Lifestyle factors and serum androgens among 636 middle aged men from seven countries in the European Prospective Investigation into Cancer and Nutrition (EPIC).
Suzuki, Reiko; Allen, Naomi E.; Appleby, Paul N.et al.
2009 • In Cancer Causes and Control, 20 (6), p. 811-21
Age Factors; Alcoholic Beverages/adverse effects; Androgens/blood; Androstane-3,17-diol/analogs & derivatives/blood; Androstenedione/blood; Body Weight; Cross-Sectional Studies; Europe/epidemiology; Humans; Life Style; Male; Middle Aged; Multicenter Studies as Topic; Neoplasms/blood/epidemiology; Nutritional Status; Prospective Studies; Questionnaires; Sex Hormone-Binding Globulin/metabolism; Smoking/adverse effects; Testosterone/blood/metabolism
Abstract :
[en] OBJECTIVE: To evaluate the association between lifestyle and dietary factors and serum concentrations of androgens in middle-aged healthy men. METHODS: We conducted a cross-sectional analysis of the association of lifestyle factors with circulating concentrations of androstenedione (A-dione), 3-alpha-androstanediol glucuronide (A-diol-g), testosterone (T), SHBG (sex hormone-binding globulin), and free testosterone (FT) among 636 men in the European Prospective Investigation into Cancer and Nutrition. RESULTS: Compared with the youngest age group (40-49 years), the oldest (70-79 years) had a higher mean concentration of SHBG (by 44%) and lower mean concentrations of A-diol-g (by 29%) FT (19%). Men in the highest BMI group (> or =29.83 kg/m(2)) had a higher mean A-diol-g concentration (by 38%) and lower mean concentration of T (by 20%) SHBG (29%) compared with the lowest (<24.16 kg/m(2)). Current smokers had higher mean concentrations of T (by 13%), SHBG (14%), and A-dione (15%) compared with never smokers. Physical activity and dietary factors were not associated with androgen concentrations, although men in the highest fifth of alcohol intake had higher mean concentrations of A-dione (by 9%), FT (11%) compared with the lowest. CONCLUSION: Our results suggest that age, body weight, smoking, and alcohol intake are associated with circulating androgen concentrations in men.
Disciplines :
Human health sciences: Multidisciplinary, general & others
Author, co-author :
Suzuki, Reiko
Allen, Naomi E.
Appleby, Paul N.
Key, Timothy J.
Dossus, Laure
Tjonneland, Anne
Fons Johnsen, Nina
Overvad, Kim
Sacerdote, Carlotta
Palli, Domenico
Krogh, Vittorio
Tumino, Rosario
Rohrmann, Sabine
Linseisen, Jakob
Boeing, Heiner
Trichopoulou, Antonia
Makrygiannis, Georgios ; Université de Liège - ULiège > Département des sciences cliniques > Chirurgie cardio-vasculaire et thoracique
Lifestyle factors and serum androgens among 636 middle aged men from seven countries in the European Prospective Investigation into Cancer and Nutrition (EPIC).
NE Allen PN Appleby GK Davey, et al. 2002 Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men Cancer Causes Control 13 353 363 10.1023/A:1015238102830 12074505 10.1023/A:1015238102830 (Pubitemid 34553516)
KT Khaw M Dowsett E Folkerd, et al. 2007 Endogenous testosterone and mortality due to all causes, cardiovascular disease, and cancer in men: European prospective investigation into cancer in Norfolk (EPIC-Norfolk) Prospective Population Study Circulation 116 2694 2701 10.1161/CIRCULATIONAHA.107.719005 18040028 10.1161/CIRCULATIONAHA.107.719005 1:CAS:528:DC%2BD2sXhtlGns7nO (Pubitemid 350291241)
E Selvin M Feinleib L Zhang, et al. 2007 Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III) Diabetes Care 30 234 238 10.2337/dc06-1579 17259487 10.2337/dc06-1579 1:CAS:528:DC%2BD2sXitlaju7o%3D (Pubitemid 46198324)
NO Kuchuk NM van Schoor SM Pluijm, et al. 2007 The association of sex hormone levels with quantitative ultrasound, bone mineral density, bone turnover and osteoporotic fractures in older men and women Clin Endocrinol (Oxf) 67 295 303 10.1111/j.1365-2265.2007.02882.x 10.1111/j.1365-2265.2007.02882.x 1:CAS:528:DC%2BD2sXpslOnsrY%3D (Pubitemid 47076310)
HL Stanley BP Schmitt RM Poses, et al. 1991 Does hypogonadism contribute to the occurrence of a minimal trauma hip fracture in elderly men? J Am Geriatr Soc 39 766 771 2071807 1:STN:280:DyaK3Mzgt1KksA%3D%3D
EA Platz E Giovannucci 2004 The epidemiology of sex steroid hormones and their signaling and metabolic pathways in the etiology of prostate cancer J Steroid Biochem Mol Biol 92 237 253 10.1016/j.jsbmb.2004.10.002 15663987 10.1016/j.jsbmb.2004.10.002 1:CAS:528:DC%2BD2MXkvVSitw%3D%3D (Pubitemid 40128245)
AW Roddam NE Allen P Appleby, et al. 2008 Endogenous sex hormones and prostate cancer: a collaborative analysis of 18 prospective studies J Natl Cancer Inst 100 170 183 10.1093/jnci/djm323 18230794 10.1093/jnci/djm323 1:CAS:528:DC%2BD1cXivFygsrg%3D
AW Hsing JK Reichardt FZ Stanczyk 2002 Hormones and prostate cancer: current perspectives and future directions Prostate 52 213 235 10.1002/pros.10108 12111697 10.1002/pros.10108 1:CAS:528:DC%2BD38XmsVWqtbk%3D (Pubitemid 34791223)
E Riboli KJ Hunt N Slimani, et al. 2002 European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection Public Health Nutr 5 1113 1124 10.1079/PHN2002394 12639222 10.1079/PHN2002394 1:STN:280:DC%2BD3s7is1Ohsw%3D%3D (Pubitemid 36313608)
PH Lahmann C Friedenreich AJ Schuit, et al. 2007 Physical activity and breast cancer risk: the European Prospective Investigation into Cancer and Nutrition Cancer Epidemiol Biomarkers Prev 16 36 42 10.1158/1055-9965.EPI-06- 0582 17179488 10.1158/1055-9965.EPI-06-0582 (Pubitemid 46174261)
RC Travis TJ Key NE Allen, et al. 2007 Serum androgens and prostate cancer among 643 cases and 643 controls in the European Prospective Investigation into Cancer and Nutrition Int J Cancer 121 1331 1338 10.1002/ijc.22814 17514649 10.1002/ijc.22814 1:CAS:528:DC%2BD2sXhtVSmtL%2FO (Pubitemid 47293802)
A Vermeulen L Verdonck JM Kaufman 1999 A critical evaluation of simple methods for the estimation of free testosterone in serum J Clin Endocrinol Metab 84 3666 3672 10.1210/jc.84.10.3666 10523012 10.1210/jc.84.10.3666 1:CAS:528:DyaK1MXms1Ohtbs%3D
S Rinaldi A Geay H Dechaud, et al. 2002 Validity of free testosterone and free estradiol determinations in serum samples from postmenopausal women by theoretical calculations Cancer Epidemiol Biomarkers Prev 11 1065 1071 12376508 1:CAS:528:DC%2BD38Xos1ekurs%3D
W Willett MJ Stampfer 1986 Total energy intake: implications for epidemiologic analyses Am J Epidemiol 124 17 27 3521261 1:STN:280: DyaL283jvFWruw%3D%3D
V Kipnis LS Freedman CC Brown, et al. 1993 Interpretation of energy adjustment models for nutritional epidemiology Am J Epidemiol 137 1376 1380 8333419 1:STN:280:DyaK3szisFGlug%3D%3D
SM Harman EJ Metter JD Tobin, et al. 2001 Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging J Clin Endocrinol Metab 86 724 731 10.1210/jc.86.2.724 11158037 10.1210/jc.86.2.724 1:CAS:528:DC%2BD3MXht1Knt7k%3D (Pubitemid 32207487)
M Muller I den Tonkelaar JH Thijssen, et al. 2003 Endogenous sex hormones in men aged 40-80 years Eur J Endocrinol 149 583 589 10.1530/eje.0.1490583 14641001 10.1530/eje.0.1490583 1:CAS:528:DC%2BD2cXhtVeitQ%3D%3D (Pubitemid 38054704)
A Gray HA Feldman JB McKinlay, et al. 1991 Age, disease, and changing sex hormone levels in middle-aged men: results of the Massachusetts Male Aging Study J Clin Endocrinol Metab 73 1016 1025 1719016 1:CAS:528: DyaK38Xlt1SmtA%3D%3D
J Svartberg M Midtby KH Bonaa, et al. 2003 The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromso Study Eur J Endocrinol 149 145 152 10.1530/eje.0.1490145 12887292 10.1530/eje.0.1490145 1:CAS:528:DC%2BD3sXms1Whu7s%3D (Pubitemid 36987157)
HA Feldman C Longcope CA Derby, et al. 2002 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 87 589 598 10.1210/jc.87.2.589 11836290 10.1210/jc.87.2.589 1:CAS:528:DC%2BD38XhsVSjurc%3D (Pubitemid 34158223)
O Ukkola J Gagnon T Rankinen, et al. 2001 Age, body mass index, race and other determinants of steroid hormone variability: the HERITAGE Family Study Eur J Endocrinol 145 1 9 10.1530/eje.0.1450001 11415846 10.1530/eje.0.1450001 1:CAS:528:DC%2BD3MXlt1Ghu7Y%3D
AH Wu AS Whittemore LN Kolonel, et al. 2001 Lifestyle determinants of 5alpha-reductase metabolites in older African-American, white, and Asian-American men Cancer Epidemiol Biomarkers Prev 10 533 538 11352865 1:CAS:528:DC%2BD3MXktlCksr8%3D
D Sparrow R Bosse JW Rowe 1980 The influence of age, alcohol consumption, and body build on gonadal function in men J Clin Endocrinol Metab 51 508 512 6773977 1:CAS:528:DyaL3cXlvVelsLc%3D
T Mulligan A Iranmanesh S Gheorghiu, et al. 1995 Amplified nocturnal luteinizing hormone (LH) secretory burst frequency with selective attenuation of pulsatile (but not basal) testosterone secretion in healthy aged men: possible Leydig cell desensitization to endogenous LH signaling-a clinical research center study J Clin Endocrinol Metab 80 3025 3031 10.1210/jc.80.10.3025 7559891 10.1210/jc.80.10.3025 1:CAS:528:DyaK2MXoslCnsbs%3D
JD Veldhuis RJ Urban G Lizarralde, et al. 1992 Attenuation of luteinizing hormone secretory burst amplitude as a proximate basis for the hypoandrogenism of healthy aging in men J Clin Endocrinol Metab 75 707 713 10.1210/jc.75.3.707 1517359 10.1210/jc.75.3.707 1:CAS:528:DyaK3sXpsVKgsw%3D%3D
T Mulligan A Iranmanesh ML Johnson, et al. 1997 Aging alters feed-forward and feedback linkages between LH and testosterone in healthy men Am J Physiol 273 R1407 R1413 9362306 1:CAS:528:DyaK2sXnt1WisrY%3D
P Lecomte N Lecureuil M Lecureuil, et al. 1998 Sex differences in the control of sex-hormone-binding globulin in the elderly: role of insulin-like growth factor-I and insulin Eur J Endocrinol 139 178 183 10.1530/eje.0.1390178 9724073 10.1530/eje.0.1390178 1:CAS:528:DyaK1cXlsV2isbo%3D
A Singh D Hamilton-Fairley R Koistinen, et al. 1990 Effect of insulin-like growth factor-type I (IGF-I) and insulin on the secretion of sex hormone binding globulin and IGF-I binding protein (IBP-I) by human hepatoma cells J Endocrinol 124 R1 R3 10.1677/joe.0.124R001 1690256 10.1677/joe.0.124R001 1:CAS:528:DyaK3cXpt1Giug%3D%3D
R Kaaks A Lukanova B Sommersberg 2000 Plasma androgens, IGF-1, body size, and prostate cancer risk: a synthetic review Prostate Cancer Prostatic Dis 3 157 172 10.1038/sj.pcan.4500421 12497092 10.1038/sj.pcan.4500421 1:CAS:528:DC%2BD3MXhtFKrsw%3D%3D
G Schneider MA Kirschner R Berkowitz, et al. 1979 Increased estrogen production in obese men J Clin Endocrinol Metab 48 633 638 429508 1:STN:280:DyaE1M7ltFersw%3D%3D
A Tchernof JP Despres A Belanger, et al. 1995 Reduced testosterone and adrenal C19 steroid levels in obese men Metabolism 44 513 519 10.1016/0026-0495(95)90060-8 7723675 10.1016/0026-0495(95)90060-8 1:CAS:528:DyaK2MXltVersrg%3D
AH Wu AS Whittemore LN Kolonel, et al. 1995 Serum androgens and sex hormone-binding globulins in relation to lifestyle factors in older African-American, white, and Asian men in the United States and Canada Cancer Epidemiol Biomarkers Prev 4 735 741 8672990 1:CAS:528:DyaK2MXpslWnt74%3D
C Couillard J Gagnon J Bergeron, et al. 2000 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 85 1026 1031 10.1210/jc.85.3.1026 10720034 10.1210/jc.85.3.1026 1:CAS:528: DC%2BD3cXisFOrurs%3D (Pubitemid 32269344)
MA Joseph JT Wei SD Harlow, et al. 2002 Relationship of serum sex-steroid hormones and prostate volume in African American men Prostate 53 322 329 10.1002/pros.10154 12430143 10.1002/pros.10154 1:CAS:528:DC%2BD38Xps1ymt7c%3D (Pubitemid 35398502)
CA Derby S Zilber D Brambilla, et al. 2006 Body mass index, waist circumference and waist to hip ratio and change in sex steroid hormones: the Massachusetts Male Ageing Study Clin Endocrinol (Oxf) 65 125 131 10.1111/j.1365-2265.2006.02560.x 10.1111/j.1365-2265.2006.02560.x 1:CAS:528:DC%2BD28XotFKmsLo%3D (Pubitemid 43911690)
AE Field GA Colditz WC Willett, et al. 1994 The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle-aged men J Clin Endocrinol Metab 79 1310 1316 10.1210/jc.79.5.1310 7962322 10.1210/jc.79.5.1310 1:CAS:528: DyaK2MXit1eksL8%3D (Pubitemid 24369840)
C Longcope HA Feldman JB McKinlay, et al. 2000 Diet and sex hormone-binding globulin J Clin Endocrinol Metab 85 293 296 10.1210/jc.85.1.293 10634401 10.1210/jc.85.1.293 1:CAS:528:DC%2BD3cXjtl2mtg%3D%3D (Pubitemid 32268828)
A Vermeulen JM Kaufman JP Deslypere, et al. 1993 Attenuated luteinizing hormone (LH) pulse amplitude but normal LH pulse frequency, and its relation to plasma androgens in hypogonadism of obese men J Clin Endocrinol Metab 76 1140 1146 10.1210/jc.76.5.1140 8496304 10.1210/jc.76.5.1140 1:STN:280: DyaK3s3ms1Onsw%3D%3D (Pubitemid 23155426)
R Horton D Hawks R Lobo 1982 3 alpha, 17 beta-androstanediol glucuronide in plasma. A marker of androgen action in idiopathic hirsutism J Clin Invest 69 1203 1206 10.1172/JCI110558 7068855 10.1172/JCI110558 1:STN:280: DyaL387mvVSqsw%3D%3D
R Horton 1992 Dihydrotestosterone is a peripheral paracrine hormone J Androl 13 23 27 1551803 1:CAS:528:DyaK38XisVyntrY%3D
A Tchernof F Labrie A Belanger, et al. 1997 Androstane-3alpha, 17beta-diol glucuronide as a steroid correlate of visceral obesity in men J Clin Endocrinol Metab 82 1528 1534 10.1210/jc.82.5.1528 9141545 10.1210/jc.82.5.1528 1:CAS:528:DyaK2sXjtVGlsr8%3D
VA Giagulli R Giorgino A Vermeulen 1993 Origin and significance of plasma androsterone glucuronide levels: a parameter of adrenal androgen secretion and hepatic 5 alpha-reductase activity J Clin Endocrinol Metab 76 918 923 10.1210/jc.76.4.918 8473406 10.1210/jc.76.4.918 1:CAS:528:DyaK3sXksVWhsbc%3D (Pubitemid 23110838)
WS Dai JP Gutai LH Kuller, et al. 1988 Cigarette smoking and serum sex hormones in men Am J Epidemiol 128 796 805 3421245 1:STN:280: DyaL1czjvVKjsg%3D%3D
A Hautanen M Manttari M Kupari, et al. 1993 Cigarette smoking is associated with elevated adrenal androgen response to adrenocorticotropin J Steroid Biochem Mol Biol 46 245 251 10.1016/0960-0760(93)90300-L 8664173 10.1016/0960-0760(93)90300-L 1:CAS:528:DyaK3sXmtF2mtr8%3D (Pubitemid 23251683)
VH Goh TY Tong HP Mok, et al. 2007 Interactions among age, adiposity, bodyweight, lifestyle factors and sex steroid hormones in healthy Singaporean Chinese men Asian J Androl 9 611 621 10.1111/j.1745-7262.2007.00322.x 17712478 10.1111/j.1745-7262.2007.00322.x 1:CAS:528:DC%2BD2sXhtFaksb7N (Pubitemid 47354663)
KM English PJ Pugh H Parry, et al. 2001 Effect of cigarette smoking on levels of bioavailable testosterone in healthy men Clin Sci (Lond) 100 661 665 10.1042/CS20010011 1:CAS:528:DC%2BD3MXltV2isr4%3D (Pubitemid 32523320)
B Isik A Ceylan R Isik 2007 Oxidative stress in smokers and non-smokers Inhal Toxicol 19 767 769 10.1080/08958370701401418 17613085 10.1080/ 08958370701401418 1:CAS:528:DC%2BD2sXnt1Sis74%3D (Pubitemid 47026974)
WS Dai LH Kuller RE LaPorte, et al. 1981 The epidemiology of plasma testosterone levels in middle-aged men Am J Epidemiol 114 804 816 7315829 1:STN:280:DyaL38%2FovVGqtQ%3D%3D
CS Mantzoros EI Georgiadis 1995 Body mass and physical activity are important predictors of serum androgen concentrations in young healthy men Epidemiology 6 432 435 10.1097/00001648-199507000-00020 7548356 10.1097/00001648-199507000-00020 1:STN:280:DyaK28%2FjvF2qtg%3D%3D
LJ White RH Dressendorfer MA Ferguson, et al. 2002 Maintenance of testosterone status in fitness joggers after increased training mileage Eur J Appl Physiol 86 498 502 10.1007/s00421-001-0575-z 11944097 10.1007/s00421-001- 0575-z 1:CAS:528:DC%2BD38XisFartb4%3D (Pubitemid 41399044)
HL Hall MG Flynn KK Carroll, et al. 1999 Effects of intensified training and detraining on testicular function Clin J Sport Med 9 203 208 10.1097/00042752-199910000-00004 10593214 10.1097/00042752-199910000-00004 1:STN:280:DC%2BD3c%2FlvVOrtQ%3D%3D
VN Hawkins K Foster-Schubert J Chubak, et al. 2008 Effect of exercise on serum sex hormones in men: a 12-month randomized clinical trial Med Sci Sports Exerc 40 223 233 10.1249/01.mss.0000321026.68454.ad 18202581 10.1249/mss.0b013e31815bbba9 1:CAS:528:DC%2BD1cXotlWltw%3D%3D
CJ Eriksson T Fukunaga R Lindman 1994 Sex hormone response to alcohol Nature 369 711 10.1038/369711a0 8008063 10.1038/369711a0 1:CAS:528: DyaK2cXkslGqtbo%3D (Pubitemid 24225357)
JH Mendelson NK Mello J Ellingboe 1977 Effects of acute alcohol intake on pituitary-gonadal hormones in normal human males J Pharmacol Exp Ther 202 676 682 894528 1:CAS:528:DyaE2sXls1amtrY%3D
A Sierksma T Sarkola CJ Eriksson, et al. 2004 Effect of moderate alcohol consumption on plasma dehydroepiandrosterone sulfate, testosterone, and estradiol levels in middle-aged men and postmenopausal women: a diet-controlled intervention study Alcohol Clin Exp Res 28 780 785 10.1097/01.ALC.0000125356. 70824.81 15166654 10.1097/01.ALC.0000125356.70824.81 1:CAS:528: DC%2BD2cXksVKhu7w%3D (Pubitemid 38661376)
TJ Key L Roe M Thorogood, et al. 1990 Testosterone, sex hormone-binding globulin, calculated free testosterone, and oestradiol in male vegans and omnivores Br J Nutr 64 111 119 10.1079/BJN19900014 2400756 10.1079/BJN19900014 1:CAS:528:DyaK3cXkslWmsr0%3D (Pubitemid 20261540)
C Wang DH Catlin B Starcevic, et al. 2005 Low-fat high-fiber diet decreased serum and urine androgens in men J Clin Endocrinol Metab 90 3550 3559 10.1210/jc.2004-1530 15741266 10.1210/jc.2004-1530 1:CAS:528: DC%2BD2MXkvFCltbw%3D (Pubitemid 41014326)
