Prevalence of low testosterone levels in men with type 2 diabetes mellitus: a cross-sectional study
Open accessAbstract
BACKGROUND: A high prevalence of low serum testosterone (LST) in men with type 2 diabetes have been reported worldwide. The aim of this study was to determine the prevalence and associated factors of LST in men with type 2 diabetes. MATERIALS AND METHODS: This was a cross-sectional study, conducted among 1,089 men (aged 30-70 years) with type 2 diabetes who consecutively attended a major diabetes center in Amman, Jordan, between August 2008 and February 2009. The patients' demographic characteristics were collected using a prestructured questionnaire. Duration of diabetes, smoking habits, presence of retinopathy, neuropathy, and nephropathy were collected from the medical records. All participants were asked to complete the Androgen Deficiency in Ageing Male (ADAM) questionnaire. Venous blood sample was collected to test for total testosterone (TT), free testosterone (FT), sex hormone binding globulin (SHBG), follicle-stimulating hormone (FSH), luteinizing hormone (LH), prolactin (PRL), serum lipids, and glycosylated hemoglobin (HbA1c). LST was defined as TT <3 ng/ml. RESULTS: Overall, 36.5% of patients with diabetes had TT level <3 ng/ml and 29% had symptoms of androgen deficiency. Of those with serum testosterone level <3 ng/ml, 80.2% had symptoms of androgen deficiency, 16.9% had primary hypogonadism (HG), and 83.1% had secondary HG. Univariate analysis showed a significant relationship between age, income, education, body mass index (BMI), smoking, duration of diabetes, diabetic nephropathy, diabetic neuropathy, and HbA1c. Multivariate logistic regression analysis indicated age, income, BMI, and diabetic neuropathy as the independent risk factors of LST. CONCLUSIONS: The prevalence of LST among men with type 2 diabetes is high. Age, income, BMI, and diabetic neuropathy were found to be the independent risk factors for LST.
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Men with a history of unexplained anemia, bone density loss, diabetes, exposure to chemotherapy, direct or scatter radiation therapy to the testes, HIV, chronic narcotic use, infertility, pituitary disorders, or chronic corticosteroid use are at risk for low testosterone.
“A meta-analysis of the literature suggests that men who have a history of unexplained anemia, 7 bone density loss, 8 diabetes, 9 exposure to chemotherapy, 10 direct or scatter radiation therapy to the testes, 11 HIV, 12 a history of chronic narcotic use, 13 infertility, 14 pituitary disorders, 15 and chronic corticosteroid use 16 are at risk for low testosterone.”
From Evaluation and Management of Testosterone Deficiency: AUA Guideline (2018) · cites this paper as [9]
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Cites
Wilkinson, C. P., Ferris, F. L., Klein, R., Lee, P. P., Agardh, C., Davis, M., Dills, D. G., Kampik, A., Pararajasegaram, R., & Verdaguer, J. (2003) · Ophthalmology · doi:10.1016/s0161-6420(03)00475-5 · Cited by 3,786 · see citing works
Diabetic nephropathy: diagnosis, prevention, and treatment
Gross, J. L., de Azevedo, M. J., Silveiro, S. P., Canani, L. H., Caramori, M. L., & Zelmanovitz, T. (2005) · Diabetes Care · doi:10.2337/diacare.28.1.164 · Cited by 1,839 · see citing works
DUNN, J. F., NISULA, B. C., & RODBARD, D. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-53-1-58 · Cited by 1,238 · see citing works
Standards of Medical Care in Diabetes—2007
American Diabetes Association (2007) · Diabetes Care · doi:10.2337/dc07-s004 · Cited by 1,190 · see citing works
Diabetes-Related Microvascular and Macrovascular Diseases in the Physical Therapy Setting
Cade, W. T. (2008) · Physical Therapy · doi:10.2522/ptj.20080008 · Cited by 1,096 · see citing works
Bhasin, S., Cunningham, G. R., Hayes, F. J., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., & Montori, V. M. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2847 · Cited by 965 · see citing works
Laaksonen, D. E., Niskanen, L., Punnonen, K., Nyyssönen, K., Tuomainen, T.-P., Valkonen, V.-P., Salonen, R., & Salonen, J. T. (2004) · Diabetes Care · doi:10.2337/diacare.27.5.1036 · Cited by 920 · see citing works
Validation of a screening questionnaire for androgen deficiency in aging males
Morley, J. E., Charlton, E., Patrick, P., Kaiser, F. E., Cadeau, P., McCready, D., & Perry, H. M. (2000) · Metabolism · doi:10.1053/meta.2000.8625 · Cited by 662 · see citing works
Frequent Occurrence of Hypogonadotropic Hypogonadism in Type 2 Diabetes
Dhindsa, S., Prabhakar, S., Sethi, M., Bandyopadhyay, A., Chaudhuri, A., & Dandona, P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0804 · Cited by 631 · see citing works
Oh, J.-Y., Barrett-Connor, E., Wedick, N. M., & Wingard, D. L. (2002) · Diabetes Care · doi:10.2337/diacare.25.1.55 · Cited by 594 · see citing works
Low testosterone levels are common and associated with insulin resistance in men with diabetes
Grossmann, M., Thomas, M. C., Panagiotopoulos, S., Sharpe, K., MacIsaac, R. J., Clarke, S., Zajac, J. D., & Jerums, G. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2177 · Cited by 468 · see citing works
Testosterone concentrations in diabetic and nondiabetic obese men
Dhindsa, S., Miller, M. G., McWhirter, C. L., Mager, D. E., Ghanim, H., Chaudhuri, A., & Dandona, P. (2010) · Diabetes Care · doi:10.2337/dc09-1649 · Cited by 352 · see citing works
Update: 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
Tenover, J. L., Matsumoto, A. M., Plymate, S. R., & Bremner, W. J. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-6-1118 · Cited by 256 · see citing works
An increase in prevalence of diabetes mellitus in Jordan over 10 years
Ajlouni, K. M., Khader, Y. S., Batieha, A. M., Ajlouni, H., & El-Khateeb, M. S. (2008) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2007.01.004 · Cited by 249 · see citing works
Self-citationLaaksonen, 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
A practical guide to male hypogonadism in the primary care setting
Dandona, P., & Rosenberg, M. T. (2010) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2010.02355.x · Cited by 225 · see citing works
The impact of cigarette smoking on human semen parameters and hormones
Trummer, H., Habermann, H., Haas, J. G., & Pummer, K. (2002) · Human Reproduction · doi:10.1093/humrep/17.6.1554 · Cited by 202 · see citing works
Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro.
Barbieri, R. L., Gochberg, J., & Ryan, K. J. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112494 · Cited by 197 · see citing works
Corona, G., Mannucci, E., Petrone, L., Ricca, V, Balercia, G., Mansani, R., Chiarini, V, Giommi, R., Forti, G., & Maggi, M. (2006) · International Journal of Impotence Research · doi:10.1038/sj.ijir.3901391 · Cited by 189 · 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
Saboor Aftab, S. A., Kumar, S., & Barber, T. M. (2013) · Clinical Endocrinology · doi:10.1111/cen.12092 · Cited by 157 · see citing works
Kim, S., Kwon, H., Park, J., Cho, B., Kim, D., Oh, S., Lee, C. M., & Choi, H.-C. (2012) · BMC Gastroenterology · doi:10.1186/1471-230x-12-69 · Cited by 153 · see citing works
Testosterone Concentration in Young Patients With Diabetes
Chandel, A., Dhindsa, S., Topiwala, S., Chaudhuri, A., & Dandona, P. (2008) · Diabetes Care · doi:10.2337/dc08-0851 · Cited by 146 · see citing works
Sex Hormone Changes in Morbidly Obese Patients after Vertical Banded Gastroplasty
Bastounis, E., Karayiannakis, A. J., Syrigos, K., Zbar, A. P., Makri, G. G., & Alexiou, D. (1998) · European Surgical Research · doi:10.1159/000008556 · Cited by 133 · see citing works
Obesity, low testosterone levels and erectile dysfunction
Diaz‐Arjonilla, M., Schwarcz, M. G., Swerdloff, R. S., & Wang, C. (2008) · International Journal of Impotence Research · doi:10.1038/ijir.2008.42 · Cited by 131 · see citing works
George, J. T., Veldhuis, J. D., Tena‐Sempere, M., Millar, R. P., & Anderson, R. A. (2012) · Clinical Endocrinology · doi:10.1111/cen.12103 · Cited by 123 · see citing works
Relationships in men of sex hormones, insulin, adiposity, and risk factors for myocardial infarction
Phillips, G. B., Jing, T.-Y., & Heymsfield, S. B. (2003) · Metabolism · doi:10.1016/s0026-0495(03)00072-6 · Cited by 118 · see citing works
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
Betancourt-Albrecht, M., & Cunningham, G. R. (2003) · International Journal of Impotence Research · doi:10.1038/sj.ijir.3901031 · Cited by 102 · see citing works
Diabetes mellitus is associated with subnormal serum levels of free testosterone in men
Rhoden, E. L., Ribeiro, E. P., Teloken, C., & Souto, C. A. V. (2005) · BJU International · doi:10.1111/j.1464-410x.2005.05728.x · Cited by 100 · see citing works
Prevalence of Androgen Deficiency in Men with Erectile Dysfunction
Köhler, T., Kim, J., Feia, K., Bodie, J., Johnson, N., Makhlouf, A. A., & Monga, M. (2008) · Urology · doi:10.1016/j.urology.2007.11.073 · Cited by 88 · see citing works
Androgen plasma levels in male diabetics
Andò, S., Rubens, R., & Rottiers, R. (1984) · Journal of Endocrinological Investigation · doi:10.1007/bf03348370 · Cited by 82 · see citing works
Low Serum Testosterone Concentration in Middle-aged Men with Type 2 Diabetes
Fukui, M., Soh, J., Tanaka, M., Kitagawa, Y., Hasegawa, G., Yoshikawa, T., Miki, T., & Nakamura, N. (2007) · Endocrine Journal · doi:10.1507/endocrj.k07-077 · Cited by 73 · see citing works
Shores, M. M., Moceri, V. M., Gruenewald, D. A., Brodkin, K. I., Matsumoto, A. M., & Kivlahan, D. R. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52562.x · Cited by 68 · see citing works
The SUBITO-DE study: sexual dysfunction in newly diagnosed type 2 diabetes male patients.
Corona, G., Giorda, C. B., Cucinotta, D., Guida, P., & Nada, E. (2013) · PubMed · doi:10.3275/8969 · Cited by 55 · see citing works
Stanworth, R. D., Kapoor, D., Channer, K. S., & Jones, T. H. (2011) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2011.03969.x · Cited by 50 · see citing works
Prevalence of and risk factors for androgen deficiency in middle-aged men in Hong Kong
Wong, S. Y. S., Chan, D. C. C., Hong, A. W. L., & Woo, J. (2006) · Metabolism · doi:10.1016/j.metabol.2006.06.019 · Cited by 49 · see citing works
Testosterone in older men after the Institute of Medicine Report: where do we go from here?
Harman, S. M. (2005) · Climacteric · doi:10.1080/13697130500118001 · Cited by 46 · see citing works
Testosterone, SHBG and risk of type 2 diabetes in the second evaluation of the Pizarra cohort study
Soriguer, F., Rubio‐Martín, E., Fernández, D., Valdés, S., García‐Escobar, E., Martín‐Núñez, G. M., Esteva, I., Almaraz, M. C., & Rojo‐Martínez, G. (2011) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2011.02559.x · Cited by 43 · see citing works
Ali, S. T., Shaikh, R. N., Ashfaqsiddiqi, N., et al. (1993) · Archives of Andrology · doi:10.3109/01485019308987744 · Cited by 41 · see citing works
Prevalence of Hypogonadism in Patients with Type 2 Diabetes Mellitus in an Asian Indian Study Group
Ganesh, H. K., Sarathi, V., George, J., Shivane, V. K., Bandgar, T., Menon, P. S., & Shah, N. S. (2009) · Endocrine Practice · doi:10.4158/ep09035.orr · Cited by 38 · see citing works
Hypogonadotrophic hypogonadism in type 2 diabetes
Dandona, P., Dhindsa, S., Chaudhuri, A., Bhatia, V., & Topiwala, S. (2008) · The Aging Male · doi:10.1080/13685530802317934 · Cited by 38 · see citing works
Serum testosterone levels in diabetic men with and without erectile dysfunction
Ghazi, S., Zohdy, W., Elkhiat, Y., & Shamloul, R. M. (2012) · Andrologia · doi:10.1111/j.1439-0272.2012.01292.x · Cited by 37 · see citing works
Tripathy, D., Dhindsa, S., Garg, R., Khaishagi, A., Syed, T., & Dandona, P. (2003) · Metabolic Syndrome and Related Disorders · doi:10.1089/154041903321648270 · Cited by 34 · see citing works
Fukui, M., Tanaka, M., Hasegawa, G., Yoshikawa, T., & Nakamura, N. (2008) · Diabetes Care · doi:10.2337/dc07-1898 · Cited by 33 · see citing works
Hypogonadism, Erectile Dysfunction, and Type 2 Diabetes Mellitus: What the Clinician Needs to Know
Tamler, R., & Deveney, T. K. (2010) · Postgraduate Medicine · doi:10.3810/pgm.2010.11.2234 · Cited by 31 · see citing works
Zhang, X., Liu, Z., Hu, X.-W., et al. (2012) · PubMed · Cited by 24 · see citing works
Rezvani, M. R., Saadatjou, S. A. R., Sorouri, S., & Fard, M. H. (2012) · PubMed · Cited by 15 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- [2]Chan JC Malik V Jia W Kadowaki T Yajnik CS Yoon KH Diabetes in Asia: Epidemiology, risk factors, and pathophysiology JAMA 2009 30 2129 40 19470990
- [16]Kapoor D Aldred H Clark S Channer KS Jones TH Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: Correlations with bioavailable testosterone and visceral adiposity Diabetes Care 2007 30 911 7 17392552
- [27]Boulton AJ Vinik AI Arezzo JC Bril V Feldman EL Freeman R Diabetic neuropathies: A statement by the American Diabetes Association Diabetes Care 2005 28 956 62 15793206
- [30]Ogbera AO Relationship between serum testosterone levels and features of the metabolic syndrome defining criteria in patients with type 2 diabetes mellitus West Afr J Med 2011 30 277 81 22669833
- [42]UK Prospective Diabetes Study (UKPDS) VIII. Study design, progress and performance Diabetologia 1991 34 877 90 1778353
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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
Evaluation and Management of Testosterone Deficiency: AUA Guideline
Mulhall, J. P., Trost, L. W., Brannigan, R. E., Kurtz, E. G., Redmon, J. B., Chiles, K. A., Lightner, D. J., Miner, M. M., Murad, M. H., Nelson, C. J., et al. (2018) · Journal of Urology · doi:10.1016/j.juro.2018.03.115 · Cited by 766 · see citing works
- Authors
- Al Hayek, A., Khader, Y., Jafal, S., Khawaja, N., Robert, A., & Ajlouni, K.
- Affiliations
- National Center for Diabetes, Endocrinology and Genetic Diseases (JO)
- Venue
- Journal of Family and Community Medicine
- Published
- 2013
- Volume
- 20
- Issue
- 3
- Pages
- 179
- ISSN
- 1319-1683 (ISSN-L)
- 2230-8229
- PMC
- PMC3957172
- OpenAlex
- W2025989795
- Cited by
- 94
- References
- 49
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 8 · 2023: 3 · 2022: 9 · 2021: 9 · 2020: 5 · 2019: 11 · 2018: 10 · 2017: 9 · 2016: 12 · 2015: 7 · 2014: 1
- FWCI
- 5.25
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- Journal of Family and Community Medicine (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- 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 › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- androgen deficiency, type 2 diabetes, hypogonadism, prevalence, risk factors, diabetic neuropathy, body mass index, age, income, smoking, diabetic nephropathy, sex hormone-binding globulin
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