The DOI matches its Crossref record; 43 of the 47 references it cites were found in a registry or an index.
Low Sex Hormone-Binding Globulin, Total Testosterone, and Symptomatic Androgen Deficiency Are Associated with Development of the Metabolic Syndrome in Nonobese Men
Abstract
Background: The metabolic syndrome (MetS), characterized by central obesity, lipid and insulin dysregulation, and hypertension, is a precursor state for cardiovascular disease. The purpose of this analysis was to determine whether low serum sex hormone levels or clinical androgen deficiency (AD) predict the development of MetS. Methods: Data were obtained from the Massachusetts Male Aging Study, a population-based prospective cohort of 1709 men observed at three time points (T1, 1987–1989; T2, 1995–1997; T3, 2002–2004). MetS was defined using a modification of the ATP III guidelines. Clinical AD was defined using a combination of testosterone levels and clinical signs and symptoms. The association between MetS and sex hormone levels or clinical AD was assessed using relative risks (RR), and 95% confidence intervals (95% CI) were estimated using Poisson regression models. Results: Analysis was conducted in 950 men without MetS at T1. Lower levels of total testosterone and SHBG were predictive of MetS, particularly among men with a body mass index (BMI) below 25 kg/m2 with adjusted RRs for a decrease in 1 sd of 1.41 (95% CI, 1.06–1.87) and 1.65 (95% CI, 1.12–2.42). Results were similar for the AD and MetS association, with RRs of 2.51 (95% CI, 1.12–5.65) among men with a BMI less than 25 compared with an RR of 1.22 (95% CI, 0.66–2.24) in men with a BMI of 25 or greater. Conclusions: Low serum SHBG, low total testosterone, and clinical AD are associated with increased risk of developing MetS over time, particularly in nonoverweight, middle-aged men (BMI, <25). Together, these results suggest that low SHBG and/or AD may provide early warning signs for cardiovascular risk and an opportunity for early intervention in nonobese men.
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
“In line with these findings, low levels of SHBG seem to be predictive of developing METS at an older age [135, 136].”
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 [136]
Citations
Cites
Grundy, S. M., Bilheimer, D. W., Chait, A., Clark, L. T., Denke, M. A., Havel, R. J., Hazzard, W. R., Hulley, S. B., Hunninghake, D. B., Kreisberg, R. A., et al. (1993) · JAMA · doi:10.1001/jama.269.23.3015 · Cited by 27,944
Expert Panel on Detection, E. (2001) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.285.19.2486 · Cited by 26,011
(1998) · PsycEXTRA Dataset · doi:10.1037/e565682010-001 · Cited by 9,453
Longitudinal Effects of Aging on Serum Total and Free Testosterone Levels in Healthy Men
Harman, S. M., Metter, E. J., Tobin, J. D., Pearson, J., & Blackman, M. R. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.2.7219 · Cited by 2,760
Feldman, H. A., Longcope, C., Derby, C. A., Johannes, C. B., Araujo, A. B., Coviello, A. D., Bremner, W. J., & McKinlay, J. B. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.2.8201 · Cited by 1,861
Self-citationSattar, N., Gaw, A., Scherbakova, O., Ford, I., O’Reilly, D. S. J., Haffner, S. M., Isles, C., Macfarlane, P. W., Packard, C. J., Cobbe, S. M., et al. (2003) · Circulation · doi:10.1161/01.cir.0000080897.52664.94 · Cited by 1,506
Epidemiology: Beyond the Basics
Szklo, M., & Nieto, F. J. (1999) · Cited by 1,441
Onset of NIDDM occurs at Least 4–7 yr Before Clinical Diagnosis
Harris, M. I., Klein, R., Welborn, T. A., & Knuiman, M. W. (1992) · Diabetes Care · doi:10.2337/diacare.15.7.815 · Cited by 1,306
Laaksonen, D. E., Niskanen, L., Punnonen, K., Nyyssönen, K., Tuomainen, T.-P., Valkonen, V.-P., Salonen, R., & Salonen, J. T. (2004) · Diabetes Care · doi:10.2337/diacare.27.5.1036 · Cited by 920
The Metabolic Syndrome as Predictor of Type 2 Diabetes
Lorenzo, C., Okoloise, M., Williams, K., Stern, M. P., & Haffner, S. M. (2003) · Diabetes Care · doi:10.2337/diacare.26.11.3153 · Cited by 800
Flagged first, then by citations
4 of the 47 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Matthews, 1996, Statistics notes, Interaction 2: compare effect sizes not P values. Br Med J, 313, 808
Cited by
Sorted by citations
Items 501–560 of 560
Circulating steroid hormones in prostate carcinogenesis. Part 1 – Androgens
Fiet, J., & Giton, F. (2010) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci.2010.040
Ianas, O. (2009) · Acta Endocrinologica (Bucharest) · doi:10.4183/aeb.2009.447
Wang, C., Nieschlag, E., RONALD, S. S., Behre, H. M., WAYNE, J. H., LOUIS, J. G., JEAN, M. K., Legros, J., Lunenfeld, B., Morales, Á., et al. (2010) · Obesity and metabolism · doi:10.14341/2071-8713-5211
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-citationEarly markers of metabolic syndrome in nonoverweight, middle-aged men
Liu, P. Y., & Handelsman, D. J. (2006) · Nature Clinical Practice Urology · doi:10.1038/ncpuro0599
Der Link zwischen erektiler Dysfunktion und metabolischem Syndrom - Möglichkeiten der Behandlung
Yassin, A. A., & Saad, F. (2008) · Journal für Kardiologie (Krause & Pachernegg GmbH)
Testicular cancer; gonadal, sexual and psychological aspects of the disease and its treatment.
Eberhard, J. (2009) · Lund University Publications (Lund University)
Effect of sacral nerve electrostimulation on sex dysfunction in male rats with spinal cord injury
Wu, J. (2013) · Asian Biomedicine · doi:10.5372/abm.v6i6.14333
Testosterone and frailty in elderly men
Emmelot‐Vonk, M. H. (2009) · Utrecht University Repository (Utrecht University)
Testerone Replacement Therapy for Men with Metabolic Syndrome
Soedjono, J. (2011)
Fibromialgia e síndrome metabólica: alterações neuroendócrinas em comum
Gagliardi, A., Alambert, P. A., dos Santos, L. R., Hime, R. C., Filho, E. R. A., Póvoa, F. F., & Contenças, A. C. D. S. (2009) · Diagn. tratamento
Roberge, C., Carpentier, A. C., Langlois, M., Baillargeon, J., Ardilouze, J., & Gallo‐Payet, N. (2007)
Возрастной гипогонадизм у мужчин с метаболическим синдромом
Mskhalaya, G., & Yu, K. S. (2010) · CyberLeninK (CyberLeninka)
Sabet, Z. (2012) · Acta Endocrinologica (Bucharest) · doi:10.4183/aeb.2012.453
Review Article Andropause: Current concepts
Singh, P. (2013)
Late-Onset Hypogonadism in Male Patients Over 60 Years of Age with Metabolic Syndrome
Kara, E., Çelik, Ö., Kadıoğlu, A., & Kadıoğlu, P. (2013) · Endocrinology research and practice. · doi:10.4274/tjem.2104
Мишустина, Е. Н., Smirnova, E. N., & Vagner, E. A. (2011) · CyberLeninK (CyberLeninka)
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)
Mora, M. (2015) · Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona)
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
Khalaf, B. H., Abdulridha, M. K., Tuma, W. E., & Najim, H. D. (2015) · Pharmaceutical and Biosciences Journal · doi:10.20510/ukjpb/3/i2/89348
Schneider, H. J., Sievers, C., Klotsche, J., Lehnert, H., Wïttchen, H., & Stalla, G. K. (2008) · 10th European Congress of Endocrinology
Antiaging and Performance-Enhancing Drugs
Yaseen, Z. (2018) · Springer eBooks · doi:10.1007/978-3-319-16223-2_6
Prostate Diseases and the Metabolic Syndrome
Haghsheno, M. (2015) · Gothenburg University Publications Electronic Archive (Gothenburg University)
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)
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
Low Total Testosterone-Component of Metabolic Syndrome
Goel, P., & Popa, A. R. (2019) · Romanian Journal of Diabetes Nutrition and Metabolic Diseases · doi:10.2478/rjdnmd-2019-0015
Luchytskyi, V. Y., & Лучицький, Є. В. (2018) · Family Medicine · doi:10.30841/2307-5112.6.2018.169885
Snyder, P. J. (2013) · Elsevier eBooks · doi:10.1016/b978-1-4557-2758-2.00016-0
Wu, J., Hu, J., Lü, H., Liao, Q., Wang, J., Wu, M., Sun, C., & Kang, M. F. (2012) · Asian Biomedicine · doi:10.5372/1905-7415.0606.136
Masum, M. D., Talukder, R. M., Maksud, S. I., Haque, E., Khanam, J., Hossain, S., & Talukder, S. M. (2020) · International Journal of Advances in Medicine · doi:10.18203/2349-3933.ijam20205038
Pakhomova, A. V., Pershina, О. V., Nebolsin, V. E., Ermakova, N. N., Krupin, V. A., Sandrikina, L. A., Pan, E. S., Widera, D., Дыгай, А. М., & Skurikhin, Е. G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.562358
Shlyakhova, N. V., Турчина, С. И., & Kosovtsova, G. V. (2020) · Endokrynologia · doi:10.31793/1680-1466.2020.25-4.310
The anti-inflammatory effects of testosterone on atherosclerosis
Bateman, L. (2020) · Sheffield Hallam University · doi:10.7190/shu-thesis-00351 · Cited by 1
Testosterone Correlation with Low and High Density Lipoprotein in Male Type 2 Diabetics
Laghari, M., Murtaza, S., Talpur, Z., Hamid, M., Adnan, F., & Ahmed, A. (2021) · Journal of Pharmaceutical Research International · doi:10.9734/jpri/2021/v33i40b32279
(2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3281de7489
Mirone, V. G., & Rocca, R. L. (2020) · Springer eBooks · doi:10.1007/978-3-030-28599-9_9
Benson, M. C. (2008) · The Journal of Urology · doi:10.1016/j.juro.2008.06.144
Muñoz, G. E., & Коган, М. И. (2017) · Oxford University Press eBooks · doi:10.1093/med/9780190466268.003.0010
Seneszenz und Altershypogonadismus
Rolf, C., Zitzmann, M., & Nieschlag, E. (2023) · Springer Reference Medizin · doi:10.1007/978-3-662-61904-9_25-1
Zolla, L. (2023) · Metabolites · doi:10.3390/metabo13060681
Seneszenz und Altershypogonadismus
Rolf, C., Zitzmann, M., & Nieschlag, E. (2023) · Springer Reference Medizin · doi:10.1007/978-3-662-61901-8_25
The Impact of Male Obesity on Sex Hormones
Moreira, E. C. N. D. G., Machado, D. A. J. F., Delfino, B. A., Matos, G. O. A., & Zaccarelli-Marino, M. A. (2023) · Journal of Obesity and Weight-loss Medication · doi:10.23937/2572-4010.1510048
Kuzmina, L. P., Kislyakova, A. A., Kolyaskina, M. M., Khotuleva, A. G., & Anokhin, N. N. (2025) · Russian Journal of Occupational Health and Industrial Ecology · doi:10.31089/1026-9428-2025-65-7-440-446
Wang, J. H., Liang, D.-Q., Yang, T.-T., Liu, Z., Li, S., Hu, J., & Wang, Z.-Y. (2025) · doi:10.2196/preprints.86480
Takeshima, Y., Yamada, Y., Teshima, T., Fujimura, T., Kakutani, S., Hakozaki, Y., Kimura, N., Akiyama, Y., Sato, Y., Kawai, T., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14539013
Low Testosterone Level in Men and Quality of Life
(2012) · SpringerReference · doi:10.1007/springerreference_73481
Tienforti, D., Antolini, F., Spagnolo, L., Capuano, C., Perfetto, E., Baroni, M. G., & Barbonetti, A. (2025) · Endocrine · doi:10.1007/s12020-025-04532-0
Garifalos, F., Menafra, D., de Angelis, C., Larocca, A., Virgolesi, M., Aprano, S., Luca, V. D., Rea, T., Attaianese, E., Perillo, M., et al. (2026) · Frontiers in Reproductive Health · doi:10.3389/frph.2025.1691309
The Aging Male Endocrine System: Clinical Insights into Andropause Management
Garg, R. (2026) · Journal of The Indian Academy of Geriatrics · doi:10.4103/jiag.jiag_83_25
Saffati, G., Riveros, C. A., Obuekwe, O., Howell, S., Deebel, N. A., Kohn, T. P., & Muthigi, A. (2026) · International Journal of Impotence Research · doi:10.1038/s41443-026-01292-x
Menafra, D., de Angelis, C., Garifalos, F., Chiodini, P., Verde, N., Piscopo, M., Galdiero, G., Fraia, D. A. D., Mazzarella, A., Paola, N. D., et al. (2026) · Journal of Endocrinological Investigation · doi:10.1007/s40618-026-03037-5
Kemp, T. (2014) · UpSpace Institutional Repository (University of Pretoria)
Genetics of Metabolic Syndrome and Genetic Lipodystrophies
JOY, T. R., & Hegele, R. A. (2009) · Springer eBooks · doi:10.1007/978-0-387-09718-3_5
Beason, T. S. (2010) · D-Scholarship@Pitt (University of Pittsburgh)
Metadata
- Authors
- Kupelian, V., Page, S. T., Araujo, A. B., Travison, T. G., Bremner, W. J., & McKinlay, J. B.
- Affiliations
- New England Research Institutes (US)
- University of Washington (US)
- New England Research Institutes (V.K., A.B.A., T.G.T., J.B.M.), Watertown, Massachusetts 02472
- Corresponding author
- McKinlay, John B.
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2006-03-01
- Volume
- 91
- Issue
- 3
- Pages
- 843-850
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2155165820
- Cited by
- 561
- References
- 47
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 9 · 2023: 11 · 2022: 15 · 2021: 11 · 2020: 16 · 2019: 20 · 2018: 25 · 2017: 24 · 2016: 18 · 2015: 27 · 2014: 29 · 2013: 39 · 2012: 51
- FWCI
- 40.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- World Health Organization
- National Institute on Aging (AG 04763, K23AG027238)
- 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 › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- metabolic syndrome, sex hormone-binding globulin, total testosterone, androgen deficiency, cardiovascular risk, middle-aged men, body mass index, Massachusetts Male Aging Study, risk prediction
- MeSH terms
- Adult, Aged, Androgens, Body Weight, Cardiovascular Diseases, Humans, Male, Massachusetts, Middle Aged, Reference Values, Sex Hormone-Binding Globulin, Socioeconomic Factors, Testosterone, Cohort Studies, Metabolic Syndrome
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