Level of sex hormone-binding globulin is positively correlated with insulin sensitivity in men with type 2 diabetes
Abstract
The level of sex hormone-binding globulin (SHBG) is associated with glucose metabolism in nondiabetic women and men, and the finding of low SHBG levels is suggested to be a predictor of the development of type 2 (noninsulin-dependent) diabetes mellitus. To further assess the relationship between SHBG levels and glucose metabolism, we measured serum concentrations of sex hormones and SHBG in 23 well characterized diabetic men, and studied the relationship between these variables and parameters of glucose and lipid metabolism. Insulin sensitivity was estimated using the hyperinsulinemic euglycemic glucose clamp technique. There was a strong positive correlation between the level of SHBG and the sensitivity to insulin in these individuals (r = 0.74; P < 0.001), which was independent of obesity and abdominal fat accumulation. Controlling for the effect of fasting C-peptide and insulin levels did not change the correlation coefficient significantly. SHBG levels did not correlate with levels of free testosterone (F-T), free estradiol (F-E2), or F-T/F-E2 ratio. F-E2 was positively correlated with levels of diastolic blood pressure and triglycerides (r = 0.44; P < 0.05 and r = 0.62; P < 0.001, respectively). These findings support earlier observations that associate insulin resistance with levels of SHBG, and for the first time demonstrate a direct correlation between sensitivity to insulin and SHBG levels in men with type 2 diabetes.
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Low SHBG is associated with metabolic syndrome and insulin resistance.
“Both low testosterone [38]–[40] and sex hormone binding globulin (SHBG) [41], [42] are associated with metabolic syndrome and insulin resistance.”
From Impact of Five Nights of Sleep Restriction on Glucose Metabolism, Leptin and Testosterone in Young Adult Men (2012) · cites this paper as [42]
SHBG was found to be negatively associated with plasma glucose, insulin levels and IR.
“In addition, SHBG was also found to be negatively associated with plasma glucose, insulin levels and IR [125–127].”
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 [127]
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“The figures of mean and variation in our study are within the same range as in previously published studies in large populations [33-37], except for one Finnish study of 54-year-old men, who seemed to exhibit slightly lower insulin sensitivity than the women in our study [38].”
ResultArathimos, R., Granell, R., Haycock, P., Richmond, R. C., Yarmolinsky, J., Relton, C. L., & Tilling, K. M. (2019) · Thorax · doi:10.1136/thoraxjnl-2018-212207 · Cited by 40 · see citing works
Traish, A. M., Abdallah, B., & Yu, G. W. (2011) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci.2011.132 · Cited by 36 · see citing works
“, 1993 [64] There is a positive relationship between total T levels and insulin sensitivity in diabetic males IR is associated with decreased levels of SHBG levels in men with T2DM Heufelder et al.”
BackgroundResultKim, M. R., Gupta, M., Travers, S., Rogers, D., van Lente, F., & Faiman, C. (1999) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1999.00636.x · Cited by 34 · see citing works
“Although we did not measure insulin levels or insulin sensitivity in these subjects, the negative correlations of SHBG to BMI and body weight [both of which influence insulin sensitivity (Birkeland et al., 1993; Peiriset al., 1993)] would lend support to the contention that insulin mediates at least some of the change…”
BackgroundResultBirkenaes, A. B., Birkeland, K., Friis, S., Opjordsmoen, S., & Andreassen, O. (2009) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31819b95fc · Cited by 32 · see citing works
“Furthermore, the levels of sex hormoneYbinding globulin (SHBG), a liver protein transporting estrogen and testosterone in blood, are negatively influenced by circulating insulin concentrations.(14,15) Finally, cortisol may increase both insulin and leptin secretion, and the intrinsic stress of psychiatric illness has…”
BackgroundSelf-citationIturriaga, H. (1999) · Alcohol and Alcoholism · doi:10.1093/alcalc/34.6.903 · Cited by 33 · see citing works
“insulin (Pugeat et al., 1991; Birkeland et al., 1993), cortisol (Tegelman et al.”
BackgroundThe free androgen index is inaccurate in women when the SHBG concentration is low
Keevil, B. G., Adaway, J., Fiers, T., Moghetti, P., & Kaufman, J. (2018) · Clinical Endocrinology · doi:10.1111/cen.13561 · Cited by 35 · see citing works
Measuring Insulin Resistance in Humans
Sharma, V. R., Matta, S. T., Haymond, M. W., & Chung, S. T. (2020) · Hormone Research in Paediatrics · doi:10.1159/000515462 · Cited by 30 · see citing works
Bhattoa, H. P., Onyeka, U., Kalina, E., Balogh, Á. L., Paragh, G., Antal‐Szalmás, P., & Káplár, M. (2013) · Clinical Rheumatology · doi:10.1007/s10067-013-2254-y · Cited by 22 · see citing works
Effects of Dietary Intake and Life Style on Bone Density in Patients with Diabetes mellitus Type 2
Román, D. A. D. L., Aller, R., Castrillón, J. L. P., de Luís, J., Sagrado, M., Izaola, O., Romero, E., Escudero, J. C. M., & Herreros, V. (2004) · Annals of Nutrition and Metabolism · doi:10.1159/000078376 · Cited by 31 · see citing works
Metabolic syndrome and hypogonadism – two peas in a pod
Ebrahimi, F., & Christ‐Crain, M. (2016) · Swiss Medical Weekly · doi:10.4414/smw.2016.14283 · Cited by 32 · see citing works
The Metabolic Syndrome in Central Hypogonadotrophic Hypogonadism
Dwyer, A. A., & Quinton, R. (2018) · Frontiers of hormone research · doi:10.1159/000485998 · Cited by 30 · see citing works
Bonnet, F., Velayoudom Cephise, F., Gautier, A., Dubois, S., Massart, C., Camara, A., Larifla, L., Balkau, B., & Ducluzeau, P. (2013) · Clinical Endocrinology · doi:10.1111/cen.12089 · Cited by 28 · see citing works
Ray, S., Chatterjee, K., De, D., & Ghosh, D. (2014) · Andrologia · doi:10.1111/and.12133 · Cited by 27
“…semen quality along with erectile dysfunction and loss of libido are generally associated with low plasma levels of gonadotrophins and testosterone (Birkeland et al., 1993; Rehman et al., 2001), and diminished testosterone production is also one of the potential causes of infertility in males…”
BackgroundAssociation of increased C-peptide serum levels and testosterone in type 2 diabetes.
Zietz, B., Cuk, A., Hügl, S., Büttner, R., Straub, R., Bauer, B., Daffner, P., Schölmerich, J., & Palitzsch, K. (2000) · European journal of internal medicine · doi:10.1016/s0953-6205(00)00122-9 · Cited by 27 · see citing works
Relationship between insulin and hypogonadism in men with metabolic syndrome
Caldas, A. D. A., Porto, A. L. A., da Motta, L. D. C., & Casulari, L. A. (2009) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302009000800015 · Cited by 25 · see citing works
“A similar decrease in the SHBG levels in hypogonadic patients has been previously described in individuals with metabolic syndrome and is associated with insulin resistance, carbohydrate intolerance and central obesity (23,32-36).”
BackgroundMitchell, A., Fall, T., Melhus, H., Wolk, A., Michaëlsson, K., & Byberg, L. (2018) · Calcified Tissue International · doi:10.1007/s00223-018-0446-9 · Cited by 25 · see citing works
“Insulin resistance measured using HOMA-IR has been shown to be inversely associated with bone size [14], potentially explained by high levels of insulin being inversely associated with sex hormone-binding globulin (SHBG), thus increasing the free concentrations of androgens and estrogens [32].”
MethodThe hepatic lipidome and HNF4α and SHBG expression in human liver
Winters, S. J., Scoggins, C. R., Appiah, D., & Ghooray, D. T. (2020) · Endocrine Connections · doi:10.1530/ec-20-0401 · Cited by 28 · see citing works
“SHBG levels are lower with obesity (2) and in patients with type 2 (T2DM) but not type 1diabetes (3,4), and in those with the Metabolic Syndrome (MetS) (5).”
BackgroundTeoh, J. Y., Chiu, P. K., Chan, S. Y. S., Poon, D. M. C., Cheung, H., Hou, S. S. M., & Ng, C. (2015) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyv025 · Cited by 22 · see citing works
González-Ortiz, M., Martínez-Abundis, E., & Lifshitz, A. (1998) · Gynecologic and Obstetric Investigation · doi:10.1159/000010030 · Cited by 22 · see citing works
Androgens and insulin resistance in type 1 diabetic men
Ebeling, P., Stenman, U., Seppälä, M. T., & Koivisto, V. A. (1995) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1995.tb02925.x · Cited by 15 · see citing works
“, 1994) and in type 2 diabetic patients (Birkeland et al., 1993) insulin sensitivity is positively correlated to serum SHBG concentration.”
BackgroundResultInfluentialXargay‐Torrent, S., Carreras‐Badosa, G., Borrat-Padrosa, S., Prats‐Puig, A., Soriano, P., Álvarez-Castaño, E., Ferri, M. J., de Zegher, F., Ibáñez, L., López‐Bermejo, A., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205592 · Cited by 21 · see citing works
“SHBG production is negatively regulated by insulin and monosaccharides and numerous studies in men, children and adolescents have shown that SHBG levels are reduced in obesity, insulin resistance, metabolic syndrome and type 2 diabetes [12,13].”
BackgroundMetabolically healthy/unhealthy components may modify bone mineral density in obese people
Mirzababaei, A., Mirzaei, K., Khorrami-nezhad, L., Maghbooli, Z., & Keshavarz, S. (2017) · Archives of Osteoporosis · doi:10.1007/s11657-017-0381-9 · Cited by 19
“Furthermore, hyperinsulinemia may also have a negative impact on sex hormone-binding globulin, hence increasing free androgens and estrogens hormone which may protect against bone loss [29, 30].”
Background
- Authors
- Birkeland, K. I., Hanssen, K. F., Torjesen, P. A., & Vaaler, S.
- Affiliations
- Oslo University Hospital (NO)
- ORCID
- Birkeland, K I
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1993-02
- Volume
- 76
- Issue
- 2
- Pages
- 275-278
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2155219543
- Cited by
- 161
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 7 · 2023: 2 · 2022: 3 · 2020: 5 · 2019: 5 · 2018: 5 · 2017: 7 · 2016: 8 · 2015: 5 · 2014: 4 · 2013: 7 · 2012: 7
- FWCI
- 3.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (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 › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- sex hormone-binding globulin, insulin sensitivity, type 2 diabetes, insulin resistance, glucose metabolism, free estradiol, free testosterone, sex hormones, triglycerides, diastolic blood pressure, men
- MeSH terms
- Adipose Tissue, Aged, Body Composition, C-Peptide, Diabetes Mellitus, Type 2, Estradiol, Humans, Insulin, Male, Middle Aged, Regression Analysis, Sex Hormone-Binding Globulin, Testosterone, Glucose Clamp Technique, Body Mass Index
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