Skip Navigation

This Article
Right arrow FREE Full Text (PDF) Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (103)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Haffner, S. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Haffner, S. M.
Social Bookmarking
 Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

American Journal of Epidemiology Vol. 143, No. 9: 889-897
Copyright © 1996 by The Johns Hopkins University School of Hygiene and Public Health


research-article

Low Levels of Sex Hormone-binding Globulin and Testosterone Predict the Development of Non-Insulin-dependent Diabetes Mellitus in Men

Steven M. Haffner1, Jessica Shaten2,, Michael P. Stem1, George Davey Smith3, Lewis Kuller4 and MRFIT Research Group

1Division of Clinical Epidemiology, Department of Medicine, University of Texas Health Science Center at San Antonio San Antonio, TX
2Multiple Risk Factor Intervention Trial Coordinating Center, Division of Biostatistics, School of Public Health, University of Minnesota Minneapolis, MN
3Department of Public Health, University of Glasgow Glasgow, Scotland
4Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh Pittsburgh, PA

Reprint requests to Jessica Shaten, University of Minnesota School of Public Health, MRFIT Coordinating Center, 2221 University Avenue S.E., Suite 200, Minneapolis, MN 55414

Few prospective data are available regarding the association of sex hormone-binding globulin (SHBG), testosterone, and the risk of developing diabetes. Stored fasting serum samples from participants enrolled in the Multiple Risk Factor Intervention Trial (MRFIT) at 22 different centers throughout the United States from December 1973 through February 1976 were used to perform a nested case-control study. For 176 initially nondiabetic men who developed diabetes during 5 years of follow-up, two controls were selected, one matched only for randomization date, treatment group, and clinic ("loose controls") and the other matched additionally for fasting glucose and body mass index ("tight controls"). When cases were compared with loose controls, higher levels of fasting insulin and lower levels of total and free testosterone and SHBG were significantly associated with increased development of diabetes. However, when cases were compared with tightly matched controls, these associations weakened considerably. Low SHBG and testosterone may constitute part of the prediabetic state in men along with previously reported variables, such as higher glucose and insulin levels and obesity. Am J Epidemiol 1996;143:889–97.

diabetes mellitus; insulin; prasterone; sex hormone-binding globulin; testosterone


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
J Gerontol A Biol Sci Med SciHome page
K. M. Lakshman, S. Bhasin, and A. B. Araujo
Sex Hormone-Binding Globulin as an Independent Predictor of Incident Type 2 Diabetes Mellitus in Men
J Gerontol A Biol Sci Med Sci, January 27, 2010; (2010): glq002v1 - glq002.
[Abstract] [Full Text] [PDF]


Home page
Exp Biol MedHome page
A. Chamson-Reig, S. M. Thyssen, D. J. Hill, and E. Arany
Exposure of the Pregnant Rat to Low Protein Diet Causes Impaired Glucose Homeostasis in the Young Adult Offspring by Different Mechanisms in Males and Females
Exp Biol Med, December 1, 2009; 234(12): 1425 - 1436.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
S. M. Patel, S. J. Ratcliffe, M. P. Reilly, R. Weinstein, S. Bhasin, M. R. Blackman, J. A. Cauley, K. Sutton-Tyrrell, J. Robbins, L. P. Fried, et al.
Higher Serum Testosterone Concentration in Older Women is Associated with Insulin Resistance, Metabolic Syndrome, and Cardiovascular Disease
J. Clin. Endocrinol. Metab., December 1, 2009; 94(12): 4776 - 4784.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
A. D. Coviello, S. Sam, R. S. Legro, and A. Dunaif
High Prevalence of Metabolic Syndrome in First-Degree Male Relatives of Women with Polycystic Ovary Syndrome Is Related to High Rates of Obesity
J. Clin. Endocrinol. Metab., November 1, 2009; 94(11): 4361 - 4366.
[Abstract] [Full Text] [PDF]


Home page
British Journal of Diabetes & Vascular DiseaseHome page
G. I Hackett, N. S Cole, A. A Deshpande, M. D Popple, D. Kennedy, and P. Wilkinson
Biochemical hypogonadism in men with type 2 diabetes in primary care practice
The British Journal of Diabetes & Vascular Disease, September 1, 2009; 9(5): 226 - 231.
[Abstract] [PDF]


Home page
Eur J EndocrinolHome page
F Bonnet, B Balkau, J M Malecot, P Picard, C Lange, F Fumeron, R Aubert, V Raverot, H Dechaud, J Tichet, et al.
Sex hormone-binding globulin predicts the incidence of hyperglycemia in women: interactions with adiponectin levels
Eur. J. Endocrinol., July 1, 2009; 161(1): 81 - 85.
[Abstract] [Full Text] [PDF]


Home page
Menopause IntHome page
A. Theodoraki and P.-M. Bouloux
Testosterone therapy in men
Menopause Int, June 1, 2009; 15(2): 87 - 92.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
A. M. Traish, F. Saad, and A. Guay
The Dark Side of Testosterone Deficiency: II. Type 2 Diabetes and Insulin Resistance
J Androl, January 1, 2009; 30(1): 23 - 32.
[Abstract] [Full Text] [PDF]


Home page
Eur J EndocrinolHome page
R D Stanworth, D Kapoor, K S Channer, and T H Jones
Androgen receptor CAG repeat polymorphism is associated with serum testosterone levels, obesity and serum leptin in men with type 2 diabetes
Eur. J. Endocrinol., December 1, 2008; 159(6): 739 - 746.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
A. A. Yassin and F. Saad
Testosterone and Erectile Dysfunction
J Androl, November 1, 2008; 29(6): 593 - 604.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
T. J. Murtola, T. L. J. Tammela, J. Lahtela, and A. Auvinen
Antidiabetic Medication and Prostate Cancer Risk: A Population-based Case-Control Study
Am. J. Epidemiol., October 15, 2008; 168(8): 925 - 931.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
V. Kupelian, F. J. Hayes, C. L. Link, R. Rosen, and J. B. McKinlay
Inverse Association of Testosterone and the Metabolic Syndrome in Men Is Consistent across Race and Ethnic Groups
J. Clin. Endocrinol. Metab., September 1, 2008; 93(9): 3403 - 3410.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
S. Basaria
Androgen Deprivation Therapy, Insulin Resistance, and Cardiovascular Mortality: An Inconvenient Truth
J Androl, September 1, 2008; 29(5): 534 - 539.
[Abstract] [Full Text] [PDF]


Home page
Diabetes and Vascular Disease ResearchHome page
D. Kapoor, K. S Channer, and T H. Jones
Rosiglitazone increases bioactive testosterone and reduces waist circumference in hypogonadal men with type 2 diabetes
Diabetes and Vascular Disease Research, June 1, 2008; 5(2): 135 - 137.
[Abstract] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
S. Shahani, M. Braga-Basaria, and S. Basaria
Androgen Deprivation Therapy in Prostate Cancer and Metabolic Risk for Atherosclerosis
J. Clin. Endocrinol. Metab., June 1, 2008; 93(6): 2042 - 2049.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
S. S. Kasturi, J. Tannir, and R. E. Brannigan
The Metabolic Syndrome and Male Infertility
J Androl, May 1, 2008; 29(3): 251 - 259.
[Abstract] [Full Text] [PDF]


Home page
Cancer Epidemiol. Biomarkers Prev.Home page
J. A. Darbinian, A. M. Ferrara, S. K. Van Den Eeden, C. P. Quesenberry Jr., B. Fireman, and L. A. Habel
Glycemic Status and Risk of Prostate Cancer
Cancer Epidemiol. Biomarkers Prev., March 1, 2008; 17(3): 628 - 635.
[Abstract] [Full Text] [PDF]


Home page
Clin. Chem.Home page
K. S. Fritz, A. J.S. McKean, J. C. Nelson, and R. B. Wilcox
Analog-Based Free Testosterone Test Results Linked to Total Testosterone Concentrations, Not Free Testosterone Concentrations
Clin. Chem., March 1, 2008; 54(3): 512 - 516.
[Abstract] [Full Text] [PDF]


Home page
CirculationHome page
K.-T. Khaw, M. Dowsett, E. Folkerd, S. Bingham, N. Wareham, R. Luben, A. Welch, and N. Day
Endogenous Testosterone and Mortality Due to All Causes, Cardiovascular Disease, and Cancer in Men: European Prospective Investigation Into Cancer in Norfolk (EPIC-Norfolk) Prospective Population Study
Circulation, December 4, 2007; 116(23): 2694 - 2701.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
M. A. Yialamas, A. A. Dwyer, E. Hanley, H. Lee, N. Pitteloud, and F. J. Hayes
Acute Sex Steroid Withdrawal Reduces Insulin Sensitivity in Healthy Men with Idiopathic Hypogonadotropic Hypogonadism
J. Clin. Endocrinol. Metab., November 1, 2007; 92(11): 4254 - 4259.
[Abstract] [Full Text] [PDF]


Home page
Cancer Epidemiol. Biomarkers Prev.Home page
S. A. Hall, S. T. Page, T. G. Travison, R. B. Montgomery, C. L. Link, and J. B. McKinlay
Do Statins Affect Androgen Levels in Men? Results from the Boston Area Community Health Survey
Cancer Epidemiol. Biomarkers Prev., August 1, 2007; 16(8): 1587 - 1594.
[Abstract] [Full Text] [PDF]


Home page
Diabetes CareHome page
D. Kapoor, H. Aldred, S. Clark, K. S. Channer, and T. H. Jones
Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes: Correlations with bioavailable testosterone and visceral adiposity
Diabetes Care, April 1, 2007; 30(4): 911 - 917.
[Abstract] [Full Text] [PDF]


Home page
Diabetes CareHome page
E. Selvin, M. Feinleib, L. Zhang, S. Rohrmann, N. Rifai, W. G. Nelson, A. Dobs, S. Basaria, S. H. Golden, and E. A. Platz
Androgens and Diabetes in Men: Results from the Third National Health and Nutrition Examination Survey (NHANES III)
Diabetes Care, February 1, 2007; 30(2): 234 - 238.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
A. J. Tande, E. A. Platz, and A. R. Folsom
The Metabolic Syndrome Is Associated with Reduced Risk of Prostate Cancer
Am. J. Epidemiol., December 1, 2006; 164(11): 1094 - 1102.
[Abstract] [Full Text] [PDF]


Home page
Arch Intern MedHome page
M. Inoue, M. Iwasaki, T. Otani, S. Sasazuki, M. Noda, S. Tsugane, and for the Japan Public Health Center-Based Prospecti
Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan.
Arch Intern Med, September 25, 2006; 166(17): 1871 - 1877.
[Abstract] [Full Text] [PDF]


Home page
Eur J EndocrinolHome page
D Kapoor, E Goodwin, K S Channer, and T H Jones
Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes.
Eur. J. Endocrinol., June 1, 2006; 154(6): 899 - 906.
[Abstract] [Full Text] [PDF]


Home page
JAMAHome page
E. L. Ding, Y. Song, V. S. Malik, and S. Liu
Sex Differences of Endogenous Sex Hormones and Risk of Type 2 Diabetes: A Systematic Review and Meta-analysis
JAMA, March 15, 2006; 295(11): 1288 - 1299.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
V. Kupelian, S. T. Page, A. B. Araujo, T. G. Travison, W. J. Bremner, and J. B. McKinlay
Low Sex Hormone-Binding Globulin, Total Testosterone, and Symptomatic Androgen Deficiency Are Associated with Development of the Metabolic Syndrome in Nonobese Men
J. Clin. Endocrinol. Metab., March 1, 2006; 91(3): 843 - 850.
[Abstract] [Full Text] [PDF]


Home page
Diabetes CareHome page
N. Pitteloud, V. K. Mootha, A. A. Dwyer, M. Hardin, H. Lee, K.-F. Eriksson, D. Tripathy, M. Yialamas, L. Groop, D. Elahi, et al.
Relationship Between Testosterone Levels, Insulin Sensitivity, and Mitochondrial Function in Men
Diabetes Care, July 1, 2005; 28(7): 1636 - 1642.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
E. S. Ford and S. Liu
Invited Commentary: Acne in Adolescence--Protecting the Heart but Damaging the Prostate Later in Life?
Am. J. Epidemiol., June 15, 2005; 161(12): 1102 - 1106.
[Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
N. Pitteloud, M. Hardin, A. A. Dwyer, E. Valassi, M. Yialamas, D. Elahi, and F. J. Hayes
Increasing Insulin Resistance Is Associated with a Decrease in Leydig Cell Testosterone Secretion in Men
J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2636 - 2641.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
G. B. Phillips
Is Atherosclerotic Cardiovascular Disease an Endocrinological Disorder? The Estrogen-Androgen Paradox
J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2708 - 2711.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
T. Kalme, M. Seppala, Q. Qiao, R. Koistinen, A. Nissinen, M. Harrela, M. Loukovaara, P. Leinonen, and J. Tuomilehto
Sex Hormone-Binding Globulin and Insulin-Like Growth Factor-Binding Protein-1 as Indicators of Metabolic Syndrome, Cardiovascular Risk, and Mortality in Elderly Men
J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1550 - 1556.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
D. E. Laaksonen, L. Niskanen, K. Punnonen, K. Nyyssonen, T.-P. Tuomainen, V.-P. Valkonen, and J. T. Salonen
The Metabolic Syndrome and Smoking in Relation to Hypogonadism in Middle-Aged Men: A Prospective Cohort Study
J. Clin. Endocrinol. Metab., February 1, 2005; 90(2): 712 - 719.
[Abstract] [Full Text] [PDF]


Home page
Am J EpidemiolHome page
C. Rodriguez, A. V. Patel, A. M. Mondul, E. J. Jacobs, M. J. Thun, and E. E. Calle
Diabetes and Risk of Prostate Cancer in a Prospective Cohort of US Men
Am. J. Epidemiol., January 15, 2005; 161(2): 147 - 152.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
S. T. Page, K. L. Herbst, J. K. Amory, A. D. Coviello, B. D. Anawalt, A. M. Matsumoto, and W. J. Bremner
Testosterone Administration Suppresses Adiponectin Levels in Men
J Androl, January 1, 2005; 26(1): 85 - 92.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
P. Y. Liu, R. S. Swerdloff, and J. D. Veldhuis
The Rationale, Efficacy and Safety of Androgen Therapy in Older Men: Future Research and Current Practice Recommendations
J. Clin. Endocrinol. Metab., October 1, 2004; 89(10): 4789 - 4796.
[Abstract] [Full Text] [PDF]


Home page
Diabetes CareHome page
D. E. Laaksonen, L. Niskanen, K. Punnonen, K. Nyyssonen, T.-P. Tuomainen, V.-P. Valkonen, R. Salonen, and J. T. Salonen
Testosterone and Sex Hormone-Binding Globulin Predict the Metabolic Syndrome and Diabetes in Middle-Aged Men
Diabetes Care, May 1, 2004; 27(5): 1036 - 1041.
[Abstract] [Full Text] [PDF]


Home page
Diabetes CareHome page
E. C. Tsai, A. M. Matsumoto, W. Y. Fujimoto, and E. J. Boyko
Association of Bioavailable, Free, and Total Testosterone With Insulin Resistance: Influence of sex hormone-binding globulin and body fat
Diabetes Care, April 1, 2004; 27(4): 861 - 868.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
P. Cousin, L. Calemard-Michel, H. Lejeune, G. Raverot, N. Yessaad, A. Emptoz-Bonneton, Y. Morel, and M. Pugeat
Influence of SHBG Gene Pentanucleotide TAAAA Repeat and D327N Polymorphism on Serum Sex Hormone-Binding Globulin Concentration in Hirsute Women
J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 917 - 924.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
P.-H. Ducluzeau, P. Cousin, E. Malvoisin, H. Bornet, H. Vidal, M. Laville, and M. Pugeat
Glucose-to-Insulin Ratio Rather than Sex Hormone-Binding Globulin and Adiponectin Levels Is the Best Predictor of Insulin Resistance in Nonobese Women with Polycystic Ovary Syndrome
J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3626 - 3631.
[Abstract] [Full Text] [PDF]


Home page
J AndrolHome page
S. Bhasin, A. B. Singh, R. P. Mac, B. Carter, M. I. Lee, and G. R. Cunningham
Managing the Risks of Prostate Disease During Testosterone Replacement Therapy in Older Men: Recommendations for a Standardized Monitoring Plan
J Androl, May 1, 2003; 24(3): 299 - 311.
[Full Text] [PDF]


Home page
Am J EpidemiolHome page
S. Ebrahim, G. D. Smith, M. May, and J. Yarnell
Shaving, Coronary Heart Disease, and Stroke: The Caerphilly Study
Am. J. Epidemiol., February 1, 2003; 157(3): 234 - 238.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
P. T. Ellison, R. G. Bribiescas, G. R. Bentley, B. C. Campbell, S. F. Lipson, C. Panter-Brick, and K. Hill
Population variation in age-related decline in male salivary testosterone
Hum. Reprod., December 1, 2002; 17(12): 3251 - 3253.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
N. Abate, S. M. Haffner, A. Garg, R. M. Peshock, and S. M. Grundy
Sex Steroid Hormones, Upper Body Obesity, and Insulin Resistance
J. Clin. Endocrinol. Metab., October 1, 2002; 87(10): 4522 - 4527.
[Abstract] [Full Text] [PDF]


Home page
J Gerontol A Biol Sci Med SciHome page
A. M. Matsumoto
Andropause: Clinical Implications of the Decline in Serum Testosterone Levels With Aging in Men
J Gerontol A Biol Sci Med Sci, February 1, 2002; 57(2): M76 - M99.
[Full Text] [PDF]


Home page
Diabetes CareHome page
J.-Y. Oh, E. Barrett-Connor, N. M. Wedick, and D. L. Wingard
Endogenous Sex Hormones and the Development of Type 2 Diabetes in Older Men and Women: the Rancho Bernardo Study
Diabetes Care, January 1, 2002; 25(1): 55 - 60.
[Abstract] [Full Text] [PDF]


Home page
JNCI J Natl Cancer InstHome page
A. W. Hsing, S. Chua Jr, Y.-T. Gao, E. Gentzschein, L. Chang, J. Deng, and F. Z. Stanczyk
Prostate Cancer Risk and Serum Levels of Insulin and Leptin: a Population-Based Study
J Natl Cancer Inst, May 16, 2001; 93(10): 783 - 789.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
J. E. Michalek, F. Z. Akhtar, and J. L. Kiel
Serum Dioxin, Insulin, Fasting Glucose, and Sex Hormone-Binding Globulin in Veterans of Operation Ranch Hand
J. Clin. Endocrinol. Metab., May 1, 1999; 84(5): 1540 - 1543.
[Abstract] [Full Text]


Home page
Clin. Chem.Home page
D. S. Ooi, J. G. Donnelly, S. J. Winters, D. E. Kelley, and B. Goodpaster
More on the Analog Free-Testosterone Assay • The authors of the article cited above respond:
Clin. Chem., May 1, 1999; 45(5): 714 - 716.
[Full Text] [PDF]


Home page
Clin. Chem.Home page
S. J. Winters, D. E. Kelley, and B. Goodpaster
The analog free testosterone assay: are the results in men clinically useful?
Clin. Chem., October 1, 1998; 44(10): 2178 - 2182.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
D. Simon, M.-A. Charles, K. Nahoul, G. Orssaud, J. Kremski, V. Hully, E. Joubert, L. Papoz, and E. Eschwege
Association between Plasma Total Testosterone and Cardiovascular Risk Factors in Healthy Adult Men: The Telecom Study
J. Clin. Endocrinol. Metab., February 1, 1997; 82(2): 682 - 685.
[Abstract] [Full Text] [PDF]



Disclaimer: Please note that abstracts for content published before 1996 were created through digital scanning and may therefore not exactly replicate the text of the original print issues. All efforts have been made to ensure accuracy, but the Publisher will not be held responsible for any remaining inaccuracies. If you require any further clarification, please contact our Customer Services Department.