Associations between sex steroids and the development of metabolic syndrome: A longitudinal study in European men

Journal of Clinical Endocrinology and Metabolism

Volumn 100, Issue 4, 2015, Pages 1396-1404

  Antonio, Leen ^a,b,p   Wu, Frederick C W ^c,d,p   O'Neill, Terence W ^e,f,p   Pye, Stephen R ^e,p   Carter, Emma L ^c   Finn, Joseph D ^c,p   Rutter, Martin K ^c,f,p   Laurent, Michaël R ^a   Huhtaniemi, Ilpo T ^g,p   Han, Thang S ^h   Lean, Michael E J ⁱ   Keevil, Brian G ^f   Pendleton, Neil ^c   Rastrelli, Giulia ^j   Forti, Gianni ^j,p   Bartfai, Gyorgy ^k,p   Casanueva, Felipe F ^l,q   Kula, Krzysztof ^m,p   Punab, Margus ^n,p   Giwercman, Aleksander ^o,p   Claessens, Frank ^a   Decallonne, Brigitte ^a,b   Vanderschueren, Dirk ^a,b,p   Petrone, Luisa ^p   Corona, Giovanni ^p   Borghs, Herman ^p   Slowikowska Hilczer, Jolanta ^p   Walczak Jedrzejowska, Renata ^p   Silman, Alan ^p   Steer, Philip ^p   Castro, Ana I ^q   Földesi, Imre ^p   Fejes, Imre ^p   Korrovitz, Paul ^p   more..

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d MANCHESTER ROYAL INFIRMARY   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h ASHFORD AND ST PETER'S HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

ⁱ UNIVERSITY OF GLASGOW   (United Kingdom)

^j UNIVERSITY OF FLORENCE   (Italy)

^k UNIVERSITY OF SZEGED   (Hungary)

^l UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^m MEDICAL UNIVERSITY OF LODZ   (Poland)

ⁿ TARTU UNIVERSITY CLINICS   (Estonia)

^o LUND UNIVERSITY HOSPITAL   (Sweden)

^p Tartu University Clinics ^*  (Estonia)

^q Santiago College   (Chile)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; SEX HORMONE; SEX HORMONE BINDING PROTEIN; TESTOSTERONE;

ADULT; AGED; ARTICLE; BODY COMPOSITION; BODY FAT; BODY MASS; CARDIOMETABOLIC RISK; COHORT ANALYSIS; COMMUNITY LIVING; CONTROLLED STUDY; DISEASE ASSESSMENT; DISEASE ASSOCIATION; ESTRADIOL BLOOD LEVEL; EUROPEAN; FOLLOW UP; HIGH RISK POPULATION; HOMEOSTASIS MODEL ASSESSMENT OF INSULIN RESISTANCE; HUMAN; INSULIN RESISTANCE; LIQUID CHROMATOGRAPHY; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MASS FRAGMENTOGRAPHY; METABOLIC SYNDROME X; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTECTION; TESTOSTERONE BLOOD LEVEL; AGING; BLOOD; EUROPE; INCIDENCE; METABOLISM; MIDDLE AGED;

ADULT; AGED; AGING; BODY COMPOSITION; BODY MASS INDEX; EUROPE; GONADAL STEROID HORMONES; HUMANS; INCIDENCE; INSULIN RESISTANCE; LONGITUDINAL STUDIES; MALE; METABOLIC SYNDROME X; MIDDLE AGED;

EID: 84927648769     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2014-4184     Document Type: Article

References (42)

1. Cornier MA, Dabelea D, Hernandez TL, et al. The metabolic syndrome. Endocrine Rev. 2008;29:777-822.
2. Gami AS, Witt BJ, Howard DE, et al. Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol. 2007;49:403-414.
3. Scuteri A, Laurent S, Cucca F, et al. Metabolic syndrome across Europe: different clusters of risk factors. European J Preventive Cardiol. 2014; doi: 10.1177/2047487314525529.
4. Rodriguez A, Muller DC, Metter EJ, et al. Aging, and rogens, and the metabolic syndrome in a longitudinal study of aging. J Clin Endocrinol Metab. 2007;92:3568-3572.
5. Laaksonen DE, Niskanen L, Punnonen K, et al. Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care. 2004;27:1036-1041.
6. Li C, Ford ES, Li B, Giles WH, Liu S. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care. 2010;33:1618-1624.
7. Kupelian V, Page ST, Araujo AB, Travison TG, Bremner WJ, McKinlay JB. Low sex hormone-binding globulin, total testosterone, and symptomatic and rogen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab. 2006;91:843-850.
8. Bhasin S, Jasjua GK, Pencina M, et al. Sex hormone-binding globulin, but not testosterone, is associated prospectively and independently with incident metabolic syndrome in men: the Framingham heart study. Diabetes care. 2011;34:2464-2470.
9. Haring R, Volzke H, Spielhagen C, Nauck M, Wallaschofski H. The role of sex hormone-binding globulin and testosterone in the risk of incident metabolic syndrome. Eur J Prev Cardiol. 2013;20:1061-1068.
10. de Ronde W, van der Schouw YT, Pierik FH, et al. Serum levels of sex hormone-binding globulin (SHBG) are not associated with lower levels of non-SHBG-bound testosterone in male newborns and healthy adult men. Clinical Endocrinol. 2005;62:498-503.
11. Kaufman JM, Vermeulen A. The decline of and rogen levels in elderly men and its clinical and therapeutic implications. Endocrine Rev. 2005;26:833-876.
12. Finkelstein JS, Lee H, Burnett-Bowie SA, et al. Gonadal steroids and body composition, strength, and sexual function in men. New Engl J Med. 2013;369:1011-1022.
13. Gates MA, Mekary RA, Chiu GR, Ding EL, Wittert GA, Araujo AB. Sex steroid hormone levels and body composition in men. J Clin Endocrinol Metab. 2013;98:2442-2450.
14. Lee DM, O'Neill TW, Pye SR, et al. The European Male Ageing Study (EMAS): design, methods and recruitment. Int J Andrology. 2009;32:11-24.
15. Siri WE. Body composition from fluid spaces and density: Analysis of methods. In: Brozek J, Henzchel A, eds. Techniques for Measuring Body Composition. Washington, National Academy of Sciences; 1961:224-244.
16. Reuben DB, Siu AL. An objective measure of physical function of elderly outpatients. The Physical Performance Test. J Am Geriatrics Soc. 1990;38:1105-1112.
17. Gallagher LM, Owen LJ, Keevil BG. Simultaneous determination of and rostenedione and testosterone in human serum by liquid chromatographytandem mass spectrometry. Ann Clin Biochem. 2007;44:48-56.
18. Labrie F, Bélanger A, Bélanger P, et al. Androgen glucuronides, instead of testosterone, as the new markers of and rogenic activity in women. J Steroid Biochem Mol Biol. 2006;99:182-188.
19. Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999;84:3666-3672.
20. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419.
21. Verschueren S, Gielen E, O'Neill TW, et al. Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporosis Int. 2013;24:87-98.
22. Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640-1645.
23. Hsu B, Cumming RG, Naganathan V, et al. Associations between circulating reproductive hormones and SHBG and prevalent and incident metabolic syndrome in community-dwelling older men: the Concord Health and Ageing in Men Project. J Clin Endocrinol Metab. 2014;99:E2686-E2691.
24. Monroe AK, Dobs AS. The effect of and rogens on lipids. Curr Opin Endocrinol, Diabetes, Obes. 2013;20:132-139.
25. Stellato RK, Feldman HA, Hamdy O, Horton ES, McKinlay JB. Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts male aging study. Diabetes Care. 2000;23:490-494.
26. Wu FC, Tajar A, Pye SR, et al. Hypothalamic-pituitary-testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European Male Aging Study. J Clin Endocrinol Metab. 2008;93:2737-2745.
27. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunology. 2011;29:415-445.
28. Shahani S, Braga-Basaria M, Basaria S. Androgen deprivation therapy in prostate cancer and metabolic risk for atherosclerosis. J Clin Endocrinol Metab. 2008;93:2042-2049.
29. Corona G, Rastrelli G, Monami M, et al. Body weight loss reverts obesity-associated hypogonadotropic hypogonadism: a systematic review and meta-analysis. Eur J Endocrinol. 2013;168:829-843.
30. Wang C, Jackson G, Jones TH, et al. Low testosterone associated with obesity and the metabolic syndrome contributes to sexual dysfunction and cardiovascular disease risk in men with type 2 diabetes. Diabetes Care. 2011;34:1669-1675.
31. Huhtaniemi IT, Tajar A, Lee DM, et al. Comparison of serum testosterone and estradiol measurements in 3174 European men using platform immunoassay and mass spectrometry; relevance for the diagnostics in aging men. Eur J Endocrinol. 2012;166:983-991.
32. de Ronde W, Pols HA, van Leeuwen JP, de Jong FH. The importance of oestrogens in males. Clinical Endocrinol. 2003;58:529-542.
33. Callewaert F, Venken K, Ophoff J, et al. Differential regulation of bone and body composition in male mice with combined inactivation of and rogen and estrogen receptor-alpha. FASEB J. 2009;23:232-240.
34. Vanderschueren D, Laurent MR, Claessens F, et al. Sex steroid actions in male bone. Endocrine Rev. 2014;35:906-960.
35. Jones ME, McInnes KJ, Boon WC, Simpson ER. Estrogen and adiposity-utilizing models of aromatase deficiency to explore the relationship. J Steroid Biochem Mol Biol. 2007;106:3-7.
36. Muller M, Grobbee DE, den Tonkelaar I, Lamberts SW, van der Schouw YT. Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab. 2005;90:2618-2623.
37. Maggio M, Lauretani F, Ceda GP, et al. Estradiol and metabolic syndrome in older italian men: The InCHIANTI Study. J Andrology. 2010;31:155-162.
38. Cheng KH, Huang SP, Huang CN, et al. The impact of estradiol and 1, 25 (OH) 2D3 on metabolic syndrome in middle-aged Taiwanese males. PloS one. 2013;8:e60295.
39. Williams G. Aromatase up-regulation, insulin and raised intracellular oestrogens in men, induce adiposity, metabolic syndrome and prostate disease, via aberrant ER-β and GPER signalling. Mol Cellular Endocrinol. 2012;351:269-278.
40. Phillips GB, Jing T, Heymsfield SB. Relationships in men of sex hormones, insulin, adiposity, and risk factors for myocardial infarction. Metabolism. 2003;52:784-790.
41. Rosner W, Auchus RJ, Azziz R, Sluss PM, Raff H. Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab. 2007;92:405-413.
42. Ohlsson C, Nilsson ME, Tivesten A, et al. Comparisons of immunoassay and mass spectrometry measurements of serum estradiol levels and their influence on clinical association studies in men. J Clin Endocrinol Metab. 2013;98:E1097-E1102.