Body composition, metabolic syndrome and testosterone in ageing men

International Journal of Impotence Research

Volumn 19, Issue 5, 2007, Pages 448-457

  Allan, C A ^a,b   Strauss, B J G ^c,d   McLachlan, R I ^a,b,c,d  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Andrology Australia   (Australia)

^c MONASH MEDICAL CENTRE   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Ageing; Body composition; Cardiovascular; Men; Metabolic; Testosterone

Indexed keywords

TESTOSTERONE;

AGING; BODY COMPOSITION; BODY FAT DISTRIBUTION; CARDIOVASCULAR RISK; HORMONAL THERAPY; HUMAN; INSULIN RELEASE; INSULIN RESISTANCE; METABOLIC SYNDROME X; OBESITY; PREVALENCE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; TESTOSTERONE BLOOD LEVEL;

AGING; ANDROGENS; BODY COMPOSITION; HUMANS; MALE; METABOLIC SYNDROME X; TESTOSTERONE;

EID: 34548458613     PISSN: 09559930     EISSN: 14765489     Source Type: Journal    
DOI: 10.1038/sj.ijir.3901552     Document Type: Review

References (98)

1. Gray A, Feldman HA, McKinlay JB, Longcope C. Age, disease, and changing sex hormone levels in middle-aged men: results of the Massachusetts Male Aging Study. J Clin Endocrinol Metab 1991; 73: 1016-1025.
2. Leifke E, Gorenoi V, Wichers C, Von Zur Muhlen A, Von Buren E, Brabant G. Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin Endocrinol (Oxf) 2000; 53: 689-695.
3. Feldman HA, Longcope C, Derby CA, Johannes CB, Araujo AB, Coviello AD et al. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 2002; 87: 589-598.
4. Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab 2001; 86: 724-731.
5. Travison TG, Araujo AB, Kupelian V, O'Donnell AB, McKinlay JB. The relative contributions of aging, health, and lifestyle factors to serum testosterone decline in men. J Clin Endocrinol Metab 2007; 92: 549-555.
6. Travison TG, Araujo AB, O'Donnell AB, Kupelian V, McKinlay JB. A population-level decline in serum testosterone levels in American men. J Clin Endocrinol Metab 2007; 92: 196-202.
7. Vermeulen A. The male climacterium. Ann Med 1993; 25: 531-534.
8. Vermeulen A, Goemaere S, Kaufman JM. Testosterone, body composition and aging. J Endocrinol Invest 1999; 22(5 Suppl): 110-116.
9. Bhasin S. Regulation of body composition by androgens. J Endocrinol Invest 2003; 26: 814-822.
10. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab 1996; 81: 4358-4365.
11. Snyder PJ, Peachey H, Berlin JA, Hannoush P, Haddad G, Dlewati A et al. Effects of testosterone replacement in hypogonadal men. J Clin Endocrinol Metab 2000; 85: 2670-2677.
12. Reed RL, Pearlmutter L, Yochum K, Meredith KE, Mooradian AD. The relationship between muscle mass and muscle strength in the elderly. J Am Geriatr Soc 1991; 39: 555-561.
13. van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab 2000; 85: 3276-3282.
14. Rolland-Cachera MF, Cole TJ, Sempe M, Tichet J, Rossignol C, Charraud A. Body mass index variations: centiles from birth to 87 years. Eur J Clin Nutr 1991; 45: 13-21.
15. Forbes GB, Reina JC. Adult lean body mass declines with age: some longitudinal observations. Metabolism 1970; 19: 653-663.
16. Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, Pichard C. Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur J Clin Nutr 2001; 55: 663-672.
17. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 2000; 89: 81-88.
18. Couillard C, Gagnon J, Bergeron J, Leon AS, Rao DC, Skinner JS et al. Contribution of body fatness and adipose tissue distribution to the age variation in plasma steroid hormone concentrations in men: the HERITAGE Family Study. J Clin Endocrinol Metab 2000; 85: 1026-1031.
19. Baumgartner RN, Rhyne RL, Garry PJ, Heymsfield SB. Imaging techniques and anatomical body composition in aging. J Nutr 1993; 123(2 Suppl): 444-448.
20. Seidell JC, Oosterlee A, Deurenberg P, Hautvast JG, Ruijs JH. Abdominal fat depots measured with computed tomography: effects of degree of obesity, sex, and age. Eur J Clin Nutr 1988; 42: 805-815.
21. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 2002; 76: 473-481.
22. Forbes GB. Longitudinal changes in adult fat-free mass: influence of body weight. Am J Clin Nutr 1999; 70: 1025-1031.
23. Wang ZM, Pierson Jr RN, Heymsfield SB. The five-level model: a new approach to organizing body-composition research. Am J Clin Nutr 1992; 56: 19-28.
24. Mauras N, Hayes V, Welch S, Rini A, Helgeson K, Dokler M et al. Testosterone deficiency in young men: marked alterations in whole body protein kinetics, strength, and adiposity. J Clin Endocrinol Metab 1998; 83: 1886-1892.
25. Smith MR, Finkelstein JS, McGovern FJ, Zietman AL, Fallon MA, Schoenfeld DA et al. Changes in body composition during androgen deprivation therapy for prostate cancer. J Clin Endocrinol Metab 2002; 87: 599-603.
26. Bhasin S, Storer TW, Berman N, Yarasheski KE, Clevenger B, Phillips J et al. Testosterone replacement increases fat-free mass and muscle size in hypogonadal men. J Clin Endocrinol Metab 1997; 82: 407-413.
27. Brodsky IG, Balagopal P, Nair KS. Effects of testosterone replacement on muscle mass and muscle protein synthesis in hypogonadal men - a clinical research center study. J Clin Endocrinol Metab 1996; 81: 3469-3475.
28. Bhasin S, Woodhouse L, Storer TW. Proof of the effect of testosterone on skeletal muscle. J Endocrinol 2001; 170: 27-38.
29. Bhasin S, Woodhouse L, Casaburi R, Singh AB, Bhasin D, Berman N et al. Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab 2001; 281: E1172-E1181.
30. Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med 1996; 335: 1-7.
31. Snyder PJ, Peachey H, Hannoush P, Berlin JA, Loh L, Lenrow DA et al. Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age. J Clin Endocrinol Metab 1999; 84: 2647-2653.
32. Page ST, Amory JK, Bowman FD, Anawalt BD, Matsumoto AM, Bremner WJ et al. Exogenous testosterone (T) alone or with finasteride increases physical performance, grip strength, and lean body mass in older men with low serum T. J Clin Endocrinol Metab 2005; 90: 1502-1510.
33. Schroeder ET, Zheng L, Yarasheski KE, Qian D, Stewart Y, Flores C et al. Treatment with oxandrolone and the durability of effects in older men. J Appl Physiol 2004; 96: 1055-1062.
34. Schroeder ET, Singh A, Bhasin S, Storer TW, Azen C, Davidson T et al. Effects of an oral androgen on muscle and metabolism in older, community-dwelling men. Am J Physiol Endocrinol Metab 2003; 284: E120-E128.
35. Ferrando AA, Sheffield-Moore M, Yeckel CW, Gilkison C, Jiang J, Achacosa A et al. Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am J Physiol Endocrinol Metab 2002; 282: E601-E607.
36. Bhasin S, Woodhouse L, Casaburi R, Singh AB, Mac RP, Lee M et al. Older men are as responsive as young men to the anabolic effects of graded doses of testosterone on the skeletal muscle. J Clin Endocrinol Metab 2005; 90: 678-688.
37. Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR et al. Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol 1995; 269(5 Part 1): E820-E826.
38. Clague JE, Wu FC, Horan MA. Difficulties in measuring the effect of testosterone replacement therapy on muscle function in older men. Int J Androl 1999; 22: 261-265.
39. Kenny AM, Prestwood KM, Gruman CA, Marcello KM, Raisz LG. Effects of transdermal testosterone on bone and muscle in older men with low bioavailable testosterone levels. J Gerontol A Biol Sci Med Sci 2001; 56: M266-M272.
40. Sih R, Morley JE, Kaiser FE, Perry III HM, Patrick P, Ross C. Testosterone replacement in older hypogonadal men: a 12-month randomized controlled trial. J Clin Endocrinol Metab 1997; 82: 1661-1667.
41. Wang C, Eyre DR, Clark R, Kleinberg D, Newman C, Iranmanesh A et al. Sublingual testosterone replacement improves muscle mass and strength, decreases bone resorption, and increases bone formation markers in hypogonadal men - a clinical research center study. J Clin Endocrinol Metab 1996; 81: 3654-3662.
42. Ly LP, Jimenez M, Zhuang TN, Celermajer DS, Conway AJ, Handelsman DJ. A double-blind, placebo-controlled, randomized clinical trial of transdermal dihydrotestosterone gel on muscular strength, mobility, and quality of life in older men with partial androgen deficiency. J Clin Endocrinol Metab 2001; 86: 4078-4088.
43. Liu PY, Wishart SM, Handelsman DJ. A double-blind, placebo-controlled, randomized clinical trial of recombinant human chorionic gonadotropin on muscle strength and physical function and activity in older men with partial age-related androgen deficiency. J Clin Endocrinol Metab 2002; 87: 3125-3135.
44. Wang C, Swedloff RS, Iranmanesh A, Dobs A, Snyder PJ, Cunningham G et al. Transdermal testosterone gel improves sexual function, mood, muscle strength, and body composition parameters in hypogonadal men. Testosterone Gel Study Group. J Clin Endocrinol Metab 2000; 85: 2839-2853.
45. Katznelson L, Rosenthal DI, Rosol MS, Anderson EJ, Hayden DL, Schoenfeld DA et al. Using quantitative CT to assess adipose distribution in adult men with acquired hypogonadism. AJR Am J Roentgenol 1998; 170: 423-427.
46. Woodhouse LJ, Gupta N, Bhasin M, Singh AB, Ross R, Phillips J et al. Dose-dependent effects of testosterone on regional adipose tissue distribution in healthy young men. J Clin Endocrinol Metab 2004; 89: 718-726.
47. Seidell JC, Bjorntorp P, Sjostrom L, Kvist H, Sannerstedt R. Visceral fat accumulation in men is positively associated with insulin, glucose, and C-peptide levels, but negatively with testosterone levels. Metabolism 1990; 39: 897-901.
48. Blackman MR, Sorkin JD, Munzer T, Bellantoni MF, Busby-Whitehead J, Stevens TE et al. Growth hormone and sex steroid administration in healthy aged women and men: a randomized controlled trial. Jama 2002; 288: 2282-2292.
49. Wittert GA, Chapman IM, Haren MT, Mackintosh S, Coates P, Morley JE. Oral testosterone supplementation increases muscle and decreases fat mass in healthy elderly males with low-normal gonadal status. J Gerontol A Biol Sci Med Sci 2003; 58: 618-625.
50. Steidle C, Schwartz S, Jacoby K, Sebree T, Smith T, Bachand R. AA2500 testosterone gel normalizes androgen levels in aging males with improvements in body composition and sexual function. J Clin Endocrinol Metab 2003; 88: 2673-2681.
51. Schroeder ET, Zheng L, Ong MD, Martinez C, Flores C, Stewart Y et al. Effects of androgen therapy on adipose tissue and metabolism in older men. J Clin Endocrinol Metab 2004; 89: 4863-4872.
52. Marin P, Holmang S, Jonsson L, Sjostrom L, Kvist H, Holm G et al. The effects of testosterone treatment on body composition and metabolism in middle-aged obese men. Int J Obes Relat Metab Disord 1992; 16: 991-997.
53. Marin P, Holmang S, Gustafsson C, Jonsson L, Kvist H, Elander A et al. Androgen treatment of abdominally obese men. Obes Res 1993; 1: 245-251.
54. Marin P. Testosterone and regional fat distribution. Obes Res 1995; 3(Suppl 4): 609S-612S.
55. Lovejoy JC, Bray GA, Greeson CS, Klemperer M, Morris J, Partington C et al. Oral anabolic steroid treatment, but not parenteral androgen treatment, decreases abdominal fat in obese, older men. Int J Obes Relat Metab Disord 1995; 19: 614-624.
56. Munzer T, Harman SM, Hees P, Shapiro E, Christmas C, Bellantoni MF et al. Effects of GH and/or sex steroid administration on abdominal subcutaneous and visceral fat in healthy aged women and men. J Clin Endocrinol Metab 2001; 86: 3604-3610.
57. Nair KS, Rizza RA, O'Brien P, Dhatariya K, Short KR, Nehra A et al. DHEA in elderly women and DHEA or testosterone in elderly men. N Engl J Med 2006; 355: 1647-1659.
58. Villareal DT, Holloszy JO. Effect of DHEA on abdominal fat and insulin action in elderly women and men: a randomized controlled trial. JAMA 2004; 292: 2243-2248.
59. Ferrannini E. Metabolic syndrome: a solution in search of a problem. J Clin Endocrinol Metab 2007; 92: 396-398.
60. Grundy SM. Metabolic syndrome: a multiplex cardiovascular risk factor. J Clin Endocrinol Metab 2007; 92: 399-404.
61. Grundy SM, Brewer Jr HB, Cleeman JI, Smith Jr SC, Lenfant C. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109: 433-438.
62. Alberti KG, Zimmet P, Shaw J. The metabolic syndrome - a new worldwide definition. Lancet 2005; 366: 1059-1062.
63. Simon D, Charles MA, Nahoul K, Orssaud G, Kremski J, Hully V et al. Association between plasma total testosterone and cardiovascular risk factors in healthy adult men: The Telecom Study. J Clin Endocrinol Metab 1997; 82: 682-685.
64. Phillips GB, Jing TY, Resnick LM, Barbagallo M, Laragh JH, Sealey JE. Sex hormones and hemostatic risk factors for coronary heart disease in men with hypertension. J Hypertens 1993; 11: 699-702.
65. Barrett-Connor E. Lower endogenous androgen levels and dyslipidemia in men with non-insulin-dependent diabetes mellitus. Ann Intern Med 1992; 117: 807-811.
66. Haffner SM, Valdez RA, Stern MP, Katz MS. Obesity, body fat distribution and sex hormones in men. Int J Obes Relat Metab Disord 1993; 17: 643-649.
67. Barrett-Connor EL. Testosterone and risk factors for cardiovascular disease in men. Diabete Metab 1995; 21: 156-161.
68. Gyllenborg J, Rasmussen SL, Borch-Johnsen K, Heitmann BL, Skakkebaek NE, Juul A. Cardiovascular risk factors in men: the role of gonadal steroids and sex hormone-binding globulin. Metabolism 2001; 50: 882-888.
69. Muller M, van der Schouw YT, Thijssen JH, Grobbee DE. Endogenous sex hormones and cardiovascular disease in men. J Clin Endocrinol Metab 2003; 88: 5076-5086.
70. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992; 340: 1111-1115.
71. Anderson TJ, Uehata A, Gerhard MD, Meredith IT, Knab S, Delagrange D et al. Close relation of endothelial function in the human coronary and peripheral circulations. J Am Coll Cardiol 1995; 26: 1235-1241.
72. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 1994; 24: 471-476.
73. Liu PY, Death AK, Handelsman DJ. Androgens and cardiovascular disease. Endocr Rev 2003; 24: 313-340.
74. Ong PJ, Patrizi G, Chong WC, Webb CM, Hayward CS, Collins P. Testosterone enhances flow-mediated brachial artery reactivity in men with coronary artery disease. Am J Cardiol 2000; 85: 269-272.
75. Webb CM, McNeill JG, Hayward CS, de Zeigler D, Collins P. Effects of testosterone on coronary vasomotor regulation in men with coronary heart disease. Circulation 1999; 100: 1690-1696.
76. Liu PY, Wishart SM, Celermajer DS, Jimenez M, Pierro ID, Conway AJ et al. Do reproductive hormones modify insulin sensitivity and metabolism in older men? A randomized, placebo-controlled clinical trial of recombinant human chorionic gonadotropin. Eur J Endocrinol 2003; 148: 55-66.
77. Kenny AM, Prestwood KM, Gruman CA, Fabregas G, Biskup B, Mansoor G. Effects of transdermal testosterone on lipids and vascular reactivity in older men with low bioavailable testosterone levels. J Gerontol A Biol Sci Med Sci 2002; 57: M460-M465.
78. Jones RD, Hugh Jones T, Channer KS. The influence of testosterone upon vascular reactivity. Eur J Endocrinol 2004; 151: 29-37.
79. Herman SM, Robinson JT, McCredie RJ, Adams MR, Boyer MJ, Celermajer DS. Androgen deprivation is associated with enhanced endothelium-dependent dilatation in adult men. Arterioscler Thromb Vasc Biol 1997; 17: 2004-2009.
80. Sader MA, Griffiths KA, Skilton MR, Wishart SM, Handelsman DJ, Celermajer DS. Physiological testosterone replacement and arterial endothelial function inmen. Clin Endocrinol (Oxf) 2003; 59: 62-67.
81. Zitzmann M, Brune M, Nieschlag E. Vascular reactivity in hypogonadal men is reduced by androgen substitution. J Clin Endocrinol Metab 2002; 87: 5030-5037.
82. Tenover JL. Experience with testosterone replacement in the elderly. Mayo Clin Proc 2000; 75(Suppl): S77-S81, discussion S82.
83. Schleich F, Legros JJ. Effects of androgen substitution on lipid profile in the adult and aging hypogonadal male. Eur J Endocrinol 2004; 151: 415-424.
84. Whitsel EA, Boyko EJ, Matsumoto AM, Anawalt BD, Siscovick DS. Intramuscular testosterone esters and plasma lipids in hypogonadalmen: a meta-analysis. Am J Med 2001; 111: 261-269.
85. Wu FC, Von Eckardstein A. Androgens and coronary artery disease. Endocr Rev 2003; 24: 183-217.
86. Allan CA, McLachlan RI. Age-related changes in testosterone and the role of replacement therapy in older men. Clin Endocrinol (Oxf) 2004; 60: 653-670.
87. Haffner SM, Shaten J, Stern MP, Smith GD, Kuller L. Low levels of sex hormone-binding globulin and testosterone predict the development of non-insulin-dependent diabetes mellitus in men. MRFIT Research Group. Multiple Risk Factor Intervention Trial. Am J Epidemiol 1996; 143: 889-897.
88. Kapoor D, Malkin CJ, Channer KS, Jones TH. Androgens, insulin resistance and vascular disease in men. Clin Endocrinol (Oxf) 2005; 63: 239-250.
89. Liu PY, Swerdloff RS, Veldhuis JD. Clinical review 171: the rationale, efficacy and safety of androgen therapy in older men: future research and current practice recommendations. J Clin Endocrinol Metab 2004; 89: 4789-4796.
90. Singh AB, Hsia S, Alaupovic P, Sinha-Hikim I, Woodhouse L, Buchanan TA et al. The effects of varying doses of Ton insulin sensitivity, plasma lipids, apolipoproteins, and C-reactive protein in healthy young men. J Clin Endocrinol Metab 2002; 87: 136-143.
91. Allan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI. The association between obesity and the diagnosis of androgen deficiency in symptomatic ageing men. Med J Aust 2006; 185: 424-427.
92. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA 2002; 288: 1723-1727.
93. Jousilahti P, Tuomilehto J, Vartiainen E, Pekkanen J, Puska P. Body weight, cardiovascular risk factors, and coronary mortality. 15-year follow-up of middle-aged men and women in eastern Finland. Circulation 1996; 93: 1372-1379.
94. Visscher TL, Seidell JC, Menotti A, Blackburn H, Nissinen A, Feskens EJ et al. Underweight and overweight in relation to mortality among men aged 40-59 and 50-69 years: the Seven Countries Study. Am J Epidemiol 2000; 151: 660-666.
95. Tenover JS. Effects of testosterone supplementation in the aging male. J Clin Endocrinol Metab 1992; 75: 1092-1098.
96. Giannoulis MG, Sonksen PH, Umpleby M, Breen L, Pentecost C, Whyte M et al. The effects of growth hormone and/or testosterone in healthy elderly men: a randomized controlled trial. J Clin Endocrinol Metab 2006; 91: 477-484.
97. Simon D, Charles MA, Lahlou N, Nahoul K, Oppert JM, Gouault-Heilmann M et al. Androgen therapy improves insulin sensitivity and decresses leptin level in healthy adult men with low plasma total testosterone: a 3-month randomized placebo-controlled trial. Diabetes Care 2001; 24: 2149-2151.
98. Snyder PJ, Peachey H, Berlin JA, Rader D, Usher D, Loh L et al. Effect of transdermal testosterone treatment on serum lipid and apolipoprotein levels in men more than 65 years of age. AM J Med 2001; 111: 255-260.