The DOI matches its Crossref record.
Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts male aging study.
Abstract
OBJECTIVE: The objective was to examine prospectively the association between low testosterone and sex hormone-binding globulin (SHBG) levels and the subsequent development of type 2 diabetes in men. RESEARCH DESIGN AND METHODS: Analyses were conducted on the cohort of the Massachusetts Male Aging Study, a population-based random sample of men aged 40-70. Of the 1,709 men enrolled in 1987-1989 (T1), 1,156 were followed up 7-10 years later (T2). Testosterone and SHBG levels at T1 were used to predict new cases of diabetes between T1 and T2. RESULTS: After controlling for potential confounders, diabetes at follow-up was predicted jointly and independently by lower baseline levels of free testosterone and SHBG. The odds ratio for future diabetes was 1.58 for a decrease of 1SD in free testosterone (4 ng/dl) and 1.89 for a 1SD decrease in SHBG (16 nmol/l), both significant at P < 0.02. CONCLUSIONS: Our prospective findings are consistent with previous, mainly cross-sectional reports, suggesting that low levels of testosterone and SHBG play some role in the development of insulin resistance and subsequent type 2 diabetes.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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 [41]
In the citing paper
“Low testosterone levels have also been found to predict insulin resistance and the future development of type 2 diabetes (3-5).”
From Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes (2007) · cites this paper as [4]
Citations
Cited by
Sorted by citations
Items 501–600 of 618
Rol' korrektsii gipogonadizma v lechenii metabolicheskogo sindroma u muzhchin
Kalinchenko, S. Y., & Tishova, Y. A. (2006) · Obesity and metabolism · doi:10.14341/2071-8713-4867 · Cited by 2
Georgescu, O., Reghina, A. D., Ioacără, S., Nica, C., & Fica, S. V. (2013) · Romanian Journal of Diabetes Nutrition and Metabolic Diseases · doi:10.2478/rjdnmd-2013-0040 · Cited by 2
Evidence of male hypogonadism at an early age as a familial risk of type 2 diabetes
Janjua, Q. M., Shahid, A., Alam, R., Rizwan, M., Saeed, S., Qazi, M. H., & Arslan, M. (2015) · Annales d Endocrinologie · doi:10.1016/j.ando.2015.10.005 · Cited by 2
Mohammad, A. A., Laleh, B., Ardakani, J. M., Chiti, Z., Rashidi, M., & Azod, L. (2010) · Iranian journal of diabetes and obesity · Cited by 2
TESTOSTERONE REPLACEMENT THERAPY AND CARDIOVASCULAR RISK
Berdnikov, S. V., & Бердникова, О. А. (2017) · Siberian medical review · doi:10.20333/2500136-2017-2-14-21 · Cited by 2
Bunruam, K., Kupittayanant, S., Rangsriwatananon, K., & Manakasem, Y. (2010) · Cited by 2
Alhammer, A. H. (2015) · Journal of Biotechnology Research Center · doi:10.24126/jobrc.2015.9.1.391 · Cited by 2
Gamidov, S. I., Тажетдинов, О. Х., Pavlovichev, A., Попова, А. Ю., & Тхагапсоева, Р. А. (2010) · Problems of Endocrinology · doi:10.14341/probl201056533-42 · Cited by 2
[Action of androgens on fat distribution and metabolic balance].
Tostain, J.-B., Heim, M., & Rossi, D. (2004) · PubMed · Cited by 1
Sleep Deprivation and Metabolic Syndrome
Mugnai, G., & Danese, A. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-420168-2.00020-x · Cited by 2
Nutritional Pathways to Protect Male Reproductive Health
Hsieh, T., Marinaro, J. A., & Shin, P. R. (2020) · Springer eBooks · doi:10.1007/978-3-030-32300-4_42 · Cited by 2
Hormonersatztherapie beim Mann - Sinn oder Unsinn?
Jockenhövel, F., & Schubert, M. (2003) · Journal für Kardiologie (Krause & Pachernegg GmbH) · Cited by 2
Salah, M., Ismail, K. A., & Khadrawy, S. M. (2021) · Research Square · doi:10.21203/rs.3.rs-814954/v1 · Cited by 2
Ab, D., & Ilyasov, R. R. I. (2017) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro201711721149-154 · Cited by 1
Abichandani, V. K., & Kalhan, A. (2023) · Chronicle of Diabetes Research and Practice · doi:10.4103/cdrp.cdrp_cdrp_20_22 · Cited by 1
Armeni, E. (2024) · Metabolism and Target Organ Damage · doi:10.20517/mtod.2023.40 · Cited by 1
Hwang, H., Kim, Y. S., Sunwoo, S., Yu, B.-Y., Bae, W.-K., Park, J. S., Park, Y., Park, Y.-K., Yang, Y. J., Kim, C.-M., et al. (2013) · Journal of Men s Health · doi:10.1089/jomh.2013.1505 · Cited by 1
Metabolic syndrome in men with sexual dysfunction
Talukder, S. K., Afsana, F., & Khan, S. J. (2010) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2010.07.001 · Cited by 1
Androgens, visceral obesity and the risks for cardiovascular disease and diabetes mellitus
Gooren, L. J. (2007) · The Journal of Men s Health and Gender · doi:10.1016/j.jmhg.2007.02.001 · Cited by 1
Al‐Khallaf, H. (2012) · Journal of Diabetes and Endocrinology · doi:10.5897/jde11.015 · Cited by 1
Can the administration of testosterone to men with late-onset hypogonadism be discontinued?
Gooren, L. J. (2008) · Journal of Men s Health · doi:10.1016/j.jomh.2008.09.005 · Cited by 1
“…clear that disease and, in particular, features of the metabolic syndrome, suppress circulating T levels, it has also been documented that low T induces the metabolic syndrome [6,31,32], dramatically demonstrated by findings in men with prostate cancer who undergo androgen ablation therapy [33–35].”
Influência da idade e do diabetes sobre esteróides sexuais e SHBG em homens
Bahia, L., & Gomes, M. B. (2003) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302003000300009 · Cited by 1
Testosterone Treatment Improves Insulin Resistance in Japanese Male Metabolic Syndrome
Ueshiba, H. (2013) · Journal of Steroids & Hormonal Science · doi:10.4172/2157-7536.1000116 · Cited by 1
METABOLI) SYNDROME AND MALE REPRODUCTIVE HEALTH
Burmistrova, T. A., & Zykova, T. A. (2012) · CyberLeninK (CyberLeninka) · Cited by 1
The Effect of Obesity on Male Reproductive Function
Tremellen, K. P., & Pearce, K. (2015) · CRC Press eBooks · doi:10.1201/b18190-13 · Cited by 1
The Efficacy of Testosterone Ointment on Insulin Resistance in Men with Metabolic Syndrome
Ueshiba, H. (2017) · Journal of Metabolic Syndrome · doi:10.4172/2167-0943.1000225 · Cited by 1
Agarwal, S., Kumar, B. N., Sushmita, Giri, R., & Verma, S. K. (2019) · International Journal of Research in Medical Sciences · doi:10.18203/2320-6012.ijrms20192481
Stanton, A. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-1793-8.00034-0 · Cited by 2
Oğuz, S. H., & Yıldız, B. O. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-98804-9.00029-3 · Cited by 1
Popova, A. V. (2012) · Obesity and metabolism · doi:10.14341/2071-8713-5127 · Cited by 1
Recent perspectives on the age-related decline of testosterone
Gooren, L. J. (2008) · Journal of Men s Health · doi:10.1016/j.jomh.2007.12.003 · Cited by 1
“This observation finds support from the prestigious Massachusetts Male Aging Study (MMAS) [11–14].”
Cardiometabolic effects of testosterone in older men
Hackett, G. I. (2015) · Cardiovascular Endocrinology · doi:10.1097/xce.0000000000000050 · Cited by 1
Tiwari, A., & Srivastava, A. (2016) · Journal of Evidence Based Medicine and Healthcare · doi:10.18410/jebmh/2016/975 · Cited by 1
Androgen Therapy in Male Patients Suffering from Type 2 Diabetes: A Review of Benefits and Risks
Hassanabad, M. F., & Fatehi, M. (2018) · Current Diabetes Reviews · doi:10.2174/1573399814666180731125724 · Cited by 1
Chin, K. (2019) · Medicine & health · doi:10.17576/mh.2019.1402.15 · Cited by 1
Male hypogonadism and pre-diabetes interplay: association or causal interaction? A systematic review
Greco, C., Corleto, R., Ebert, R., Simoni, M., Rochira, V., & Santi, D. (2021) · Metabolism and Target Organ Damage · doi:10.20517/mtod.2021.14 · Cited by 1
Cardiovascular Disease, Insulin Resistance, Metabolic Syndrome, and AGA/FPHL
Anastassakis, K. (2022) · Springer eBooks · doi:10.1007/978-3-030-76111-0_21 · Cited by 1
Long-Term Morbidity of Late-Onset Hypogonadism
Behre, H. M. (2005) · European Urology Supplements · doi:10.1016/j.eursup.2005.05.003 · Cited by 1
Traish, A. M., Saad, F., & Guay, A. T. (2008) · Cited by 1
Sexualidad y reproducción, un campo importante de la endocrinología
Becerra-Fernández, A. (2006) · Endocrinología y Nutrición · doi:10.1016/s1575-0922(06)71064-6 · Cited by 1
Prostate Cancer Incidence Among Men Using Statins, Finasteride or Antidiabetic Drugs
Murtola, T. J. (2009) · Tampere University Institutional Repository (Tampere University) · Cited by 1
Testosterone, SHBG, and the Metabolic Cardiovascular Syndrome
Zmuda, J. M., & Winters, S. J. (2004) · Humana Press eBooks · doi:10.1007/978-1-59259-727-7_17 · Cited by 1
Hackett, G. I. (2017) · Wiley eBooks · doi:10.1002/9781118954621.ch13 · Cited by 1
CARDIOVASCULAR ENDOCRINOLOGY Endogenous Sex Hormones and Cardiovascular Disease in Men
Muller, M., van der Schouw, T., Thijssen, J. H. H., & Grobbee, D. E. (2003) · Cited by 1
Erectile and Sex Hormone Dysfunction and Cardiovascular Consequences in CKD
Solak, Y., & Kanbay, M. (2014) · Springer eBooks · doi:10.1007/978-3-319-09162-4_16
The interrelationship of sex steroid levels, body composition and bone characteristics in men
Lapauw, B. (2009) · Ghent University Academic Bibliography (Ghent University)
Hormonwirkungen und Hormontherapie
Schubert, M., Jockenhövel, F., Brüning, J. C., Allolio, B., Callies, F., Lerchl, A., Gerhards, S., Kühnert, B., & Nieschlag, E. (2004) · Springer eBooks · doi:10.1007/978-3-642-18705-6_2
Rozhivanov, R. V. (2012) · Obesity and metabolism · doi:10.14341/2071-8713-5123
As, A., Morgunov, L. Y., & Olisaev, R. V. (2007) · Diabetes Mellitus · doi:10.14341/2072-0351-5798
The Effect of Testosterone Therapy on the Mortality Rate in Men Suffering From Diabetes Mellitus
Tran, D. (2015) · CommonKnowledge Research Repository (Pacific University Oregon)
Testosterone Replacement Therapy in Men: Effects on Fertility and Health
Chan, P. T. K. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7187-5_4
Déficit androgénico y síndrome metabólico
Hernández, J. J. C. (2007) · Revista Internacional de Andrología · doi:10.1016/s1698-031x(07)74065-7
Male hypogonadism and the metabolic syndrome: lessons from clinical studies
Rodzvilla, J. P. (2006) · Drug Development Research · doi:10.1002/ddr.20135
“…Male Aging Study at the first follow-up visit (7 to 10 years after enrollment) found that the incidence of diabetes in men who were non-diabetic at the study’s inception was significantly increased in men with lower SHBG and lower T, both free and total at baseline [Stellato et al., 2000].”
Schubert, M. (2015) · Info Diabetologie · doi:10.1007/s15034-015-0516-2
Hall, S. A., Page, S. T., Travison, T. G., Montgomery, B., Link, C. L., & McKinlay, J. B. (2007) · Annals of Epidemiology · doi:10.1016/j.annepidem.2007.07.024
Self-citationPsychosocial stress and male gonadal function
Nilsson, P. M., & Båvenholm, P. (2002) · International Congress Series · doi:10.1016/s0531-5131(01)00470-8
Masui, Y., Hamasaki, H., Sako, A., et al. (2012) · Journal of Endocrinology and Metabolism · doi:10.4021/jem.v2i4-5.136
Diagnosing and Evaluating Androgen Deficiency, Including Andropause
Richard, C. Y. T. (2012) · Springer eBooks · doi:10.1007/978-1-4471-4766-4_4
Farrell, J. A. B., Deshmukh, A., & Baghaie, A. A. (2010) · Expert Review of Endocrinology & Metabolism · doi:10.1586/eem.09.59
artigo original Influência da Idade e do Diabetes Sobre Esteróides Sexuais e SHBG em Homens
Bahia, L., & Gomes, M. B. (2003)
Review Testosterone and Erectile Dysfunction
Yassin, A. A., Saad, F., & Schering, B. (2008)
Cambios fisiológicos durante el envejecimiento del sistema reproductor masculino
Wiechers, L. L., & Cuéllar, H. L. P. (2007) · Revista de Endocrinología y Nutrición
Low Testosterone Levels in Male Patients with Hypertension,
Agarwal, S. K. (2015)
Short title - Testosterone and Erectile Dysfunction
Yassin, A. A., Saad, F., & Schering, B. (2008)
Mandal, P. K., Majumdar, G., Ghosh, S., Swaika, S., Chakraborty, M., & Swaika, B. C. (2013) · Journal of Advances in Medicine
Возрастной гипогонадизм у мужчин с метаболическим синдромом
Mskhalaya, G., & Yu, K. S. (2010) · CyberLeninK (CyberLeninka)
Testosterone and cardiovascular disease
Yuen, K. C. J. (2014) · Cardiovascular Endocrinology · doi:10.1097/xce.0000000000000038
Benefits of testosterone replacementHACKETT
Hackett, G. I. (2013)
Diabetes and Metabolic Syndrome Disorders Review Article
Ediz, C., & Altıntaş, R. (2014)
13. Late Onset Hypogonadism Syndrome
Horie, S. (2013) · Nihon Naika Gakkai Zasshi · doi:10.2169/naika.102.914
Testosterone and Risk Factors in the Metabolic Syndrome: Implications for Erectile Dysfunction
Guay, A. T., & Traish, A. M. (2011)
Fertility and Testosterone Improvement in Male Patients After Bariatric Surgery
Luconi, M., Corona, G., Facchiano, E., Lucchese, M., & Maggi, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800872-0.00010-x
Levels of Endogenous Sex Hormones in Male Vegetarians and Non-Vegetarians
Dogbe, Y. Y. (2015)
Slepynina, Y. S., & Каретникова, В. Н. (2012) · CyberLeninK (CyberLeninka)
Gianatti, E. (2016) · Minerva Access (University of Melbourne)
Obesity and Aging in Late-Onset Hypogonadism
Rastrelli, G., & Wu, F. C. W. (2017) · Springer eBooks · doi:10.1007/978-3-319-53298-1_17
Functional Hypogonadism: Diabetes Mellitus, Obesity, Metabolic Syndrome, and Testosterone
Meirelles, R. M. D. R. (2017) · Springer eBooks · doi:10.1007/978-3-319-46086-4_7
Causas y consecuencias del hipogonadismo en varones con diabetes mellitus tipo 2
Ruiz, A. H. (2015) · Gredos (University of Salamanca) · doi:10.14201/gredos.128430
EVALUATION OF TESTOSTERONE DEFICIENCY IN PATIENTS OF TYPE 2 DIABETES MELLITUS
Chandel, K., Gupta, A., Agrawal, P., & Nath, K. (2016) · Journal of Evolution of Medical and Dental Sciences · doi:10.14260/jemds/2016/309
Ganie, M. A., Rahaman, S. H., & Raizada, N. (2017) · Springer eBooks · doi:10.1007/978-981-10-3695-8_23
Chirurgie bariatrique et fertilité
Rives‐Lange, C., Boudaoud, A. A., Czernichow, S., Bretault, M., Barsamian, C., Radu, A., Lévy, R., Bouillot, J., & Carette, C. (2017) · Obésité · doi:10.1007/s11690-017-0569-6
Late-onset androgen deficiency syndrome in males. Modern approaches to diagnosis and treatment
Кирилюк, М. Л. (2013) · Clinical endocrinology and endocrine surgery · doi:10.24026/1818-1384.3(44).2013.77904
Hendrik Isbarn, A., BOCCON-GIBOD, L., Carroll, P. R., Montorsi, F., Schulman, C., Smith, M. R., Sternberg, C. N., & Studer, U. E. (2009)
Effects of testosterone levels on mortality and cardiovascular risk in men with Type 2 diabetes
Muraleedharan, V. (2018) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
Gesundheitsvorsorge für den älteren Mann: Präventionskonzepte aus internistischer Sicht
Ae, H., & Despeghel-Schoene, M. (2004) · Journal für Kardiologie (Krause & Pachernegg GmbH)
TESTOSTERONE LEVEL IN TYPE 2 DIABETIC MALE PATIENTS
Mustafa, H. M., Fattah, F., & Salih, I. (2020) · Journal of Sulaimani Medical College · doi:10.17656/jsmc.10235
Health Consequences of Circadian Disruption
Rogers, N. L., & Whitwell, B. G. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-378610-4.00274-6
Nedogoda, S. V., Salasyuk, A. S., Barykina, I. N., et al. (2013) · Cardiosomatics · doi:10.26442/cs45034
Influence of androgen deprivation therapy on glucose metabolism and ambulatory glucose profile
Grickevich, E. Y., Скуридина, Д. В., & Perekhodov, S. N. (2021) · Meditsinskiy sovet = Medical Council · doi:10.21518/2079-701x-2021-7-172-182
The anti-inflammatory effects of testosterone on atherosclerosis
Bateman, L. (2020) · Sheffield Hallam University · doi:10.7190/shu-thesis-00351 · Cited by 1
Effects of metabolic syndrome on erectile dysfunction
Khan, A. I., Enobakhare, O., Stoddard, M. D., Eidelberg, A., Punjani, N., & Kashanian, J. A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819765-3.00014-5
郭洪丹 (2010) · Journal of Tonghua Normal University
Sugimoto, K., Murakawa, Y., Zhang, W., et al. (2000) · Diabetes/Metabolism Research and Reviews · doi:10.1002/1520-7560(200009/10)16:5
Vettor, R., & Angelo, D. V. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.66105-6
Rozhivanov, R. V. (2013) · Obesity and metabolism · doi:10.14341/2071-8713-5071
Cleffi, S., Neto, A. S., Reis, L. O., Maia, P., Fonseca, F. L. A., Wroclawski, M. L., Neves, M., Pompeo, A. C. L., Giglio, A. D., Faria, E. F., et al. (2011) · Actas Urológicas Españolas · doi:10.4321/s0210-48062011000500002
Nutritional Pathways to Protect Male Reproductive Health
Hsieh, T., & Shin, P. R. (2013) · Springer eBooks · doi:10.1007/978-1-4614-9158-3_16
Janjgava, S., Zerekidze, T., Uchava, L., Giorgadze, E., & Asatiani, K. (2014) · Open Access Macedonian Journal of Medical Sciences · doi:10.3889/oamjms.2014.107
Metadata
- Authors
- Stellato, R. K., Feldman, H. A., Hamdy, O., Horton, E. S., & McKinlay, J. B.
- Affiliations
- New England Research Institutes (US)
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2000-04-01
- Volume
- 23
- Issue
- 4
- Pages
- 490-494
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2086247313
- Cited by
- 618
- References
- 0
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 12 · 2023: 9 · 2022: 10 · 2021: 16 · 2020: 16 · 2019: 13 · 2018: 20 · 2017: 32 · 2016: 34 · 2015: 37 · 2014: 36 · 2013: 40 · 2012: 38
- FWCI
- 8.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (7p01ag004673-05)
- National Institute on Aging (AG 04673)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 51345, R01DK044995, DK44995, R01DK051345)
- 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
- testosterone, sex hormone-binding globulin, type 2 diabetes, free testosterone, insulin resistance, middle-aged men, Massachusetts Male Aging Study, diabetes risk factors, older men
- MeSH terms
- Adult, Aged, Aging, Diabetes Mellitus, Type 2, Heart Diseases, Humans, Hypertension, Longitudinal Studies, Male, Massachusetts, Middle Aged, Predictive Value of Tests, Sex Hormone-Binding Globulin, Testosterone, Time Factors, Cohort Studies, Health Behavior, Racial Groups
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review