Cited by 151Hormonal and reproductive studiesDiabetes, Cardiovascular Risks, and LipoproteinsSperm and Testicular Function

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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

Vikan, Torkel, Schirmer, Henrik, Njølstad, Inger, Svartberg, Johan·2010·European Journal of Endocrinology

DOI 10.1530/eje-09-0943

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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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“Based on previous studies, we hypothesized that higher levels of these androgens would be associated with less insulin resistance and lower risk of diabetes (13) (14) (15) (16).”
Cardiovascular risk and testosterone – from subclinical atherosclerosis to lipoprotein function to heart failure
Gencer, B., Bonomi, M., Adorni, M. P., Sirtori, C. R., Mach, F., & Ruscica, M. (2021) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09628-2 · Cited by 58
“…[93] 794 11.8 73.6 HR 1.38 (1.02-1.85) Haring (2010) [156] 1954 7.2 58.7 RR 4.93 (1.21-20.26) Menke (2010) [157] 1114 8 40 RR 1.24 (0.85-1.78) Vikan (2010) [158] 1568 11.2 59.6 RR 1.09 (0.74-1.63) Haring (2012) [156] 2039 5.5 20-79 RR 2.05 (1.61-2.60)b Pye (2014) [159] 2599 4.3 40-79 RR 2.30…”
Influential
Androgen Deprivation Therapy, Hypogonadism and Cardiovascular Toxicity in Men with Advanced Prostate Cancer
Gheorghe, G. S., Hodorogea, A. S., Ciobanu, A., Nanea, I. T., & Gheorghe, A. C. D. (2021) · Current Oncology · doi:10.3390/curroncol28050289 · Cited by 44
Serum sex hormone-binding globulin and testosterone in relation to cardiovascular disease risk factors in young men: a population-based study
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Role of sex hormones in diabetic nephropathy
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Type 2 Diabetes and Testosterone Therapy
Hackett, G. I. (2018) · The World Journal of Men s Health · doi:10.5534/wjmh.180027 · Cited by 39
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Background
Sex steroids and glucose metabolism
Allan, C. A. (2014) · Asian Journal of Andrology · doi:10.4103/1008-682x.122589 · Cited by 38
Relation between Sex Hormone Concentrations, Peripheral Arterial Disease, and Change in Ankle-Brachial Index: Findings from the Framingham Heart Study
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“spective investigations have shown that low total testosterone (TT) concentrations in men were associated with a less favorable cardiovascular risk profile including obesity (6), incident metabolic syndrome (7), diabetes mellitus (8), dyslipidemia (9), hypertension (10), and mortality (11).”
Background
Epigenetic modification in diabetic kidney disease
Liu, Z., Liu, J., Wang, W., An, X., Luo, L., Yu, D., & Sun, W. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1133970 · Cited by 38
Circulating Estrone Levels Are Associated Prospectively With Diabetes Risk in Men of the Framingham Heart Study
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“Cardiovascular disease 258 (18) 123 (12)”
Result
Insulin resistance and sex hormone-binding globulin are independently correlated with low free testosterone levels in obese males
Souteiro, P., Belo, S., Oliveira, S. C., Neves, J. S., Magalhães, D. M. D. S., Pedro, J. M. P., Bettencourt‐Silva, R., Costa, M. M., Varela, A. T. I. F., Queirós, J., et al. (2018) · Andrologia · doi:10.1111/and.13035 · Cited by 31
Middle-Aged Diabetic Females and Males Present Distinct Susceptibility to Alzheimer Disease-like Pathology
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Single-nucleotide polymorphism, rs1799941 in the Sex Hormone-Binding Globulin (SHBG) gene, related to both serum testosterone and SHBG levels and the risk of myocardial infarction, type 2 diabetes, cancer and mortality in men: the Tromsø Study
Svartberg, J., Schirmer, H., Wilsgaard, T., Mathiesen, E. B., Njølstad, I., Løchen, M.-L., & Jorde, R. (2014) · Andrology · doi:10.1111/j.2047-2927.2013.00174.x · Cited by 32
“…levels tends to predict the development of metabolic syndrome and type 2 diabetes mellitus (T2DM) (Oh et al., 2002; Laaksonen et al., 2004; Vikan et al., 2010) and have been associated with both all-cause mortality and cardiovascular disease (CVD) mortality (Vikan et al., 2009a; Araujo…”
BackgroundSelf-citation
Effects of glucagon‐like peptide 1 receptor agonists on testicular dysfunction: A systematic review and meta‐analysis
Salvio, G., Ciarloni, A., Ambo, N., Bordoni, M., Perrone, M., Rossi, S., & Balercia, G. (2025) · Andrology · doi:10.1111/andr.70022 · Cited by 35
Classic and Novel Sex Hormone Binding Globulin Effects on the Cardiovascular System in Men
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“Although reduced levels of circulating SHBG decrease total testosterone levels, the effect of low testosterone on SHBG expression is not fully understood [105].”
Background
Sex hormones and the risk of type 2 diabetes mellitus: A 9‐year follow up among elderly men in F inland
Salminen, M. J., Vahlberg, T. J., Räihä, I. J., NISKANEN, L. K., Kivelä, S., & Irjala, K. M. A. (2014) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/ggi.12312 · Cited by 30
Metabolic Effects of Testosterone Therapy in Men with Type 2 Diabetes and Metabolic Syndrome
Hackett, G. I. (2019) · Sexual Medicine Reviews · doi:10.1016/j.sxmr.2018.12.004 · Cited by 39
Stable Intraprostatic Dihydrotestosterone in Healthy Medically Castrate Men Treated With Exogenous Testosterone
Thirumalai, A., Cooper, L. A., Rubinow, K. B., Amory, J. K., Lin, D. W., Wright, J. L., Marck, B. T., Matsumoto, A. M., & Page, S. T. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-1483 · Cited by 27
Androgens for postmenopausal women’s health?
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“A study, however, found that the risk ofT2DM associated with testosterone, as well as, to estradiol and SHBG levels, was not independent of the body mass index or the waist circumference [65].”
The Role of Estrogens and Vitamin D in Cardiomyocyte Protection: A Female Perspective
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Role of sex steroids, intrahepatic fat and liver enzymes in the association between SHBG and metabolic features
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Clinical correlates of sex hormones in women: The study of health in Pomerania
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Androgen receptor CAG repeat length polymorphism modifies the impact of testosterone on insulin sensitivity in men
Möhlig, M., Arafat, A. M., Osterhoff, M. A., Isken, F., Weickert, M. O., Spranger, J., Pfeiffer, A. F. H., & Schöfl, C. (2011) · European Journal of Endocrinology · doi:10.1530/eje-10-1022 · Cited by 29
Inhibition of estradiol synthesis attenuates renal injury in male streptozotocin-induced diabetic rats
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Testosterone Levels and Quality of Life in Diverse Male Patients With Cancers Unrelated to Androgens
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Association of glyphosate exposure with multiple adverse outcomes and potential mediators.
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Haring, R., Xanthakis, V., Coviello, A., Sullivan, L., Bhasin, S., Wallaschofski, H., Murabito, J. M., & Vasan, R. S. (2012) · International Journal of Andrology · doi:10.1111/j.1365-2605.2012.01285.x · Cited by 22
“, 2009) or type 2 diabetes (Vikan et al., 2010; Schipf et al., 2011), whereas these conditions are also associated with decreased TT concentrations (Laaksonen et al.”
Influential
The Evaluation of Serum Levels of Testosterone in Type 2 Diabetic Men and Its Relation with Lipid Profile
Mattack, N. (2015) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2015/11049.5381 · Cited by 21
An overview of the contribution of fatness and fitness factors, and the role of exercise, in the formation of health status for individuals who are overweight
Clark, J. E. (2012) · Journal of Diabetes & Metabolic Disorders · doi:10.1186/2251-6581-11-19 · Cited by 19
“Testosterone/Adrenal Androgens [72-82] Testes Adrenal Cortex Skeletal Muscle (hypertrophy, add contractile tissue)”
Background
Genome-wide association studies on serum sex steroid levels
Vandenput, L., & Ohlsson, C. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.03.009 · Cited by 19
“…common disorders such as the metabolic syndrome (Haring et al., 2009; Kupelian et al., 2006), hypertension (Torkler et al., 2011), type 2 diabetes (Vikan et al., 2010), osteoporosis (Fink et al., 2006; Meier et al., 2008), sarcopenia (Cawthon et al., 2009), cardiovascular disease (Ohlsson et al.,…”
Background
Comparison of serum free testosterone, luteinizing hormone and follicle stimulating hormone levels in diabetics and non-diabetics men- a case-control study.
Rezvani, M., Saadatjou, S. A., Sorouri, S., & Fard, M. H. (2012) · Journal of research in health sciences · doi:10.34172/jrhs12730 · Cited by 19
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Immunological and mass spectrometric assays of SHBG: consistent and inconsistent metabolic associations in healthy men.
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“In contrast to women, increased estradiol levels in men are associated with increased risk of developing DM2 [131].”
Background
Marked Increase in Incident Gynecomastia: A 20-Year National Registry Study, 1998 to 2017
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Low Sex Hormone-Binding Globulin Levels Associate with Prediabetes in Chinese Men Independent of Total Testosterone
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“Previous study also showed that it was not serum TT but SHBG was the most powerful predictor of T2DM in men, which predicted T2DM independently of TT [27, 31].”
BackgroundResult
Combined inhibition of aromatase activity and dihydrotestosterone supplementation attenuates renal injury in male streptozotocin (STZ)-induced diabetic rats
Manigrasso, M. B., Sawyer, R. T., Hutchens, Z. M., Flynn, E. R., & Maric‐Bilkan, C. (2012) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00569.2011 · Cited by 15
“Men with type 1 and type 2 diabetes, as well as experimental models of diabetes, exhibit decreased circulating testosterone (9, 12–13, 18, 39, 42, 44) and increased circulating estradiol levels (42, 44).”
Background
Sex Hormone-Binding Globulin and the Metabolic Syndrome
Hammond, G. L. (2017) · Springer eBooks · doi:10.1007/978-3-319-53298-1_15 · Cited by 13
Male Reproduction and Aging
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Perspectives for metabolomics in testosterone replacement therapy
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Diabetes surpasses obesity as a risk factor for low serum testosterone level
Khalil, S. H. A., Dandona, P., Osman, N. A., Assaad, R. S., Zaitoon, B. T. A., Almas, A. A., & Amin, N. G. (2024) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-024-01373-1 · Cited by 11
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Putative causal inference for the relationship between obesity and sex hormones in males: a bidirectional Mendelian randomization study
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Mediated relationships between multiple metals exposure and fasting blood glucose by reproductive hormones in Chinese men.
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Sex Differences in Exercise Performance and Exercise Training Among Persons with Type 2 Diabetes
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The Role of Steroidomics in the Diagnosis of Alzheimer’s Disease and Type 2 Diabetes Mellitus
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“Literature data on the relationship of estradiol and estrone levels to T2DM are discrepant [58,88,92,93] (also see the review in [43]).”
Background
Update on Testosterone Replacement Therapy in Hypogonadal Men
Leung, K. M. Y. B., Alrabeeah, K. A., & Carrier, S. (2015) · Current Urology Reports · doi:10.1007/s11934-015-0523-9 · Cited by 6

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
ORCID: Schirmer, Henrik
Njølstad, Inger
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
DOI: 10.1530/eje-09-0943
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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Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men

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