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Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men
Abstract
Objective: To study the impact of endogenous sex hormone levels in community-dwelling men on later risk for type 2 diabetes. Design: Population-based prospective cohort study. Methods: For the analyses, 1454 men who participated in the fourth Tromsø study (1994–1995) were used. Cases of diabetes were retrieved and validated until 31.12.05 following a detailed protocol. The prospective association between sex hormones and diabetes was examined using Cox proportional hazard regression analysis, allowing for multivariate adjustments. Results: There was a significantly lowered multi-adjusted risk for later diabetes with higher normal total testosterone levels, both linearly per s.d. increase (hazard ratio (HR) 0.71, confidence interval (CI) 0.54–0.92) and in the higher quartiles of total testosterone than in the lowest quartiles (HR 0.53, CI 0.33–0.84). A reduced multi-adjusted risk for incident diabetes was also found for men with higher sex hormone-binding globulin (SHBG) levels, both linearly per s.d. increase (HR 0.55, CI 0.39–0.79) and when comparing the third (HR 0.38, CI 0.18–0.81) and the fourth quartile (HR 0.37, CI 0.17–0.82) to the lowest quartile. The associations with total testosterone and SHBG were no longer significant after inclusion of waist circumference to the multivariate models. Estradiol (E 2) was positively associated with incident diabetes after multivariate adjustments including waist circumference when comparing the second (HR 0.49, CI 0.26–0.93) and the third (HR 0.51, CI 0.27–0.96) quartile to the highest quartile. Conclusion: Men with higher E 2 levels had an increased risk of later diabetes independent of obesity, while men with lower total testosterone and SHBG had an increased risk of diabetes that appeared to be dependent on obesity.
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“The same inverse association between SHBG and T2D has been confirmed in multiple other studies in both men and women [120–123].”
From Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology (2022) · cites this paper as [123]
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Prevalence of the metabolic syndrome and its relationship with diabetes mellitus by aging
Kawada, T., Otsuka, T., Endo, T., & Kon, Y. (2011) · The Aging Male · doi:10.3109/13685538.2011.565092 · Cited by 7
“Obese men had a greater decline of free and total testosterone and sex hormone binding globulin (SHBG) levels, compared to men who were never classified as obese, and men with low total testosterone and low SHBG have an increased risk of diabetes [21].”
BackgroundMakimura, H., Stanley, T. L., Sun, N., Connelly, J. M., Hemphill, L., & Grinspoon, S. K. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03859.x · Cited by 6
Testosterone Therapy and Glucose Homeostasis in Men with Testosterone Deficiency (Hypogonadism)
Saad, F. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-70178-3_23 · Cited by 6
“Several studies have reported that TD is associated with increased risk of T2DM (Vikan et al. 2010; Salminen et al. 2015; Schipf et al. 2011).”
BackgroundSofer, Y., Nevo, N., Vechoropoulos, M., Shefer, G., Osher, E., Landis, N., Tordjman, K., Hammond, G. L., & Stern, N. (2018) · Endocrine Connections · doi:10.1530/ec-17-0240 · Cited by 6
Mucinski, J. M., Kelley, D. E., Winters, S. J., & Goodpaster, B. H. (2025) · Obesity · doi:10.1002/oby.24269 · Cited by 6
“SHBG is lower in men and women with T2D compared to participants without T2D [5], and this relationship appears to be independent of changes in other sex hormones [18].”
Testosterone therapy in hypogonadal patients and the associated risks of cardiovascular events
Kharaba, Z. J., Buabeid, M. A., Ibrahim, N. A., Jirjees, F., Al-Obaidi, H. J., Kaddaha, A., Khajehkarimoddini, L., & Alfoteih, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110423 · Cited by 10
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Risk factors for late-onset hypogonadism
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“In the fourth Tromsø study, men with lower TT have an increased risk of diabetes (Vikan et al., 2010).”
BackgroundSato, Y., Tajima, A., Katsurayama, M., Nozawa, S., Yoshiike, M., Koh, E., Kanaya, J., Namiki, M., Matsumiya, K., Tsujimura, A., et al. (2017) · Human Reproduction Open · doi:10.1093/hropen/hox002 · Cited by 4
“…levels have been observed to affect health adversely causing diseases, including metabolic syndromes (Kupelian et al., 2006; Haring et al., 2009), type two diabetes (Vikan et al., 2010), cardiovascular diseases (Vikan et al., 2009; Araujo et al., 2011) and carcinogenesis (Sharifi et al., 2005).”
BackgroundSerum High-Sensitivity C-Reactive Protein and Endogenous Sex Hormones in Diabetic Men
Alaaraji, S. F. T. (2016) · Journal of Biotechnology Research Center · doi:10.24126/jobrc.2016.10.1.463 · Cited by 4
“84 insulin resistance, which is an important cause for inducing type 2 diabetes and other abnormalities including hyperglycemia, hypertension, dyslipidemia, or carotid atherosclerosis [7].”
BackgroundEffects and significance of estradiol in men
Tõke, J., Czirják, G., Bezzegh, A., Vásárhelyi, B., Rácz, K., & Patócs, A. (2014) · Orvosi Hetilap · doi:10.1556/oh.2014.29914 · Cited by 4
“Egy későbbi vizsgálat azt is kimutatta, hogy ez a hatás független a tesztoszteron mennyiségétől és a BMI-től [41].”
Meng, Y., Yang, X., Fan, Y., Liu, M. R., Zhou, F., Wang, Q., Lu, Y., Zhu, Y., & Yan, H. (2025) · Translational Vision Science & Technology · doi:10.1167/tvst.14.2.17 · Cited by 2
“10,11 However, data from others suggested that elevating levels of estradiol and testosterone were related with an increased risk of T2DM in postmenopausal women, 3,12 and another study demonstrated that FSH, LH, and estradiol were not correlated with DR in women.”
Vásquez-Tirado, G. A., Guarniz-Salavarria, J. D., Quispe-Castañeda, C. V., Contreras-Cabrera, J. M., Cuadra-Campos, M. D. C., Meregildo-Rodríguez, E. D., Segura-Plasencia, N. M., & Arbayza-Ávalos, Y. K. (2024) · Endocrine · doi:10.1007/s12020-024-04019-4 · Cited by 3
“Only three studies evaluated high FT and the risk of developing T2DM [23, 34, 44], showing that there was no association (OR 1.29; 95% CI 0.25 – 6.78; p = 0.35) without signi fi cant heterogeneity (I 2 : 5”
InfluentialKharaba, Z. J., Buabeid, M. A., & Alfoteih, Y. (2020) · Critical Reviews in Toxicology · doi:10.1080/10408444.2020.1789944 · Cited by 2
The Association of Free Testosterone Levels in Men and Lifestyle Factors and Chronic Disease Status
Cardarelli, R., Singh, M., Meyer, J., Balyakina, E., Perez, O., & King, M. R. (2014) · Journal of Primary Care & Community Health · doi:10.1177/2150131913520234 · Cited by 7
The influence of obesity in patients with prostate cancer - Review of the literature
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Mei, Y., Lyu, Y., Le, J., Li, D., Liu, H., Zhao, Z., & Li, Y. (2022) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3564 · Cited by 2
“Similar conclusions have been reported in animal experiments, emphasising the significance of testosterone in T2DM.5 Male patients in this study had decreased testosterone levels, a finding in accordance with previous research reports.”
BackgroundInfluentialSex hormones and adaptive potential of the circulatory system in men of the European and Asian North
Николаевна, М. И., Типисова, Е. В., Alikina, V. А., & Эдуардовна, Е. А. (2021) · Сибирский научный медицинский журнал · doi:10.18699/ssmj20210412 · Cited by 3
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Tuomisto, A., Pinola, P., Pesonen, P., Franks, P. W., Martikainen, H. K., Tapanainen, J. S., Niinimäki, M. J., & Morin-Papunen, L. C. (2025) · Andrology · doi:10.1111/andr.70122 · Cited by 1
“Nevertheless, the association between AGM and T, whether analyzed in quartiles or as a continuous variable, remained significant independently of WC.”
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Chijioke, O. E. (2024) · International Journal of Innovative Science and Research Technology (IJISRT) · doi:10.38124/ijisrt/ijisrt24nov674
Onisiforou, A., & Zanos, P. (2024) · bioRxiv · doi:10.1101/2024.06.25.600630
“In contrast to women, increased estradiol levels in men are associated with increased risk of developing DM2 (112).”
BackgroundStudy of Acute Coronary Syndrome in Premenopausal Women in Correlation with Sex Hormones
Nanjappa, V., Raveesh, H., Kuldeep, A., S., S., & N., M. C. (2022) · Indian Journal of Cardiovascular Disease in Women · doi:10.25259/mm_ijcdw_485
Pakhomov, S. P., Orlova, V., Verzilina, I., Sukhih, N., Nagorniy, A., & Matrosova, A. (2021) · doi:10.22092/ari.2021.356170.1796
“Sex hormone-binding globulin levels increase free testosterone due to a decrease in estrogen (35).”
BackgroundMi, W., Feng, X., Wang, Z.-Q., Ye, X., Shu, H., Yu, B., & Li, C. (2021) · Research Square · doi:10.21203/rs.3.rs-519946/v1
Balzo, D. D. D., Messina, D. N., Corte, C., Stoizik, J. A. M., Laur, J. D. L., & Elizalde, R. F. P. (2016) · Revista Argentina de Endocrinología y Metabolismo · doi:10.1016/j.raem.2016.07.002
Association between androgen deficiency and metabolic syndrome in men with type 2 diabetes mellitus
Mohieldein, A., Alzohairy, M. A., & Hasan, M. (2014) · International Journal of Biomedical Research · doi:10.7439/ijbr.v5i3.535
Hannemann, A., Friedrich, N., Spielhagen, C., Nauck, M., & Haring, R. (2012) · Journal of Laboratory Medicine · doi:10.1515/jlm-2011-0002
Badreldin, D., Mehanna, M., Elgayar, N., & Swelem, R. (2016) · Egyptian Journal of Obesity Diabetes and Endocrinology · doi:10.4103/2356-8062.200937
Metabolomics for the Individualized Therapy of Androgen Deficiency Syndrome in Male Adults
Haring, R., Budde, K., & Wallaschofski, H. (2012) · Springer eBooks · doi:10.1007/978-1-4614-1689-0_10
Metadata
- Authors
- Vikan, T., Schirmer, H., Njølstad, I., & Svartberg, J.
- Affiliations
- University Hospital of North Norway (NO)
- UiT The Arctic University of Norway (NO)
- Corresponding author
- Vikan, Torkel
- Venue
- European Journal of Endocrinology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-04
- Volume
- 162
- Issue
- 4
- Pages
- 747-754
- ISSN
- 0804-4643 (ISSN-L)
- 1479-683X
- OpenAlex
- W2111837311
- Cited by
- 151
- References
- 43
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 9 · 2022: 6 · 2021: 11 · 2020: 8 · 2019: 6 · 2018: 4 · 2017: 13 · 2016: 14 · 2015: 11 · 2014: 11 · 2013: 9 · 2012: 18
- FWCI
- 11.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Endocrinology (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
- type 2 diabetes, testosterone, sex hormone-binding globulin, estradiol, sex hormones, men, diabetes risk, waist circumference, obesity, Tromsø Study
- MeSH terms
- Blood Pressure, Cholesterol, Diabetes Mellitus, Type 2, Estradiol, Humans, Male, Norway, Prospective Studies, Surveys and Questionnaires, Regression Analysis, Retrospective Studies, Sex Hormone-Binding Globulin, Testosterone, Triglycerides, Cohort Studies, Body Mass Index, Waist Circumference
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