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      Can Low SHBG Serum Concentration Be A Good Early Marker Of Male Hypogonadism In Metabolic Syndrome?

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          Abstract

          Introduction

          In men suffering from metabolic syndrome, accompanying insulin resistance may result in a lowering of sex hormone–binding globulin (SHBG) plasma levels and cause changes in their androgenic status.

          Aim

          The objective of the research was to assess selected androgens and SHBG plasma levels in males meeting diagnostic criteria for MS compared to healthy males.

          Patients and methods

          The group consisted of 65 men aged between 40 and 70 years old fitting IDF metabolic syndrome criteria and 84 controls. Dehydroepiandrosterone (DHEA) and its sulphate (DHEA–S), total and free testosterone and SHBG serum levels were evaluated. Calculated free and bioavailable testosterone were estimated using an algorithm proposed by the International Society for the Study of the Aging Male.

          Results

          Men diagnosed with MS showed a statistically significant decrease in plasma levels of DHEA in comparison to healthy ones: 11.579 (8.39–15.56) vs 14.014 (9.611–17.125) ng/mL; p = 0.0350, SHBG: 47.46 (35.78–62.83) vs 71.965 (54.45–91.56) nM/L; p<0.0001 and total testosterone: 5.2 (3.8–6.5) vs 6.3 (5.4–8.25) ng/mL; p = 0.0001 (values presented as a median with Q1–Q3).

          Conclusion

          The results suggest that SHBG is a good early marker for metabolic dysregulation in MS, considering its strength of association and significance is comparable to, or better than, those of MS criteria.

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          Most cited references54

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          Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study.

          Carol A Derby, John B. McKinlay, William J Bremner … (2002)
          We used longitudinal data from the Massachusetts Male Aging Study, a large population-based random-sample cohort of men aged 40-70 yr at baseline, to establish normative age trends for serum level of T and related hormones in middle-aged men and to test whether general health status affected the age trends. Of 1,709 men enrolled in 1987-1989, 1,156 were followed up 7-10 yr afterward. By repeated-measures statistical analysis, we estimated simultaneously the cross-sectional age trend of each hormone between subjects within the baseline data, the cross-sectional trend between subjects within the follow-up data, and the longitudinal trend within subjects between baseline and follow-up. Total T declined cross-sectionally at 0.8%/yr of age within the follow-up data, whereas both free and albumin-bound T declined at about 2%/yr, all significantly more steeply than within the baseline data. Sex hormone-binding globulin increased cross-sectionally at 1.6%/yr in the follow-up data, similarly to baseline. The longitudinal decline within subjects between baseline and follow-up was considerably steeper than the cross-sectional trend within measurement times for total T (1.6%/yr) and bioavailable T (2-3%/yr). Dehydroepiandrosterone, dehydroepiandrosterone sulfate, cortisol, and estrone showed significant longitudinal declines, whereas dihydrotestosterone, pituitary gonadotropins, and PRL rose longitudinally. Apparent good health, defined as absence of chronic illness, prescription medication, obesity, or excessive drinking, added 10-15% to the level of several androgens and attenuated the cross-sectional trends in T and LH but did not otherwise affect longitudinal or cross-sectional trends. The paradoxical finding that longitudinal age trends were steeper than cross-sectional trends suggests that incident poor health may accelerate the age-related decline in androgen levels.
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            Sex hormone-binding globulin and risk of type 2 diabetes in women and men.

            Eric Ding, Yiqing Song, JoAnn Manson … (2009)
            Circulating sex hormone-binding globulin levels are inversely associated with insulin resistance, but whether these levels can predict the risk of developing type 2 diabetes is uncertain. We performed a nested case-control study of postmenopausal women in the Women's Health Study who were not using hormone therapy (359 with newly diagnosed type 2 diabetes and 359 controls). Plasma levels of sex hormone-binding globulin were measured; two polymorphisms of the gene encoding sex hormone-binding globulin, SHBG, that were robustly associated with the protein levels were genotyped and applied in mendelian randomization analyses. We then conducted a replication study in an independent cohort of men from the Physicians' Health Study II (170 with newly diagnosed type 2 diabetes and 170 controls). Among women, higher plasma levels of sex hormone-binding globulin were prospectively associated with a lower risk of type 2 diabetes: multivariable odds ratios were 1.00 for the first (lowest) quartile of plasma levels, 0.16 (95% confidence interval [CI], 0.08 to 0.33) for the second quartile, 0.04 (95% CI, 0.01 to 0.12) for the third quartile, and 0.09 (95% CI, 0.03 to 0.21) for the fourth (highest) quartile (P<0.001 for trend). These prospective associations were replicated among men (odds ratio for the highest quartile of plasma levels vs. the lowest quartile, 0.10; 95% CI, 0.03 to 0.36; P<0.001 for trend). As compared with homozygotes of the respective wild-type allele, carriers of a variant allele of the SHBG single-nucleotide polymorphism (SNP) rs6259 had 10% higher sex hormone-binding globulin levels (P=0.005), and carriers of an rs6257 variant had 10% lower plasma levels (P=0.004); variants of both SNPs were also associated with a risk of type 2 diabetes in directions corresponding to their associated sex hormone-binding globulin levels. In mendelian randomization analyses, the predicted odds ratio of type 2 diabetes per standard-deviation increase in the plasma level of sex hormone-binding globulin was 0.28 (95% CI, 0.13 to 0.58) among women and 0.29 (95% CI, 0.15 to 0.58) among men, a finding that suggests that sex hormone-binding globulin may have a causal role in the risk of type 2 diabetes. Low circulating levels of sex hormone-binding globulin are a strong predictor of the risk of type 2 diabetes in women and men. The clinical usefulness of both SHBG genotypes and plasma levels in stratification and intervention for the risk of type 2 diabetes warrants further examination. 2009 Massachusetts Medical Society
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              Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men.

              David Laaksonen, Leo Niskanen, Kari Punnonen … (2004)
              In men, hypoandrogenism is associated with features of the metabolic syndrome, but the role of sex hormones in the pathogenesis of the metabolic syndrome and diabetes is not well understood. We assessed the association of low levels of testosterone and sex hormone-binding globulin (SHBG) with the development of the metabolic syndrome and diabetes in men. Concentrations of SHBG and total and calculated free testosterone and factors related to insulin resistance were determined at baseline in 702 middle-aged Finnish men participating in a population-based cohort study. These men had neither diabetes nor the metabolic syndrome. After 11 years of follow-up, 147 men had developed the metabolic syndrome (National Cholesterol Education Program criteria) and 57 men diabetes. Men with total testosterone, calculated free testosterone, and SHBG levels in the lower fourth had a severalfold increased risk of developing the metabolic syndrome (odds ratio [OR] 2.3, 95% CI 1.5-3.4; 1.7, 1.2-2.5; and 2.8, 1.9-4.1, respectively) and diabetes (2.3, 1.3-4.1; 1.7, 0.9-3.0; and 4.3, 2.4-7.7, respectively) after adjustment for age. Adjustment for potential confounders such as cardiovascular disease, smoking, alcohol intake, and socioeconomic status did not alter the associations. Factors related to insulin resistance attenuated the associations, but they remained significant, except for free testosterone. Low total testosterone and SHBG levels independently predict development of the metabolic syndrome and diabetes in middle-aged men. Thus, hypoandrogenism is an early marker for disturbances in insulin and glucose metabolism that may progress to the metabolic syndrome or frank diabetes and may contribute to their pathogenesis.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Diabetes Metab Syndr Obes
                Journal ID (iso-abbrev): Diabetes Metab Syndr Obes
                Journal ID (publisher-id): DMSO
                Journal ID (pmc): dmso
                Title: Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy
                Publisher: Dove
                ISSN (Electronic): 1178-7007
                Publication date (Electronic): 21 October 2019
                Publication date Collection: 2019
                Volume: 12
                Pages: 2181-2191
                Affiliations
                [1 ]Student Scientific Club of Endocrinology, Poznan University of Medical Sciences , Poznań, Wielkopolskie, Poland
                [2 ]Outpatients Clinic of Endocrine Diseases , Wschowa, Lubuskie, Poland
                [3 ]Department of Nephrology, Transplantology and Internal Medicine, Poznan University of Medical Sciences , Poznań, Wielkopolskie, Poland
                [4 ]Department of Endocrinology, Metabolism and Internal Medicine, Poznań University of Medical Sciences , Poznań, Wielkopolskie, Poland
                Author notes
                Correspondence: Katarzyna Lacka Department of Endocrinology, Metabolism and Internal Medicine, Poznan University of Medical Sciences , Poznań, Przybyszewskiego 4960-834, PolandTel +4861604905086 Email kktlacka@gmail.com
                Author information
                http://orcid.org/0000-0003-1109-2273
                http://orcid.org/0000-0001-5505-3992
                http://orcid.org/0000-0002-0323-1096
                http://orcid.org/0000-0003-2386-4795
                Article
                Publisher ID: 218545
                DOI: 10.2147/DMSO.S218545
                PMC ID: 6814954
                PubMed ID: 31695461
                SO-VID: 6f7c3557-33ef-4a8c-ba4f-259277eae2c1
                Copyright © © 2019 Jarecki et al.
                License:

                This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms ( https://www.dovepress.com/terms.php).

                History
                Date received : 06 June 2019
                Date accepted : 06 August 2019
                Page count
                Figures: 3, Tables: 4, References: 62, Pages: 11
                Funding
                Funded by: not-for-profit sector
                Categories
                Subject: Original Research

                ScienceOpen disciplines: Endocrinology & Diabetes
                Keywords: ms,dhea,testosterone,crp,cholesterol,androgens
                Data availability:
                ScienceOpen disciplines: Endocrinology & Diabetes
                Keywords: ms, dhea, testosterone, crp, cholesterol, androgens

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