prediabetic Zucker Diabetic Fatty Rats by Diazoxide
Alemzadeh, R., & Tushaus, K. (2004) · Endocrinology · doi:10.1210/en.2003-1523 · Cited by 38 · see citing works
The Paraventricular Nucleus of the Hypothalamus Has a Major Role in Thyroid Hormone Feedback Regulation of Thyrotropin Synthesis and Secretion
Taylor, T., Wondisford, F. E., Blaine, T. A., & Weintraub, B. D. (1990) · Endocrinology · doi:10.1210/endo-126-1-317 · Cited by 54 · see citing works
Growth hormone binding protein in the rat: effects of gonadal steroids
Carmignac, D. F., Gabrielsson, B. G., & Robinson, I. C. A. F. (1993) · Endocrinology · doi:10.1210/endo.133.6.8243263 · Cited by 68 · see citing works

Authors: Grossmann, M.
Affiliations: The University of Melbourne (AU)
Corresponding author: Grossmann, Mathis
ORCID: Grossmann, Mathis
Venue: The Journal of Clinical Endocrinology & Metabolism
Publisher: The Endocrine Society
Published: 2011-08
Volume: 96
Issue: 8
Pages: 2341-2353
ISSN: 0021-972X (ISSN-L)
1945-7197
DOI: 10.1210/jc.2011-0118
OpenAlex: W2052908410
Semantic Scholar: 02ca366051d56bcc9b4342c6af536316a1bace52
Cited by: 350
References: 119
Citations by year: 2026: 17 · 2025: 30 · 2024: 21 · 2023: 24 · 2022: 12 · 2021: 24 · 2020: 21 · 2019: 15 · 2018: 25 · 2017: 25 · 2016: 26 · 2015: 24 · 2014: 31 · 2013: 31 · 2012: 21
FWCI: 22.19
Type: journal article
Language: en
Open access: closed
Locations: The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords: androgen deficiency, type 2 diabetes, men, testosterone replacement therapy, sex hormone-binding globulin, metabolic syndrome, insulin resistance, visceral fat, body composition, lifestyle intervention, weight loss, physical activity, aging
MeSH terms: Androgens, Diabetes Mellitus, Type 2, Humans, Hypogonadism, Male, Testosterone

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Low Testosterone in Men with Type 2 Diabetes: Significance and Treatment

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