Clinical correlates of sex steroids and gonadotropins in men over the late adulthood: the Framingham Heart Study
Open accessAbstract
Low serum concentrations of sex steroids and gonadotropins in men have been associated with increased cardiometabolic risk and mortality, but the clinical correlates of these hormones in men over late adulthood are less clearly understood. We analysed up to five serial measurements of total testosterone (TT), dehydroepiandrosterone sulphate (DHEAS), follicle stimulating hormone (FSH), luteinizing hormone (LH) and total estradiol (EST) in older men in the original cohort of the Framingham Heart Study to determine the short- (2-years; 1,165 person-observations in 528 individuals) and long-term (up to 10-years follow-up; 2520 person-observations in 835 individuals with mean baseline age: 71.2 years) clinical correlates of these sex steroids and gonadotropins using multilevel modelling and Generalized Estimating Equations. Age, body mass index and pre-existing type 2 diabetes were inversely related to long-term TT concentrations, whereas higher systolic blood pressure showed a positive association. Furthermore, age and pre-existing cardiovascular disease (CVD) were inversely associated and HDL cholesterol concentrations positively associated with long-term DHEAS concentrations respectively. Analyses of short-term changes revealed age was inversely related to DHEAS, but positively related to FSH and LH concentrations. Our community-based study identified modifiable correlates of decreasing TT and DHEAS concentrations in elderly men, suggesting that maintenance of a low CVD risk factor burden may mitigate the age-related decline of these hormones over the late adulthood.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 large prospective observational studies, weight gain and development of comorbidities were consistently associated with an acceleration of the age-related decline in testosterone levels.
“In large prospective observational studies, weight gain and development of comorbidities were consistently associated with an acceleration of the age-related decline in testosterone levels (17, 18).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [18]
In the Framingham Heart Study, a high cardiovascular disease risk factor burden markedly increased the age-related testosterone decline.
“In the Framingham Heart Study, a high cardiovascular disease risk factor burden markedly increased the age-related testosterone decline (18).”
From A Perspective on Middle-Aged and Older Men With Functional Hypogonadism: Focus on Holistic Management (2017) · cites this paper as [18]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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 · see citing works
Epidemiological approaches to heart disease: the Framingham study
Dawber, T. R., Meadors, G. F., & Moore, F. E. (1951) · American Journal of Public Health and the Nations Health · doi:10.2105/ajph.41.3.279 · Cited by 2,148 · see citing works
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 · see citing works
Self-citationAN INVESTIGATION OF CORONARY HEART DISEASE IN FAMILIES
Kannel, W. B., Feinleib, M., McNAMARA, P. M., Garrison, R. J., & Castelli, W. P. (1979) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a112813 · Cited by 1,635 · see citing works
Adverse Events Associated with Testosterone Administration
Basaria, S., Coviello, A. D., Travison, T. G., Storer, T. W., Farwell, W. R., Jette, A. M., Eder, R., Tennstedt, S., Ulloor, J., Zhang, A., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa1000485 · Cited by 1,494 · see citing works
Self-citationRosner, W., Auchus, R. J., Azziz, R., Sluss, P. M., & Raff, H. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1864 · Cited by 1,176 · see citing works
Gray, A., Feldman, H. A., McKinlay, J. B., & Longcope, C. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-73-5-1016 · Cited by 1,104 · see citing works
Wu, F. C. W., Tajar, A., Pye, S. R., Silman, A. J., Finn, J. D., O'Neill, T. W., Bartfai, G., Casanueva, F., Forti, G., Giwercman, A., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1972 · Cited by 939 · see citing works
Morley, J. E., Kaiser, F. E., Perry, H. M., Patrick, P., Morley, P. M. K., Stauber, P. M., Vellas, B., Baumgartner, R. N., & Garry, P. J. (1997) · Metabolism · doi:10.1016/s0026-0495(97)90057-3 · Cited by 830 · see citing works
Low Serum Testosterone and Mortality in Older Men
Laughlin, G. A., Barrett-Connor, E., & Bergstrom, J. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1792 · Cited by 798 · see citing works
Khaw, K.-T., Dowsett, M., Folkerd, E., Bingham, S., Wareham, N., Luben, R., Welch, A., & Day, N. (2007) · Circulation · doi:10.1161/circulationaha.107.719005 · Cited by 743 · see citing works
A prospective study of dehydroepiandrosterone sulfate, mortality and cardiovascular disease.
Barrett-Connor, E., Khaw, K.-T., & Yen, S. S. C. (1986) · New England Journal of Medicine · doi:10.1056/nejm198612113152405 · Cited by 681 · see citing works
Kupelian, V., Page, S. T., Araujo, A. B., Travison, T. G., Bremner, W. J., & McKinlay, J. B. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1326 · Cited by 561 · see citing works
Automated enzymatic standardized lipid analyses for plasma and lipoprotein fractions
McNamara, J. R., & Schaefer, E. J. (1987) · Clinica Chimica Acta · doi:10.1016/0009-8981(87)90188-4 · Cited by 524 · see citing works
Vermeulen, A. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.5.1821 · Cited by 455 · see citing works
Travison, T. G., Araujo, A. B., Kupelian, V., O’Donnell, A. B., & McKinlay, J. B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1859 · Cited by 410 · see citing works
Type 2 diabetes mellitus and testosterone: a meta-analysis study: Type 2 diabetes and testosterone
Corona, G., Monami, M., Rastrelli, G., Aversa, A., Sforza, A., Lenzi, A., Forti, G., Mannucci, E., & Maggi, M. (2011) · International Journal of Andrology · doi:10.1111/j.1365-2605.2010.01117.x · Cited by 370 · see citing works
Endogenous sex hormones and cardiovascular disease in men. A prospective population-based study.
Barrett-Connor, E. L., & Khaw, K. (1988) · Circulation · doi:10.1161/01.cir.78.3.539 · Cited by 367 · see citing works
Zmuda, J. M., Cauley, J. A., Kriska, A. M., Glynn, N. W., Gutai, J. P., & Kuller, L. H. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009326 · Cited by 362 · see citing works
Endogenous sex hormones in men aged 40-80 years
Muller, M., den Tonkelaar, I., Thijssen, J., Grobbee, D., & van der Schouw, Y. (2003) · European Journal of Endocrinology · doi:10.1530/eje.0.1490583 · Cited by 346 · see citing works
A Population-Level Decline in Serum Testosterone Levels in American Men
Travison, T. G., de Araújo, A. B., O’Donnell, A. B., Kupelian, V. A., & McKinlay, J. B. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1375 · Cited by 335 · see citing works
Derby, C. A., Zilber, S., Brambilla, D., Morales, K. H., & McKinlay, J. B. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02560.x · Cited by 315 · see citing works
Haring, R., Völzke, H., Steveling, A., Krebs, A., Felix, S. B., Schöfl, C., Dörr, M., Nauck, M., & Wallaschofski, H. (2010) · European Heart Journal · doi:10.1093/eurheartj/ehq009 · Cited by 310 · see citing works
Self-citationAmin, S., Zhang, Y., Sawin, C. T., Evans, S. R., Hannan, M. T., Kiel, D. P., Wilson, P. W. F., & Felson, D. T. (2000) · Annals of Internal Medicine · doi:10.7326/0003-4819-133-12-200012190-00010 · Cited by 290 · see citing works
Sex Steroids and All-Cause and Cause-Specific Mortality in Men
de Araújo, A. B. (2007) · Archives of Internal Medicine · doi:10.1001/archinte.167.12.1252 · Cited by 272 · see citing works
Leifke, E., Gorenoi, V., Wichers, C., Von Zur Mühlen, A., Von Büren, E., & Brabant, G. (2000) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2000.01159.x · Cited by 262 · see citing works
Svartberg, J., Midtby, M., Bonaa, K., Sundsfjord, J., Joakimsen, R., & Jorde, R. (2003) · European Journal of Endocrinology · doi:10.1530/eje.0.1490145 · Cited by 257 · see citing works
Relationship of sex hormones to lipids and lipoproteins in nondiabetic men
Haffner, S. M., Mykkänen, L. M., Valdez, R. A., & Katz, M. S. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.6.8263149 · Cited by 236 · see citing works
Laaksonen, D. E., Niskanen, L., Punnonen, K., Nyyssönen, K., Tuomainen, T.-P., Valkonen, V.-P., & Salonen, J. T. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0970 · Cited by 230 · see citing works
Endogenous Sex Hormones and Cardiovascular Disease in Men
Muller, M., van der Schouw, Y. T., Thijssen, J. H. H., & Grobbee, D. E. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030611 · Cited by 210 · see citing works
Andersson, A., Jensen, T. K., Juul, A., Petersen, J. H., Jørgensen, T., & Skakkebæk, N. E. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2633 · Cited by 174 · see citing works
Low testosterone levels are associated with carotid atherosclerosis in men
Svartberg, J. B., von Mühlen, D. G., Mathiesen, E. B., Joakimsen, O., Bønaa, K. H., & Stensland-Bugge, E. (2006) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2006.01637.x · Cited by 163 · see citing works
Mohr, B. A., Bhasin, S., Link, C. L., O’Donnell, A. B., & McKinlay, J. B. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02241 · Cited by 163 · see citing works
Self-citationPrediction of Metabolic Syndrome by Low Serum Testosterone Levels in Men
Haring, R., Völzke, H., Felix, S. B., Schipf, S., Dörr, M., Rosskopf, D., Nauck, M. A., Schöfl, C., & Wallaschofski, H. (2009) · Diabetes · doi:10.2337/db09-0031 · Cited by 152 · see citing works
Self-citationVikan, T., Schirmer, H., Njølstad, I., & Svartberg, J. (2010) · European Journal of Endocrinology · doi:10.1530/eje-09-0943 · Cited by 151 · cited 6× · see citing works
“, 2009) or type 2 diabetes (Vikan et al., 2010; Schipf et al., 2011), whereas these conditions are also associated with decreased TT concentrations (Laaksonen et al.”
InfluentialEndogenous sex hormones and ischemic heart disease in men. The Caerphilly prospective study.
YARNELL, J. W. G., Beswick, A. D., Sweetnam, P. M., & Riad-Fahmy, D. (1993) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.13.4.517 · Cited by 104 · see citing works
Haring, R., Ittermann, T., Völzke, H., Krebs, A., Zygmunt, M., Felix, S. B., Grabe, H. J., Nauck, M. A., & Wallaschofski, H. (2010) · The Aging Male · doi:10.3109/13685538.2010.487553 · Cited by 101 · see citing works
Self-citationBaltimore Longitudinal Study of Aging
Salkind, N. J. (2005) · Encyclopedia of Human Development · doi:10.4135/9781412952484.n73 · Cited by 99 · see citing works
Lapauw, B., Goemaere, S., Zmierczak, H., Pottelbergh, I. V., Mahmoud, A., Taes, Y., Bacquer, D. D., Vansteelandt, S., & Kaufman, J. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0873 · Cited by 93 · see citing works
Haring, R., Baumeister, S. E., Völzke, H., Dörr, M., Felix, S. B., Kroemer, H. K., Nauck, M. A., & Wallaschofski, H. (2010) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1097/hjr.0b013e32833c1a8d · Cited by 89 · see citing works
Self-citationVikan, T., Johnsen, S. H., Schirmer, H., Njølstad, I., & Svartberg, J. B. (2009) · European Journal of Epidemiology · doi:10.1007/s10654-009-9322-2 · Cited by 87 · see citing works
Mendelson, J. H., Sholar, M. B., Mutschler, N. H., Jaszyna-Gasior, M., Goletiani, N. V., Siegel, A. J., & Mello, N. K. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.052928 · Cited by 81 · see citing works
Torkler, S., Wallaschofski, H., Baumeister, S. E., Völzke, H., Dörr, M., Felix, S. B., Rettig, R., Nauck, M. A., & Haring, R. (2010) · The Aging Male · doi:10.3109/13685538.2010.529194 · Cited by 81 · see citing works
Self-citationAre declining testosterone levels a major risk factor for ill-health in aging men?
Yeap, B. B. (2008) · International Journal of Impotence Research · doi:10.1038/ijir.2008.60 · Cited by 75 · see citing works
Metabolic and cardiovascular effects of androgen deprivation therapy
Hakimian, P., Blute, M., Kashanian, J. A., Chan, S. M., Silver, D. A., & Shabsigh, R. (2008) · British Journal of Urology · doi:10.1111/j.1464-410x.2008.07933.x · Cited by 74 · see citing works
Schipf, S., Haring, R., Friedrich, N., Nauck, M. A., Lau, K., Alte, D., Stang, A., Völzke, H., & Wallaschofski, H. (2010) · The Aging Male · doi:10.3109/13685538.2010.524955 · Cited by 52 · see citing works
Self-citationCappola, A. R., O’Meara, E. S., Guo, W., Bartz, T. M., Fried, L. P., & Newman, A. B. (2009) · The Journals of Gerontology Series A · doi:10.1093/gerona/glp129 · Cited by 46 · see citing works
Yasui, T., Uemura, H., Irahara, M., Arai, M., Kojimahara, N., Okabe, R., Ishii, Y., Tashiro, S.-I., & Satō, H. (2008) · Clinica Chimica Acta · doi:10.1016/j.cca.2008.08.006 · Cited by 33 · see citing works
Sanders, J. L., Boudreau, R. M., Cappola, A. R., Arnold, A. M., Robbins, J. A., Cushman, M., & Newman, A. B. (2010) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.02724.x · Cited by 32 · see citing works
Decreasing Testosterone with Increasing Age: More Factors, More Questions
Snyder, P. J. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0922 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Schipf S Haring R Friedrich N Nauck MA Lau K Alte D Stang A Volzke H Wallaschofski H 2010 Low Total Testosterone is Associated with Increased Risk of Incident Type 2 Diabetes Mellitus in Men: Results from the Study of Health in Pomerania (SHIP) Aging Male 21039324
Cited by
Sorted by citations
Grossmann, M., & Matsumoto, A. M. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3580 · Cited by 246 · see citing works
Longitudinal changes in testosterone over five years in community-dwelling men
Shi, Z., Araujo, A. B., Martin, S., O'Loughlin, P., & Wittert, G. A. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3842 · Cited by 165 · see citing works
- Authors
- Haring, R., Xanthakis, V., Coviello, A., Sullivan, L., Bhasin, S., Wallaschofski, H., Murabito, J. M., & Vasan, R. S.
- Affiliations
- Universitätsmedizin Greifswald (DE)
- General Department of Preventive Medicine (VN)
- Boston University (US)
- Corresponding author
- Haring, R.
- Vasan, R. S.
- Venue
- International Journal of Andrology
- Publisher
- Wiley
- Published
- 2012-05-29
- Volume
- 35
- Issue
- 6
- Pages
- 775-782
- ISSN
- 0105-6263 (ISSN-L)
- 1365-2605
- PMC
- PMC3434249
- OpenAlex
- W2099456194
- Cited by
- 22
- References
- 50
- Citations by year
- 2026: 1 · 2022: 1 · 2021: 1 · 2018: 3 · 2017: 1 · 2016: 2 · 2015: 5 · 2014: 4 · 2013: 4
- FWCI
- 3.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- International Journal of Andrology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (n01hc25195-41-0-1)
- National Heart, Lung, and Blood Institute (N01‐HC25195, N01-HC-025195)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK092938)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Menopause: Health Impacts and Treatments
- Keywords
- sex steroids, gonadotropins, old age, older men, total testosterone, dehydroepiandrosterone sulfate, follicle-stimulating hormone, luteinizing hormone, estradiol, cardiovascular disease, cardiometabolic risk, HDL cholesterol, systolic blood pressure, type 2 diabetes, Framingham Heart Study
- MeSH terms
- Aged, Cardiovascular Diseases, Gonadotropins, Humans, Longitudinal Studies, Male, Massachusetts, Middle Aged, Gonadal Steroid Hormones
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