Sex Differences of Endogenous Sex Hormones and Risk of Type 2 Diabetes: A Systematic Review and Meta-analysis
Abstract
CONTEXT: Inconsistent data suggest that endogenous sex hormones may have a role in sex-dependent etiologies of type 2 diabetes, such that hyperandrogenism may increase risk in women while decreasing risk in men. OBJECTIVE: To systematically assess studies evaluating the association of plasma levels of testosterone, sex hormone-binding globulin (SHBG), and estradiol with risk of type 2 diabetes. DATA SOURCES: Systematic search of EMBASE and MEDLINE (1966-June 2005) for English-language articles using the keywords diabetes, testosterone, sex-hormone-binding-globulin, and estradiol; references of retrieved articles; and direct author contact. STUDY SELECTION: From 80 retrieved articles, 43 prospective and cross-sectional studies were identified, comprising 6974 women and 6427 men and presenting relative risks (RRs) or hormone levels for cases and controls. DATA EXTRACTION: Information on study design, participant characteristics, hormone levels, and risk estimates were independently extracted by 2 investigators using a standardized protocol. DATA SYNTHESIS: Results were pooled using random effects and meta-regressions. Cross-sectional studies indicated that testosterone level was significantly lower in men with type 2 diabetes (mean difference, -76.6 ng/dL; 95% confidence interval [CI], -99.4 to -53.6) and higher in women with type 2 diabetes compared with controls (mean difference, 6.1 ng/dL; 95% CI, 2.3 to 10.1) (P<.001 for sex difference). Similarly, prospective studies showed that men with higher testosterone levels (range, 449.6-605.2 ng/dL) had a 42% lower risk of type 2 diabetes (RR, 0.58; 95% CI, 0.39 to 0.87), while there was suggestion that testosterone increased risk in women (P = .06 for sex difference). Cross-sectional and prospective studies both found that SHBG was more protective in women than in men (P< or =.01 for sex difference for both), with prospective studies indicating that women with higher SHBG levels (>60 vs < or =60 nmol/L) had an 80% lower risk of type 2 diabetes (RR, 0.20; 95% CI, 0.12 to 0.30), while men with higher SHBG levels (>28.3 vs < or =28.3 nmol/L) had a 52% lower risk (RR, 0.48; 95% CI, 0.33 to 0.69). Estradiol levels were elevated among men and postmenopausal women with diabetes compared with controls (P = .007). CONCLUSIONS: This systematic review indicates that endogenous sex hormones may differentially modulate glycemic status and risk of type 2 diabetes in men and women. High testosterone levels are associated with higher risk of type 2 diabetes in women but with lower risk in men; the inverse association of SHBG with risk was stronger in women than in men.
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Low levels of endogenous SHBG have been linked with poor glucose tolerance.
“low levels of endogenous SHBG have been linked with poor glucose tolerance [62], [63]”
From Impact of Five Nights of Sleep Restriction on Glucose Metabolism, Leptin and Testosterone in Young Adult Men (2012) · cites this paper as [63]
Higher SHBG levels are associated with reduced risk of type 2 diabetes.
“higher levels associated with reduced risk of type 2 diabetes [63], [64].”
From Impact of Five Nights of Sleep Restriction on Glucose Metabolism, Leptin and Testosterone in Young Adult Men (2012) · cites this paper as [63]
The association between SHBG and T2D holds after adjusting for BMI and other common risk factors, implying lower SHBG as a predictor for T2D is at least partially independent of BMI.
“Importantly, the association between SHBG and T2D also holds after adjusting for BMI and other common risk factors, implying lower SHBG as a predictor for T2D is at least partially independent of BMI [118, 121, 124].”
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 [118]
Lower SHBG was an independent risk factor for the development of T2D, inferring a five- or ninefold higher risk for male and female subjects, respectively, as compared to the reference group.
“In a large longitudinal cohort study, lower SHBG was an independent risk factor for the development of T2D, inferring a five- or ninefold higher risk for male and female subjects, respectively, as compared to the reference group, hereby confirming findings from smaller studies [117–119].”
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 [118]
Sex steroid hormone concentrations have been associated with health conditions in men, including prostate cancer, diabetes, low bone mineral density, lower urinary tract symptoms, impaired cognitive function, and cardiovascular disease.
“Sex steroid hormone concentrations have been previously shown to be associated with health conditions in men, including prostate cancer [1], diabetes [2, 3], low bone mineral density [4], lower urinary tract symptoms [5], impaired cognitive function [6, 7] and cardiovascular disease [8–10].”
From Association of cigarette smoking, alcohol consumption, and physical activity with sex steroid hormone levels in US men (2009) · cites this paper as [3]
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- Authors
- Ding, E. L., Song, Y., Malik, V. S., & Liu, S.
- Affiliations
- Brigham and Women's Hospital (US)
- American Medical Association (US)
- University of California, Los Angeles (US)
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2006-03-15
- Volume
- 295
- Issue
- 11
- Pages
- 1288
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- OpenAlex
- W2028647952
- Cited by
- 1,354
- References
- 23
- Citations by year
- 2026: 36 · 2025: 51 · 2024: 64 · 2023: 58 · 2022: 71 · 2021: 62 · 2020: 65 · 2019: 66 · 2018: 61 · 2017: 91 · 2016: 82 · 2015: 76 · 2014: 68 · 2013: 83 · 2012: 90
- FWCI
- 38.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA009001-29)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK066401-02, R01DK066401)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Keywords
- type 2 diabetes, sex differences, testosterone, sex hormone-binding globulin, estradiol, endogenous sex hormones, hyperandrogenism, diabetes risk, women's health
- MeSH terms
- Diabetes Mellitus, Type 2, Estradiol, Female, Humans, Male, Risk Factors, Sex Characteristics, Sex Hormone-Binding Globulin, Gonadal Steroid Hormones, Testosterone
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